Skip to main content
SpringerLink
Log in
Book cover

Emerging Trends in Cell and Gene Therapy pp 637–695Cite as

Cell and Gene Transfer Strategies for Vascularization During Skin Wound Healing

  • Chapter
  • First Online:

Abstract

Adequate vascularization is pivotal to skin wound healing. Therefore, designing efficient revascularization strategies based on the mechanisms behind electromechanical stimulation of wound vascularization would be beneficial to the growing number of patients in need of improved wound healing. Recent attention has centered on applying gene/protein transfer and cell differentiation/transplantation approaches to stimulate and mimic the molecular events occurring during wound revascularization. Although both gene/protein transfer and cell differentiation/transplantation are faced with important challenges, researchers have made tremendous advances and shown both strategies to be a promising approach. In this chapter, we give an overview of the myriad of molecular players involved in neovascularization. We also discuss the molecular mechanisms of neovascularization during wound healing and provide an in-depth review on neovascular strategies and techniques for wound healing and tissue-engineered skin equivalents.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  1. Bender AE, Bender DA (1995) A dictionary of food and nutrition. Oxford University Press, New York

    Google Scholar 

  2. Braverman IM (2000) The cutaneous microcirculation. J Investig Dermatol Symp Proc 5:3–9

    Article  PubMed  CAS  Google Scholar 

  3. Li L et al (2006) Age-related changes of the cutaneous microcirculation in vivo. Gerontology 52:142–153

    Article  PubMed  Google Scholar 

  4. Alitalo K, Tammela T, Petrova TV (2005) Lymphangiogenesis in development and human disease. Nature 438:946–953

    Article  PubMed  CAS  Google Scholar 

  5. Gurtner GC, Werner S, Barrandon Y, Longaker MT (2008) Wound repair and regeneration. Nature 453:314–321

    Article  PubMed  CAS  Google Scholar 

  6. Shaw TJ, Martin P (2009) Wound repair at a glance. J Cell Sci 122:3209–3213

    Article  PubMed  CAS  Google Scholar 

  7. Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M (2008) Growth factors and cytokines in wound healing. Wound Repair Regen 16:585–601

    Article  PubMed  Google Scholar 

  8. Rhett JM et al (2008) Novel therapies for scar reduction and regenerative healing of skin wounds. Trends Biotechnol 26:173–180

    Article  PubMed  CAS  Google Scholar 

  9. Kose O, Waseem A (2008) Keloids and hypertrophic scars: are they two different sides of the same coin? Dermatol Surg 34:336–346

    Article  PubMed  CAS  Google Scholar 

  10. van der Veer WM et al (2011) Time course of the angiogenic response during normotrophic and hypertrophic scar formation in humans. Wound Repair Regen 19:292–301

    Article  PubMed  Google Scholar 

  11. Hendrickx B, Vranckx JJ, Luttun A (2011) Cell-based vascularization strategies for skin tissue engineering. Tissue Eng Part B Rev 17:13–24

    Article  PubMed  Google Scholar 

  12. Benest AV, Augustin HG (2009) Tension in the vasculature. Nat Med 15:608–610

    Article  PubMed  CAS  Google Scholar 

  13. Kilarski WW, Samolov B, Petersson L, Kvanta A, Gerwins P (2009) Biomechanical regulation of blood vessel growth during tissue vascularization. Nat Med 15:657–664

    Article  PubMed  CAS  Google Scholar 

  14. Liu L et al (2008) Age-dependent impairment of HIF-1alpha expression in diabetic mice: correction with electroporation-facilitated gene therapy increases wound healing, angiogenesis, and circulating angiogenic cells. J Cell Physiol 217:319–327

    Article  PubMed  CAS  Google Scholar 

  15. Cianfarani F et al (2006) Placenta growth factor in diabetic wound healing: altered expression and therapeutic potential. Am J Pathol 169:1167–1182

    Article  PubMed  CAS  Google Scholar 

  16. Wetterau M et al (2011) Topical prolyl hydroxylase domain-2 silencing improves diabetic murine wound closure. Wound Repair Regen 19:481–486

    Article  PubMed  Google Scholar 

  17. Mace KA, Yu DH, Paydar KZ, Boudreau N, Young DM (2007) Sustained expression of Hif-1alpha in the diabetic environment promotes angiogenesis and cutaneous wound repair. Wound Repair Regen 15:636–645

    Article  PubMed  Google Scholar 

  18. Yu DH, Mace KA, Hansen SL, Boudreau N, Young DM (2007) Effects of decreased insulin-like growth factor-1 stimulation on hypoxia inducible factor 1-alpha protein synthesis and function during cutaneous repair in diabetic mice. Wound Repair Regen 15:628–635

    Article  PubMed  Google Scholar 

  19. Niessen K et al (2011) The Notch1-Dll4 signaling pathway regulates mouse postnatal lymphatic development. Blood 118:1989–1997

    Article  PubMed  CAS  Google Scholar 

  20. Gilbertson DG et al (2001) Platelet-derived growth factor C (PDGF-C), a novel growth factor that binds to PDGF alpha and beta receptor. J Biol Chem 276:27406–27414

    Article  PubMed  CAS  Google Scholar 

  21. Henderson PW et al (2011) Stromal-derived factor-1 delivered via hydrogel drug-delivery vehicle accelerates wound healing in vivo. Wound Repair Regen 19:420–425

    Article  PubMed  Google Scholar 

  22. Kawanabe T, Kawakami T, Yatomi Y, Shimada S, Soma Y (2007) Sphingosine 1-phosphate accelerates wound healing in diabetic mice. J Dermatol Sci 48:53–60

    Article  PubMed  CAS  Google Scholar 

  23. Jin Q et al (2008) Nanofibrous scaffolds incorporating PDGF-BB microspheres induce chemokine expression and tissue neogenesis in vivo. PLoS One 3:e1729

    Article  PubMed  CAS  Google Scholar 

  24. Sun W et al (2007) Collagen membranes loaded with collagen-binding human PDGF-BB accelerate wound healing in a rabbit dermal ischemic ulcer model. Growth Factors 25:309–318

    Article  PubMed  CAS  Google Scholar 

  25. Li H et al (2008) Research of PDGF-BB gel on the wound healing of diabetic rats and its pharmacodynamics. J Surg Res 145:41–48

    Article  PubMed  CAS  Google Scholar 

  26. Steed DL (2006) Clinical evaluation of recombinant human platelet-derived growth factor for the treatment of lower extremity ulcers. Plast Reconstr Surg 117:143S–149S; discussion 150S-151S

    Article  PubMed  CAS  Google Scholar 

  27. Lee JA et al (2005) Lentiviral transfection with the PDGF-B gene improves diabetic wound healing. Plast Reconstr Surg 116:532–538

    Article  PubMed  CAS  Google Scholar 

  28. Pereira CT, Herndon DN, Rocker R, Jeschke MG (2007) Liposomal gene transfer of keratinocyte growth factor improves wound healing by altering growth factor and collagen expression. J Surg Res 139:222–228

    Article  PubMed  CAS  Google Scholar 

  29. Obara K et al (2005) Acceleration of wound healing in healing-impaired db/db mice with a photocrosslinkable chitosan hydrogel containing fibroblast growth factor-2. Wound Repair Regen 13:390–397

    Article  PubMed  Google Scholar 

  30. Obara K et al (2003) Photocrosslinkable chitosan hydrogel containing fibroblast growth factor-2 stimulates wound healing in healing-impaired db/db mice. Biomaterials 24:3437–3444

    Article  PubMed  CAS  Google Scholar 

  31. Pandit A, Ashar R, Feldman D, Thompson A (1998) Investigation of acidic fibroblast growth factor delivered through a collagen scaffold for the treatment of full-thickness skin defects in a rabbit model. Plast Reconstr Surg 101:766–775

    Article  PubMed  CAS  Google Scholar 

  32. Pandit AS, Feldman DS, Caulfield J, Thompson A (1998) Stimulation of angiogenesis by FGF-1 delivered through a modified fibrin scaffold. Growth Factors 15:113–123

    Article  PubMed  CAS  Google Scholar 

  33. Greenhalgh DG, Sprugel KH, Murray MJ, Ross R (1990) PDGF and FGF stimulate wound healing in the genetically diabetic mouse. Am J Pathol 136:1235–1246

    PubMed  CAS  Google Scholar 

  34. Badillo AT, Chung S, Zhang L, Zoltick P, Liechty KW (2007) Lentiviral gene transfer of SDF-1alpha to wounds improves diabetic wound healing. J Surg Res 143:35–42

    Article  PubMed  CAS  Google Scholar 

  35. Han G et al (2012) Nitric oxide-releasing nanoparticles accelerate wound healing by promoting fibroblast migration and collagen deposition. Am J Pathol 180:1465–1473

    Article  PubMed  CAS  Google Scholar 

  36. Luo JD et al (2009) Sonic hedgehog improves delayed wound healing via enhancing cutaneous nitric oxide function in diabetes. Am J Physiol Endocrinol Metab 297:E525–E531

    Article  PubMed  CAS  Google Scholar 

  37. Zhu H, Wei X, Bian K, Murad F (2008) Effects of nitric oxide on skin burn wound healing. J Burn Care Res 29:804–814

    Article  PubMed  Google Scholar 

  38. Bitto A et al (2008) Angiopoietin-1 gene transfer improves impaired wound healing in genetically diabetic mice without increasing VEGF expression. Clin Sci (Lond) 114(707–718)

    Google Scholar 

  39. Cho CH et al (2006) COMP-angiopoietin-1 promotes wound healing through enhanced angiogenesis, lymphangiogenesis, and blood flow in a diabetic mouse model. Proc Natl Acad Sci USA 103:4946–4951

    Article  PubMed  CAS  Google Scholar 

  40. Galeano M et al (2006) Recombinant human erythropoietin improves angiogenesis and wound healing in experimental burn wounds. Crit Care Med 34:1139–1146

    Article  PubMed  CAS  Google Scholar 

  41. Luo JD, Wang YY, Fu WL, Wu J, Chen AF (2004) Gene therapy of endothelial nitric oxide synthase and manganese superoxide dismutase restores delayed wound healing in type 1 diabetic mice. Circulation 110:2484–2493

    Article  PubMed  CAS  Google Scholar 

  42. Galeano M et al (2003) Effect of recombinant adeno-associated virus vector-mediated vascular endothelial growth factor gene transfer on wound healing after burn injury. Crit Care Med 31:1017–1025

    Article  PubMed  CAS  Google Scholar 

  43. Hamed S et al (2010) Topical erythropoietin promotes wound repair in diabetic rats. J Invest Dermatol 130:287–294

    Article  PubMed  CAS  Google Scholar 

  44. Sorg H et al (2009) Effects of erythropoietin in skin wound healing are dose related. FASEB J 23:3049–3058

    Article  PubMed  CAS  Google Scholar 

  45. Sayan H, Ozacmak VH, Guven A, Aktas RG, Ozacmak ID (2006) Erythropoietin stimulates wound healing and angiogenesis in mice. J Invest Surg 19:163–173

    Article  PubMed  Google Scholar 

  46. Galeano M et al (2004) Recombinant human erythropoietin stimulates angiogenesis and wound healing in the genetically diabetic mouse. Diabetes 53:2509–2517

    Article  PubMed  CAS  Google Scholar 

  47. Buemi M et al (2004) Recombinant human erythropoietin stimulates angiogenesis and healing of ischemic skin wounds. Shock 22:169–173

    Article  PubMed  CAS  Google Scholar 

  48. Cianfarani F et al (2006) Granulocyte/macrophage colony-stimulating factor treatment of human chronic ulcers promotes angiogenesis associated with de novo vascular endothelial growth factor transcription in the ulcer bed. Br J Dermatol 154:34–41

    Article  PubMed  CAS  Google Scholar 

  49. Jeschke MG, Schubert T, Klein D (2004) Exogenous liposomal IGF-I cDNA gene transfer leads to endogenous cellular and physiological responses in an acute wound. Am J Physiol Regul Integr Comp Physiol 286:R958–R966

    Article  PubMed  CAS  Google Scholar 

  50. Jeschke MG et al (2002) Non-viral liposomal keratinocyte growth factor (KGF) cDNA gene transfer improves dermal and epidermal regeneration through stimulation of epithelial and mesenchymal factors. Gene Ther 9:1065–1074

    Article  PubMed  CAS  Google Scholar 

  51. Lynch SE, Colvin RB, Antoniades HN (1989) Growth factors in wound healing. Single and synergistic effects on partial thickness porcine skin wounds. J Clin Invest 84:640–646

    Article  PubMed  CAS  Google Scholar 

  52. Deodato B et al (2002) Recombinant AAV vector encoding human VEGF165 enhances wound healing. Gene Ther 9:777–785

    Article  PubMed  CAS  Google Scholar 

  53. Lee PY, Chesnoy S, Huang L (2004) Electroporatic delivery of TGF-beta1 gene works synergistically with electric therapy to enhance diabetic wound healing in db/db mice. J Invest Dermatol 123:791–798

    Article  PubMed  CAS  Google Scholar 

  54. Dickens S, Vermeulen P, Hendrickx B, Van den Berge S, Vranckx JJ (2008) Regulable vascular endothelial growth factor165 overexpression by ex vivo expanded keratinocyte cultures promotes matrix formation, angiogenesis, and healing in porcine full-thickness wounds. Tissue Eng Part A 14:19–27

    Article  PubMed  CAS  Google Scholar 

  55. Gallagher KA et al (2007) Diabetic impairments in NO-mediated endothelial progenitor cell mobilization and homing are reversed by hyperoxia and SDF-1 alpha. J Clin Invest 117:1249–1259

    Article  PubMed  CAS  Google Scholar 

  56. Asai J, Takenaka H, Katoh N, Kishimoto S (2006) Dibutyryl cAMP influences endothelial progenitor cell recruitment during wound neovascularization. J Invest Dermatol 126:1159–1167

    Article  PubMed  CAS  Google Scholar 

  57. Kwon MJ et al (2012) Effective healing of diabetic skin wounds by using nonviral gene therapy based on minicircle vascular endothelial growth factor DNA and a cationic dendrimer. J Gene Med 14:272–278

    Article  PubMed  CAS  Google Scholar 

  58. Ko J et al (2011) Comparison of EGF with VEGF non-viral gene therapy for cutaneous wound healing of streptozotocin diabetic mice. Diabetes Metab J 35:226–235

    Article  PubMed  Google Scholar 

  59. Yoon CS et al (2009) Sonoporation of the minicircle-VEGF(165) for wound healing of diabetic mice. Pharm Res 26:794–801

    Article  PubMed  CAS  Google Scholar 

  60. Saaristo A et al (2006) Vascular endothelial growth factor-C accelerates diabetic wound healing. Am J Pathol 169:1080–1087

    Article  PubMed  CAS  Google Scholar 

  61. Takeda N et al (2004) Endothelial PAS domain protein 1 gene promotes angiogenesis through the transactivation of both vascular endothelial growth factor and its receptor, Flt-1. Circ Res 95:146–153

    Article  PubMed  CAS  Google Scholar 

  62. Galiano RD et al (2004) Topical vascular endothelial growth factor accelerates diabetic wound healing through increased angiogenesis and by mobilizing and recruiting bone marrow-derived cells. Am J Pathol 164:1935–1947

    Article  PubMed  CAS  Google Scholar 

  63. Romano Di Peppe S et al (2002) Adenovirus-mediated VEGF(165) gene transfer enhances wound healing by promoting angiogenesis in CD1 diabetic mice. Gene Ther 9:1271–1277

    Article  PubMed  CAS  Google Scholar 

  64. Rio MD et al (1999) Nonviral transfer of genes to pig primary keratinocytes. Induction of angiogenesis by composite grafts of modified keratinocytes overexpressing VEGF driven by a keratin promoter. Gene Ther 6:1734–1741

    Article  PubMed  CAS  Google Scholar 

  65. Jazwa A et al (2010) Combined vascular endothelial growth factor-A and fibroblast growth factor 4 gene transfer improves wound healing in diabetic mice. Genet Vaccines Ther 8:6

    Article  PubMed  CAS  Google Scholar 

  66. Jeschke MG, Herndon DN (2007) The combination of IGF-I and KGF cDNA improves dermal and epidermal regeneration by increased VEGF expression and neovascularization. Gene Ther 14:1235–1242

    Article  PubMed  CAS  Google Scholar 

  67. Jeschke MG, Klein D (2004) Liposomal gene transfer of multiple genes is more effective than gene transfer of a single gene. Gene Ther 11:847–855

    Article  PubMed  CAS  Google Scholar 

  68. Zheng Y et al (2007) Chimeric VEGF-ENZ7/PlGF specifically binding to VEGFR-2 accelerates skin wound healing via enhancement of neovascularization. Arterioscler Thromb Vasc Biol 27:503–511

    Article  PubMed  CAS  Google Scholar 

  69. Hamed S et al (2011) Fibronectin potentiates topical erythropoietin-induced wound repair in diabetic mice. J Invest Dermatol 131:1365–1374

    Article  PubMed  CAS  Google Scholar 

  70. Ackermann M et al (2011) Priming with a combination of proangiogenic growth factors improves wound healing in normoglycemic mice. Int J Mol Med 27:647–653

    PubMed  CAS  Google Scholar 

  71. Ortega S, Ittmann M, Tsang SH, Ehrlich M, Basilico C (1998) Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc Natl Acad Sci USA 95:5672–5677

    Article  PubMed  CAS  Google Scholar 

  72. Carmeliet P et al (2001) Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 7:575–583

    Article  PubMed  CAS  Google Scholar 

  73. Sarkar K et al (2012) Tie2-dependent knockout of HIF-1 impairs burn wound vascularization and homing of bone marrow-derived angiogenic cells. Cardiovasc Res 93:162–169

    Article  PubMed  CAS  Google Scholar 

  74. Zhang X et al (2010) Impaired angiogenesis and mobilization of circulating angiogenic cells in HIF-1alpha heterozygous-null mice after burn wounding. Wound Repair Regen 18:193–201

    Article  PubMed  CAS  Google Scholar 

  75. Mitchell K et al (2009) Alpha3beta1 integrin in epidermis promotes wound angiogenesis and keratinocyte-to-endothelial-cell crosstalk through the induction of MRP3. J Cell Sci 122:1778–1787

    Article  PubMed  CAS  Google Scholar 

  76. Zweers MC et al (2007) Integrin alpha2beta1 is required for regulation of murine wound angiogenesis but is dispensable for reepithelialization. J Invest Dermatol 127:467–478

    Article  PubMed  CAS  Google Scholar 

  77. Uutela M et al (2004) PDGF-D induces macrophage recruitment, increased interstitial pressure, and blood vessel maturation during angiogenesis. Blood 104:3198–3204

    Article  PubMed  CAS  Google Scholar 

  78. Lee PC et al (1999) Impaired wound healing and angiogenesis in eNOS-deficient mice. Am J Physiol 277:H1600–H1608

    PubMed  CAS  Google Scholar 

  79. Chin LC et al (2011) The influence of nitric oxide synthase 2 on cutaneous wound angiogenesis. Br J Dermatol 165:1223–1235

    Article  PubMed  CAS  Google Scholar 

  80. Yamasaki K et al (1998) Reversal of impaired wound repair in iNOS-deficient mice by topical adenoviral-mediated iNOS gene transfer. J Clin Invest 101:967–971

    Article  PubMed  CAS  Google Scholar 

  81. Most D, Efron DT, Shi HP, Tantry US, Barbul A (2002) Characterization of incisional wound healing in inducible nitric oxide synthase knockout mice. Surgery 132:866–876

    Article  PubMed  Google Scholar 

  82. Low QE et al (2001) Wound healing in MIP-1alpha(−/−) and MCP-1(−/−) mice. Am J Pathol 159:457–463

    Article  PubMed  CAS  Google Scholar 

  83. Devalaraja RM et al (2000) Delayed wound healing in CXCR2 knockout mice. J Invest Dermatol 115:234–244

    Article  PubMed  CAS  Google Scholar 

  84. Fang Y, Gong SJ, Wang Y, Xu YH, Bao SS (2007) Effect of GMCSF-absence on neovascularization during wound healing. Zhonghua Zheng Xing Wai Ke Za Zhi 23:233–235

    PubMed  Google Scholar 

  85. Fang Y, Gong SJ, Xu YH, Hambly BD, Bao S (2007) Impaired cutaneous wound healing in granulocyte/macrophage colony-stimulating factor knockout mice. Br J Dermatol 157:458–465

    Article  PubMed  CAS  Google Scholar 

  86. Mann A, Breuhahn K, Schirmacher P, Blessing M (2001) Keratinocyte-derived granulocyte-macrophage colony stimulating factor accelerates wound healing: stimulation of keratinocyte proliferation, granulation tissue formation, and vascularization. J Invest Dermatol 117:1382–1390

    Article  PubMed  CAS  Google Scholar 

  87. Streit M et al (2000) Thrombospondin-1 suppresses wound healing and granulation tissue formation in the skin of transgenic mice. EMBO J 19:3272–3282

    Article  PubMed  CAS  Google Scholar 

  88. Kyriakides TR, Tam JW, Bornstein P (1999) Accelerated wound healing in mice with a disruption of the thrombospondin 2 gene. J Invest Dermatol 113:782–787

    Article  PubMed  CAS  Google Scholar 

  89. Matthies AM, Low QE, Lingen MW, DiPietro LA (2002) Neuropilin-1 participates in wound angiogenesis. Am J Pathol 160:289–296

    Article  PubMed  CAS  Google Scholar 

  90. Brooks PC, Clark RA, Cheresh DA (1994) Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 264:569–571

    Article  PubMed  CAS  Google Scholar 

  91. Howdieshell TR et al (2001) Antibody neutralization of vascular endothelial growth factor inhibits wound granulation tissue formation. J Surg Res 96:173–182

    Article  PubMed  CAS  Google Scholar 

  92. Fu X, Li X, Cheng B, Chen W, Sheng Z (2005) Engineered growth factors and cutaneous wound healing: success and possible questions in the past 10 years. Wound Repair Regen 13:122–130

    Article  PubMed  Google Scholar 

  93. Riedel K et al (2006) Current status of genetic modulation of growth factors in wound repair. Int J Mol Med 17:183–193

    PubMed  Google Scholar 

  94. Adams RH, Alitalo K (2007) Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 8:464–478

    Article  PubMed  CAS  Google Scholar 

  95. Carmeliet P, De Smet F, Loges S, Mazzone M (2009) Branching morphogenesis and antiangiogenesis candidates: tip cells lead the way. Nat Rev Clin Oncol 6:315–326

    Article  PubMed  CAS  Google Scholar 

  96. Eilken HM, Adams RH (2010) Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr Opin Cell Biol 22:617–625

    Article  PubMed  CAS  Google Scholar 

  97. Potente M, Gerhardt H, Carmeliet P (2011) Basic and therapeutic aspects of angiogenesis. Cell 146:873–887

    Article  PubMed  CAS  Google Scholar 

  98. De Smet F, Segura I, De Bock K, Hohensinner PJ, Carmeliet P (2009) Mechanisms of vessel branching: filopodia on endothelial tip cells lead the way. Arterioscler Thromb Vasc Biol 29:639–649

    Article  PubMed  CAS  Google Scholar 

  99. LaVan FB, Hunt TK (1990) Oxygen and wound healing. Clin Plast Surg 17:463–472

    PubMed  CAS  Google Scholar 

  100. Hendrickx B et al (2010) Integration of blood outgrowth endothelial cells in dermal fibroblast sheets promotes full thickness wound healing. Stem Cells 28:1165–1177

    PubMed  CAS  Google Scholar 

  101. Andrikopoulou E et al (2011) Current Insights into the role of HIF-1 in cutaneous wound healing. Curr Mol Med 11:218–235

    Article  PubMed  CAS  Google Scholar 

  102. Augustin HG, Koh GY, Thurston G, Alitalo K (2009) Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol 10:165–177

    Article  PubMed  CAS  Google Scholar 

  103. Moya IM et al (2012) Stalk cell phenotype depends on integration of Notch and Smad1/5 signaling cascades. Dev Cell 22:501–514

    Article  PubMed  CAS  Google Scholar 

  104. Jones CA et al (2008) Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat Med 14:448–453

    Article  PubMed  CAS  Google Scholar 

  105. Gu C et al (2005) Semaphorin 3E and plexin-D1 control vascular pattern independently of neuropilins. Science 307:265–268

    Article  PubMed  CAS  Google Scholar 

  106. Lu X et al (2004) The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 432:179–186

    Article  PubMed  CAS  Google Scholar 

  107. Schmidt M et al (2007) EGFL7 regulates the collective migration of endothelial cells by restricting their spatial distribution. Development 134:2913–2923

    Article  PubMed  CAS  Google Scholar 

  108. Jakobsson L et al (2010) Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat Cell Biol 12:943–953

    Article  PubMed  CAS  Google Scholar 

  109. Harrington LS et al (2008) Regulation of multiple angiogenic pathways by Dll4 and Notch in human umbilical vein endothelial cells. Microvasc Res 75:144–154

    Article  PubMed  CAS  Google Scholar 

  110. Boulton ME, Cai J, Grant MB (2008) Gamma-Secretase: a multifaceted regulator of angiogenesis. J Cell Mol Med 12:781–795

    Article  PubMed  CAS  Google Scholar 

  111. Guarani V et al (2011) Acetylation-dependent regulation of endothelial Notch signalling by the SIRT1 deacetylase. Nature 473:234–238

    Article  PubMed  CAS  Google Scholar 

  112. Phng LK et al (2009) Nrarp coordinates endothelial Notch and Wnt signaling to control vessel density in angiogenesis. Dev Cell 16:70–82

    Article  PubMed  CAS  Google Scholar 

  113. Zeeb M, Strilic B, Lammert E (2010) Resolving cell-cell junctions: lumen formation in blood vessels. Curr Opin Cell Biol 22:626–632

    Article  PubMed  CAS  Google Scholar 

  114. Iruela-Arispe ML, Davis GE (2009) Cellular and molecular mechanisms of vascular lumen formation. Dev Cell 16:222–231

    Article  PubMed  CAS  Google Scholar 

  115. Carmeliet P et al (1999) Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98:147–157

    Article  PubMed  CAS  Google Scholar 

  116. Jin SW, Beis D, Mitchell T, Chen JN, Stainier DY (2005) Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 132:5199–5209

    Article  PubMed  CAS  Google Scholar 

  117. Francis SE et al (2002) Central roles of alpha5beta1 integrin and fibronectin in vascular development in mouse embryos and embryoid bodies. Arterioscler Thromb Vasc Biol 22:927–933

    Article  PubMed  CAS  Google Scholar 

  118. Zovein AC et al (2010) Beta1 integrin establishes endothelial cell polarity and arteriolar lumen formation via a Par3-dependent mechanism. Dev Cell 18:39–51

    Article  PubMed  CAS  Google Scholar 

  119. Almagro S et al (2010) The motor protein myosin-X transports VE-cadherin along filopodia to allow the formation of early endothelial cell-cell contacts. Mol Cell Biol 30:1703–1717

    Article  PubMed  CAS  Google Scholar 

  120. Fantin A et al (2010) Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 116:829–840

    Article  PubMed  CAS  Google Scholar 

  121. Tammela T et al (2011) VEGFR-3 controls tip to stalk conversion at vessel fusion sites by reinforcing Notch signalling. Nat Cell Biol 13:1202–1213

    Article  PubMed  CAS  Google Scholar 

  122. Luttun A et al (2002) Revascularization of ischemic tissues by PlGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat Med 8:831–840

    PubMed  CAS  Google Scholar 

  123. Frontini MJ et al (2011) Fibroblast growth factor 9 delivery during angiogenesis produces durable, vasoresponsive microvessels wrapped by smooth muscle cells. Nat Biotechnol 29:421–427

    Article  PubMed  CAS  Google Scholar 

  124. Bergers G, Song S (2005) The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol 7:452–464

    Article  PubMed  CAS  Google Scholar 

  125. Gaengel K, Genove G, Armulik A, Betsholtz C (2009) Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler Thromb Vasc Biol 29:630–638

    Article  PubMed  CAS  Google Scholar 

  126. Mazzone M et al (2009) Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 136:839–851

    Article  PubMed  CAS  Google Scholar 

  127. Stoll SJ, Bartsch S, Augustin HG, Kroll J (2011) The transcription factor HOXC9 regulates endothelial cell quiescence and vascular morphogenesis in zebrafish via inhibition of interleukin 8. Circ Res 108:1367–1377

    Article  PubMed  CAS  Google Scholar 

  128. Anand S et al (2010) MicroRNA-132-mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis. Nat Med 16:909–914

    Article  PubMed  CAS  Google Scholar 

  129. Goettsch W et al (2008) Flow-dependent regulation of angiopoietin-2. J Cell Physiol 214:491–503

    Article  PubMed  CAS  Google Scholar 

  130. Hristov M, Zernecke A, Liehn EA, Weber C (2007) Regulation of endothelial progenitor cell homing after arterial injury. Thromb Haemost 98:274–277

    PubMed  CAS  Google Scholar 

  131. Aicher A, Zeiher AM, Dimmeler S (2005) Mobilizing endothelial progenitor cells. Hypertension 45:321–325

    Article  PubMed  CAS  Google Scholar 

  132. Leone AM et al (2009) From bone marrow to the arterial wall: the ongoing tale of endothelial progenitor cells. Eur Heart J 30:890–899

    Article  PubMed  Google Scholar 

  133. Asahara T et al (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964–967

    Article  PubMed  CAS  Google Scholar 

  134. Ahn GO, Brown JM (2009) Role of endothelial progenitors and other bone marrow-derived cells in the development of the tumor vasculature. Angiogenesis 12:159–164

    Article  PubMed  CAS  Google Scholar 

  135. Fadini GP, Losordo D, Dimmeler S (2012) Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res 110:624–637

    Article  PubMed  CAS  Google Scholar 

  136. Ingram DA, Caplice NM, Yoder MC (2005) Unresolved questions, changing definitions, and novel paradigms for defining endothelial progenitor cells. Blood 106:1525–1531

    Article  PubMed  CAS  Google Scholar 

  137. Pearson JD (2009) Endothelial progenitor cells – hype or hope? J Thromb Haemost 7:255–262

    Article  PubMed  CAS  Google Scholar 

  138. Richardson MR, Yoder MC (2011) Endothelial progenitor cells: quo vadis? J Mol Cell Cardiol 50:266–272

    Article  PubMed  CAS  Google Scholar 

  139. Luttun A, Verfaillie CM (2007) Will the real EPC please stand up? Blood 109:1795–1796

    Article  CAS  Google Scholar 

  140. Timmermans F et al (2009) Endothelial progenitor cells: identity defined? J Cell Mol Med 13:87–102

    Article  PubMed  Google Scholar 

  141. Watt SM, Athanassopoulos A, Harris AL, Tsaknakis G (2010) Human endothelial stem/progenitor cells, angiogenic factors and vascular repair. J R Soc Interface 7(Suppl 6):S731–S751

    Article  PubMed  Google Scholar 

  142. Hattori K et al (2002) Placental growth factor reconstitutes hematopoiesis by recruiting VEGFR1(+) stem cells from bone-marrow microenvironment. Nat Med 8:841–849

    PubMed  CAS  Google Scholar 

  143. Heissig B et al (2002) Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109:625–637

    Article  PubMed  CAS  Google Scholar 

  144. Aicher A et al (2003) Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 9:1370–1376

    Article  PubMed  CAS  Google Scholar 

  145. Cheng XW et al (2007) Mechanisms underlying the impairment of ischemia-induced neovascularization in matrix metalloproteinase 2-deficient mice. Circ Res 100:904–913

    Article  PubMed  CAS  Google Scholar 

  146. Urbich C et al (2005) Cathepsin L is required for endothelial progenitor cell-induced neovascularization. Nat Med 11:206–213

    Article  PubMed  CAS  Google Scholar 

  147. Levesque JP, Takamatsu Y, Nilsson SK, Haylock DN, Simmons PJ (2001) Vascular cell adhesion molecule-1 (CD106) is cleaved by neutrophil proteases in the bone marrow following hematopoietic progenitor cell mobilization by granulocyte colony-stimulating factor. Blood 98:1289–1297

    Article  PubMed  CAS  Google Scholar 

  148. Levesque JP, Hendy J, Takamatsu Y, Simmons PJ, Bendall LJ (2003) Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J Clin Invest 111:187–196

    PubMed  CAS  Google Scholar 

  149. Li B et al (2006) VEGF and PlGF promote adult vasculogenesis by enhancing EPC recruitment and vessel formation at the site of tumor neovascularization. FASEB J 20:1495–1497

    Article  PubMed  CAS  Google Scholar 

  150. Li X et al (2005) Revascularization of ischemic tissues by PDGF-CC via effects on endothelial cells and their progenitors. J Clin Invest 115:118–127

    PubMed  CAS  Google Scholar 

  151. Ishida Y et al (2012) Pivotal role of the CCL5/CCR5 interaction for recruitment of endothelial progenitor cells in mouse wound healing. J Clin Invest 122:711–721

    Article  PubMed  CAS  Google Scholar 

  152. Dimmeler S (2010) Regulation of bone marrow-derived vascular progenitor cell mobilization and maintenance. Arterioscler Thromb Vasc Biol 30:1088–1093

    Article  PubMed  CAS  Google Scholar 

  153. Zampetaki A, Kirton JP, Xu Q (2008) Vascular repair by endothelial progenitor cells. Cardiovasc Res 78:413–421

    Article  PubMed  CAS  Google Scholar 

  154. Velazquez OC (2007) Angiogenesis and vasculogenesis: inducing the growth of new blood vessels and wound healing by stimulation of bone marrow-derived progenitor cell mobilization and homing. J Vasc Surg 45(Suppl A):A39–A47

    Article  PubMed  Google Scholar 

  155. Thom SR et al (2011) Vasculogenic stem cell mobilization and wound recruitment in diabetic patients: increased cell number and intracellular regulatory protein content associated with hyperbaric oxygen therapy. Wound Repair Regen 19:149–161

    Article  PubMed  Google Scholar 

  156. Yu X, Cohen DM, Chen CS (2012) miR-125b is an adhesion-regulated microRNA that protects mesenchymal stem cells from anoikis. Stem Cells 30:956–964

    Article  PubMed  CAS  Google Scholar 

  157. Ruiz de Almodovar C, Luttun A, Carmeliet P (2006) An SDF-1 trap for myeloid cells stimulates angiogenesis. Cell 124:18–21

    Article  PubMed  CAS  Google Scholar 

  158. Grunewald M et al (2006) VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 124:175–189

    Article  PubMed  CAS  Google Scholar 

  159. Bluff JE, Ferguson MW, O’Kane S, Ireland G (2007) Bone marrow-derived endothelial progenitor cells do not contribute significantly to new vessels during incisional wound healing. Exp Hematol 35:500–506

    Article  PubMed  CAS  Google Scholar 

  160. Aicher A et al (2007) Nonbone marrow-derived circulating progenitor cells contribute to postnatal neovascularization following tissue ischemia. Circ Res 100:581–589

    Article  PubMed  CAS  Google Scholar 

  161. Ergun S, Tilki D, Klein D (2011) Vascular wall as a reservoir for different types of stem and progenitor cells. Antioxid Redox Signal 15:981–995

    Article  PubMed  CAS  Google Scholar 

  162. Majesky MW, Dong XR, Hoglund V, Daum G, Mahoney WM Jr (2012) The adventitia: a progenitor cell niche for the vessel wall. Cells Tissues Organs 195:73–81

    Article  PubMed  Google Scholar 

  163. Majesky MW, Dong XR, Hoglund V, Mahoney WM Jr, Daum G (2011) The adventitia: a dynamic interface containing resident progenitor cells. Arterioscler Thromb Vasc Biol 31:1530–1539

    Article  PubMed  CAS  Google Scholar 

  164. Pacilli A, Pasquinelli G (2009) Vascular wall resident progenitor cells: a review. Exp Cell Res 315:901–914

    Article  PubMed  CAS  Google Scholar 

  165. Psaltis PJ, Harbuzariu A, Delacroix S, Holroyd EW, Simari RD (2011) Resident vascular progenitor cells – diverse origins, phenotype, and function. J Cardiovasc Transl Res 4:161–176

    Article  PubMed  Google Scholar 

  166. Torsney E, Xu Q (2011) Resident vascular progenitor cells. J Mol Cell Cardiol 50:304–311

    Article  PubMed  CAS  Google Scholar 

  167. Chen CW, Corselli M, Peault B, Huard J (2012) Human blood-vessel-derived stem cells for tissue repair and regeneration. J Biomed Biotechnol 2012:597439

    PubMed  Google Scholar 

  168. Cordes KR, Srivastava D (2009) MicroRNA regulation of cardiovascular development. Circ Res 104:724–732

    Article  PubMed  CAS  Google Scholar 

  169. Caporali A, Emanueli C (2011) MicroRNA regulation in angiogenesis. Vascul Pharmacol 55:79–86

    Article  PubMed  CAS  Google Scholar 

  170. Fichtlscherer S, Zeiher AM, Dimmeler S (2011) Circulating microRNAs: biomarkers or mediators of cardiovascular diseases? Arterioscler Thromb Vasc Biol 31:2383–2390

    Article  PubMed  CAS  Google Scholar 

  171. Ohtani K, Dimmeler S (2011) Control of cardiovascular differentiation by microRNAs. Basic Res Cardiol 106:5–11

    Article  PubMed  CAS  Google Scholar 

  172. Wang S et al (2008) The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell 15:261–271

    Article  PubMed  CAS  Google Scholar 

  173. Bonauer A et al (2009) MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science 324:1710–1713

    Article  PubMed  CAS  Google Scholar 

  174. Kane NM et al (2012) Role of microRNAs 99b, 181a, and 181b in the differentiation of human embryonic stem cells to vascular endothelial cells. Stem Cells 30:643–654

    Article  PubMed  CAS  Google Scholar 

  175. Sen CK (2011) MicroRNAs as new maestro conducting the expanding symphony orchestra of regenerative and reparative medicine. Physiol Genomics 43:517–520

    Article  PubMed  CAS  Google Scholar 

  176. Howard L, Kane NM, Milligan G, Baker AH (2011) MicroRNAs regulating cell pluripotency and vascular differentiation. Vascul Pharmacol 55:69–78

    Article  PubMed  CAS  Google Scholar 

  177. Guo L, Zhao RC, Wu Y (2011) The role of microRNAs in self-renewal and differentiation of mesenchymal stem cells. Exp Hematol 39:608–616

    Article  PubMed  CAS  Google Scholar 

  178. Teta M et al (2012) Inducible deletion of epidermal Dicer and Drosha reveals multiple functions for miRNAs in postnatal skin. Development 139:1405–1416

    Article  PubMed  CAS  Google Scholar 

  179. Bavan L, Midwood K, Nanchahal J (2011) MicroRNA epigenetics: a new avenue for wound healing research. BioDrugs 25:27–41

    Article  PubMed  CAS  Google Scholar 

  180. Shilo S, Roy S, Khanna S, Sen CK (2007) MicroRNA in cutaneous wound healing: a new paradigm. DNA Cell Biol 26:227–237

    Article  PubMed  CAS  Google Scholar 

  181. Zou Z et al (2010) More insight into mesenchymal stem cells and their effects inside the body. Expert Opin Biol Ther 10:215–230

    Article  PubMed  CAS  Google Scholar 

  182. Banerjee S, Bacanamwo M (2010) DNA methyltransferase inhibition induces mouse embryonic stem cell differentiation into endothelial cells. Exp Cell Res 316:172–180

    Article  PubMed  CAS  Google Scholar 

  183. Hunt TK, Twomey P, Zederfeldt B, Dunphy JE (1967) Respiratory gas tensions and pH in healing wounds. Am J Surg 114:302–307

    Article  PubMed  CAS  Google Scholar 

  184. O’Toole EA et al (1997) Hypoxia increases human keratinocyte motility on connective tissue. J Clin Invest 100:2881–2891

    Article  PubMed  Google Scholar 

  185. Kan C, Abe M, Yamanaka M, Ishikawa O (2003) Hypoxia-induced increase of matrix metalloproteinase-1 synthesis is not restored by reoxygenation in a three-dimensional culture of human dermal fibroblasts. J Dermatol Sci 32:75–82

    Article  PubMed  CAS  Google Scholar 

  186. Feugate JE, Li Q, Wong L, Martins-Green M (2002) The cxc chemokine cCAF stimulates differentiation of fibroblasts into myofibroblasts and accelerates wound closure. J Cell Biol 156:161–172

    Article  PubMed  CAS  Google Scholar 

  187. Chaudhuri V, Zhou L, Karasek M (2007) Inflammatory cytokines induce the transformation of human dermal microvascular endothelial cells into myofibroblasts: a potential role in skin fibrogenesis. J Cutan Pathol 34:146–153

    Article  PubMed  CAS  Google Scholar 

  188. Zhang S, Uludag H (2009) Nanoparticulate systems for growth factor delivery. Pharm Res 26:1561–1580

    Article  PubMed  CAS  Google Scholar 

  189. Lee K, Silva EA, Mooney DJ (2011) Growth factor delivery-based tissue engineering: general approaches and a review of recent developments. J R Soc Interface 8:153–170

    Article  PubMed  CAS  Google Scholar 

  190. Chen FM, Zhang M, Wu ZF (2010) Toward delivery of multiple growth factors in tissue engineering. Biomaterials 31:6279–6308

    Article  PubMed  CAS  Google Scholar 

  191. McCarty DM, Monahan PE, Samulski RJ (2001) Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther 8:1248–1254

    Article  PubMed  CAS  Google Scholar 

  192. Dileo J, Miller TE Jr, Chesnoy S, Huang L (2003) Gene transfer to subdermal tissues via a new gene gun design. Hum Gene Ther 14:79–87

    Article  PubMed  CAS  Google Scholar 

  193. Hacein-Bey-Abina S et al (2003) A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 348:255–256

    Article  PubMed  Google Scholar 

  194. Chen S et al (2005) Efficient transduction of vascular endothelial cells with recombinant adeno-associated virus serotype 1 and 5 vectors. Hum Gene Ther 16:235–247

    Article  PubMed  CAS  Google Scholar 

  195. Liechty KW et al (1999) Adenoviral-mediated overexpression of platelet-derived growth factor-B corrects ischemic impaired wound healing. J Invest Dermatol 113:375–383

    Article  PubMed  CAS  Google Scholar 

  196. Sun L, Li J, Xiao X (2000) Overcoming adeno-associated virus vector size limitation through viral DNA heterodimerization. Nat Med 6:599–602

    Article  PubMed  CAS  Google Scholar 

  197. Eriksson E et al (1998) In vivo gene transfer to skin and wound by microseeding. J Surg Res 78:85–91

    Article  PubMed  CAS  Google Scholar 

  198. Vranckx JJ et al (2005) In vivo gene delivery of Ad-VEGF121 to full-thickness wounds in aged pigs results in high levels of VEGF expression but not in accelerated healing. Wound Repair Regen 13:51–60

    Article  PubMed  Google Scholar 

  199. Eming SA et al (1999) Particle-mediated gene transfer of PDGF isoforms promotes wound repair. J Invest Dermatol 112:297–302

    Article  PubMed  CAS  Google Scholar 

  200. Dickens S et al (2010) Nonviral transfection strategies for keratinocytes, fibroblasts, and endothelial progenitor cells for ex vivo gene transfer to skin wounds. Tissue Eng Part C Methods 16:1601–1608

    Article  PubMed  CAS  Google Scholar 

  201. Dijkmans PA et al (2004) Microbubbles and ultrasound: from diagnosis to therapy. Eur J Echocardiogr 5:245–256

    Article  PubMed  CAS  Google Scholar 

  202. Nyborg WL et al (2006) Emerging therapeutic ultrasound. World Scientific, Hackensack

    Google Scholar 

  203. Chen ZY, He CY, Ehrhardt A, Kay MA (2003) Minicircle DNA vectors devoid of bacterial DNA result in persistent and high-level transgene expression in vivo. Mol Ther 8:495–500

    Article  PubMed  CAS  Google Scholar 

  204. Felgner PL, Ringold GM (1989) Cationic liposome-mediated transfection. Nature 337:387–388

    Article  PubMed  CAS  Google Scholar 

  205. Jacobsen F et al (2006) Polybrene improves transfection efficacy of recombinant replication-deficient adenovirus in cutaneous cells and burned skin. J Gene Med 8:138–146

    Article  PubMed  CAS  Google Scholar 

  206. Yotnda P et al (2002) Bilamellar cationic liposomes protect adenovectors from preexisting humoral immune responses. Mol Ther 5:233–241

    Article  PubMed  CAS  Google Scholar 

  207. Kazuki Y et al (2011) Refined human artificial chromosome vectors for gene therapy and animal transgenesis. Gene Ther 18:384–393

    Article  PubMed  CAS  Google Scholar 

  208. Oshimura M, Katoh M (2008) Transfer of human artificial chromosome vectors into stem cells. Reprod Biomed Online 16:57–69

    Article  PubMed  Google Scholar 

  209. Gossen M et al (1995) Transcriptional activation by tetracyclines in mammalian cells. Science 268:1766–1769

    Article  PubMed  CAS  Google Scholar 

  210. Yao F et al (1998) Tetracycline repressor, tetR, rather than the tetR-mammalian cell transcription factor fusion derivatives, regulates inducible gene expression in mammalian cells. Hum Gene Ther 9:1939–1950

    Article  PubMed  CAS  Google Scholar 

  211. Yao F, Theopold C, Hoeller D, Bleiziffer O, Lu Z (2006) Highly efficient regulation of gene expression by tetracycline in a replication-defective herpes simplex viral vector. Mol Ther 13:1133–1141

    Article  PubMed  CAS  Google Scholar 

  212. No D, Yao TP, Evans RM (1996) Ecdysone-inducible gene expression in mammalian cells and transgenic mice. Proc Natl Acad Sci USA 93:3346–3351

    Article  PubMed  CAS  Google Scholar 

  213. Wang Y, O’Malley BW Jr, Tsai SY, O’Malley BW (1994) A regulatory system for use in gene transfer. Proc Natl Acad Sci USA 91:8180–8184

    Article  PubMed  CAS  Google Scholar 

  214. Braselmann S, Graninger P, Busslinger M (1993) A selective transcriptional induction system for mammalian cells based on Gal4-estrogen receptor fusion proteins. Proc Natl Acad Sci USA 90:1657–1661

    Article  PubMed  CAS  Google Scholar 

  215. Mills AA (2001) Changing colors in mice: an inducible system that delivers. Genes Dev 15:1461–1467

    Article  PubMed  CAS  Google Scholar 

  216. Fasolo A, Sessa C (2012) Targeting mTOR pathways in human malignancies. Curr Pharm Des 18:2766–2777

    Article  PubMed  CAS  Google Scholar 

  217. Sauer B, Henderson N (1988) Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1. Proc Natl Acad Sci USA 85:5166–5170

    Article  PubMed  CAS  Google Scholar 

  218. Peattie RA et al (2006) Dual growth factor-induced angiogenesis in vivo using hyaluronan hydrogel implants. Biomaterials 27:1868–1875

    Article  PubMed  CAS  Google Scholar 

  219. Riley CM et al (2006) Stimulation of in vivo angiogenesis using dual growth factor-loaded crosslinked glycosaminoglycan hydrogels. Biomaterials 27:5935–5943

    Article  PubMed  CAS  Google Scholar 

  220. Dogan AK, Gumusderelioglu M, Aksoz E (2005) Controlled release of EGF and bFGF from dextran hydrogels in vitro and in vivo. J Biomed Mater Res B Appl Biomater 74:504–510

    PubMed  Google Scholar 

  221. Nillesen ST et al (2007) Increased angiogenesis and blood vessel maturation in acellular collagen-heparin scaffolds containing both FGF2 and VEGF. Biomaterials 28:1123–1131

    Article  PubMed  CAS  Google Scholar 

  222. Richardson TP, Peters MC, Ennett AB, Mooney DJ (2001) Polymeric system for dual growth factor delivery. Nat Biotechnol 19:1029–1034

    Article  PubMed  CAS  Google Scholar 

  223. Chen RR, Silva EA, Yuen WW, Mooney DJ (2007) Spatio-temporal VEGF and PDGF delivery patterns blood vessel formation and maturation. Pharm Res 24:258–264

    Article  PubMed  CAS  Google Scholar 

  224. Knighton DR, Ciresi KF, Fiegel VD, Austin LL, Butler EL (1986) Classification and treatment of chronic nonhealing wounds. Successful treatment with autologous platelet-derived wound healing factors (PDWHF). Ann Surg 204:322–330

    Article  PubMed  CAS  Google Scholar 

  225. Borrione P, Gianfrancesco AD, Pereira MT, Pigozzi F (2010) Platelet-rich plasma in muscle healing. Am J Phys Med Rehabil 89:854–861

    Article  PubMed  Google Scholar 

  226. Pallua N, Wolter T, Markowicz M (2010) Platelet-rich plasma in burns. Burns 36:4–8

    Article  PubMed  Google Scholar 

  227. Yu W, Wang J, Yin J (2011) Platelet-rich plasma: a promising product for treatment of peripheral nerve regeneration after nerve injury. Int J Neurosci 121:176–180

    Article  PubMed  Google Scholar 

  228. Demidova-Rice TN, Wolf L, Deckenback J, Hamblin MR, Herman IM (2012) Human platelet-rich plasma- and extracellular matrix-derived peptides promote impaired cutaneous wound healing in vivo. PLoS One 7:e32146

    Article  PubMed  CAS  Google Scholar 

  229. Blanton MW et al (2009) Adipose stromal cells and platelet-rich plasma therapies synergistically increase revascularization during wound healing. Plast Reconstr Surg 123:56S–64S

    Article  PubMed  CAS  Google Scholar 

  230. Vermeulen P et al (2009) A plasma-based biomatrix mixed with endothelial progenitor cells and keratinocytes promotes matrix formation, angiogenesis, and reepithelialization in full-thickness wounds. Tissue Eng Part A 15:1533–1542

    Article  PubMed  CAS  Google Scholar 

  231. Anitua E et al (2008) Effectiveness of autologous preparation rich in growth factors for the treatment of chronic cutaneous ulcers. J Biomed Mater Res B Appl Biomater 84:415–421

    PubMed  Google Scholar 

  232. Foster TE, Puskas BL, Mandelbaum BR, Gerhardt MB, Rodeo SA (2009) Platelet-rich plasma: from basic science to clinical applications. Am J Sports Med 37:2259–2272

    Article  PubMed  Google Scholar 

  233. Steed DL et al (2008) Amnion-derived cellular cytokine solution: a physiological combination of cytokines for wound healing. Eplasty 8:e18

    PubMed  Google Scholar 

  234. Bergmann J et al (2009) The effect of amnion-derived cellular cytokine solution on the epithelialization of partial-thickness donor site wounds in normal and streptozotocin-induced diabetic swine. Eplasty 9:e49

    PubMed  Google Scholar 

  235. Payne WG et al (2010) Effect of amnion-derived cellular cytokine solution on healing of experimental partial-thickness burns. World J Surg 34:1663–1668

    Article  PubMed  Google Scholar 

  236. Daniel JM, Sedding DG (2011) Circulating smooth muscle progenitor cells in arterial remodeling. J Mol Cell Cardiol 50:273–279

    Article  PubMed  CAS  Google Scholar 

  237. Orlandi A, Bennett M (2010) Progenitor cell-derived smooth muscle cells in vascular disease. Biochem Pharmacol 79:1706–1713

    Article  PubMed  CAS  Google Scholar 

  238. Sirker AA, Astroulakis ZM, Hill JM (2009) Vascular progenitor cells and translational research: the role of endothelial and smooth muscle progenitor cells in endogenous arterial remodelling in the adult. Clin Sci (Lond) 116(283–299)

    Google Scholar 

  239. Templin C et al (2009) Ex vivo expanded haematopoietic progenitor cells improve dermal wound healing by paracrine mechanisms. Exp Dermatol 18:445–453

    Article  PubMed  CAS  Google Scholar 

  240. Carmeliet P, Luttun A (2001) The emerging role of the bone marrow-derived stem cells in (therapeutic) angiogenesis. Thromb Haemost 86:289–297

    PubMed  CAS  Google Scholar 

  241. Lyden D et al (2001) Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 7:1194–1201

    Article  PubMed  CAS  Google Scholar 

  242. Takakura N (2006) Role of hematopoietic lineage cells as accessory components in blood vessel formation. Cancer Sci 97:568–574

    Article  PubMed  CAS  Google Scholar 

  243. Melero-Martin JM et al (2010) Host myeloid cells are necessary for creating bioengineered human vascular networks in vivo. Tissue Eng Part A 16:2457–2466

    Article  PubMed  CAS  Google Scholar 

  244. Huber TL (2010) Dissecting hematopoietic differentiation using the embryonic stem cell differentiation model. Int J Dev Biol 54:991–1002

    Article  PubMed  CAS  Google Scholar 

  245. Huber TL, Kouskoff V, Fehling HJ, Palis J, Keller G (2004) Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432:625–630

    Article  PubMed  CAS  Google Scholar 

  246. Keller G (2005) Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev 19:1129–1155

    Article  PubMed  CAS  Google Scholar 

  247. Davison PM, Bensch K, Karasek MA (1980) Isolation and growth of endothelial cells from the microvessels of the newborn human foreskin in cell culture. J Invest Dermatol 75:316–321

    Article  PubMed  CAS  Google Scholar 

  248. Supp DM, Wilson-Landy K, Boyce ST (2002) Human dermal microvascular endothelial cells form vascular analogs in cultured skin substitutes after grafting to athymic mice. FASEB J 16:797–804

    Article  PubMed  CAS  Google Scholar 

  249. Richard L, Velasco P, Detmar M (1998) A simple immunomagnetic protocol for the selective isolation and long-term culture of human dermal microvascular endothelial cells. Exp Cell Res 240:1–6

    Article  PubMed  CAS  Google Scholar 

  250. Kubota Y, Kleinman HK, Martin GR, Lawley TJ (1988) Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J Cell Biol 107:1589–1598

    Article  PubMed  CAS  Google Scholar 

  251. Gupta K, Ramakrishnan S, Browne PV, Solovey A, Hebbel RP (1997) A novel technique for culture of human dermal microvascular endothelial cells under either serum-free or serum-supplemented conditions: isolation by panning and stimulation with vascular endothelial growth factor. Exp Cell Res 230:244–251

    Article  PubMed  CAS  Google Scholar 

  252. Sorrell JM, Baber MA, Caplan AI (2007) A self-assembled fibroblast-endothelial cell co-culture system that supports in vitro vasculogenesis by both human umbilical vein endothelial cells and human dermal microvascular endothelial cells. Cells Tissues Organs 186:157–168

    Article  PubMed  Google Scholar 

  253. Nor JE et al (2001) Engineering and characterization of functional human microvessels in immunodeficient mice. Lab Invest 81:453–463

    Article  PubMed  CAS  Google Scholar 

  254. Polchow B et al (2012) Cryopreservation of human vascular umbilical cord cells under good manufacturing practice conditions for future cell banks. J Transl Med 10:98

    Article  PubMed  CAS  Google Scholar 

  255. Unger RE, Krump-Konvalinkova V, Peters K, Kirkpatrick CJ (2002) In vitro expression of the endothelial phenotype: comparative study of primary isolated cells and cell lines, including the novel cell line HPMEC-ST1.6R. Microvasc Res 64:384–397

    Article  PubMed  CAS  Google Scholar 

  256. Hannan RL et al (1988) Endothelial cells synthesize basic fibroblast growth factor and transforming growth factor beta. Growth Factors 1:7–17

    Article  PubMed  CAS  Google Scholar 

  257. Bhang SH et al (2012) Three-dimensional cell grafting enhances the angiogenic efficacy of human umbilical vein endothelial cells. Tissue Eng Part A 18:310–319

    Article  PubMed  CAS  Google Scholar 

  258. Alajati A et al (2008) Spheroid-based engineering of a human vasculature in mice. Nat Methods 5:439–445

    Article  PubMed  CAS  Google Scholar 

  259. Schechner JS et al (2000) In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc Natl Acad Sci USA 97:9191–9196

    Article  PubMed  CAS  Google Scholar 

  260. Yoder MC et al (2007) Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 109:1801–1809

    Article  PubMed  CAS  Google Scholar 

  261. Awad O et al (2006) Differential healing activities of CD34+ and CD14+ endothelial cell progenitors. Arterioscler Thromb Vasc Biol 26:758–764

    Article  PubMed  CAS  Google Scholar 

  262. Case J et al (2007) Human CD34+ AC133+ VEGFR-2+ cells are not endothelial progenitor cells but distinct, primitive hematopoietic progenitors. Exp Hematol 35:1109–1118

    Article  PubMed  CAS  Google Scholar 

  263. Kim SY et al (2005) Differentiation of endothelial cells from human umbilical cord blood AC133-CD14+ cells. Ann Hematol 84:417–422

    Article  PubMed  CAS  Google Scholar 

  264. Rehman J, Li J, Orschell CM, March KL (2003) Peripheral blood “endothelial progenitor cells” are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 107:1164–1169

    Article  PubMed  Google Scholar 

  265. Sieveking DP, Buckle A, Celermajer DS, Ng MK (2008) Strikingly different angiogenic properties of endothelial progenitor cell subpopulations: insights from a novel human angiogenesis assay. J Am Coll Cardiol 51:660–668

    Article  PubMed  CAS  Google Scholar 

  266. Shepherd BR et al (2006) Vascularization and engraftment of a human skin substitute using circulating progenitor cell-derived endothelial cells. FASEB J 20:1739–1741

    Article  PubMed  CAS  Google Scholar 

  267. Yoder MC (2010) Is endothelium the origin of endothelial progenitor cells? Arterioscler Thromb Vasc Biol 30:1094–1103

    Article  PubMed  CAS  Google Scholar 

  268. van Beem RT et al (2009) Blood outgrowth endothelial cells from cord blood and peripheral blood: angiogenesis-related characteristics in vitro. J Thromb Haemost 7:217–226

    Article  PubMed  CAS  Google Scholar 

  269. Corselli M et al (2008) Clinical scale ex vivo expansion of cord blood-derived outgrowth endothelial progenitor cells is associated with high incidence of karyotype aberrations. Exp Hematol 36:340–349

    Article  PubMed  CAS  Google Scholar 

  270. Au P et al (2008) Differential in vivo potential of endothelial progenitor cells from human umbilical cord blood and adult peripheral blood to form functional long-lasting vessels. Blood 111:1302–1305

    Article  PubMed  CAS  Google Scholar 

  271. Suh W et al (2005) Transplantation of endothelial progenitor cells accelerates dermal wound healing with increased recruitment of monocytes/macrophages and neovascularization. Stem Cells 23:1571–1578

    Article  PubMed  Google Scholar 

  272. Sander AL et al (2011) Systemic transplantation of progenitor cells accelerates wound epithelialization and neovascularization in the hairless mouse ear wound model. J Surg Res 165:165–170

    Article  PubMed  Google Scholar 

  273. Goldstein LJ et al (2006) Endothelial progenitor cell release into circulation is triggered by hyperoxia-induced increases in bone marrow nitric oxide. Stem Cells 24:2309–2318

    Article  PubMed  CAS  Google Scholar 

  274. Barcelos LS et al (2009) Human CD133+ progenitor cells promote the healing of diabetic ischemic ulcers by paracrine stimulation of angiogenesis and activation of Wnt signaling. Circ Res 104:1095–1102

    Article  PubMed  CAS  Google Scholar 

  275. Reinisch A, Strunk D (2009) Isolation and animal serum free expansion of human umbilical cord derived mesenchymal stromal cells (MSCs) and endothelial colony forming progenitor cells (ECFCs). J Vis Exp 8(32):pii.1525

    Google Scholar 

  276. Krenning G, van Luyn MJ, Harmsen MC (2009) Endothelial progenitor cell-based neovascularization: implications for therapy. Trends Mol Med 15:180–189

    Article  PubMed  CAS  Google Scholar 

  277. Yoon CH et al (2005) Synergistic neovascularization by mixed transplantation of early endothelial progenitor cells and late outgrowth endothelial cells: the role of angiogenic cytokines and matrix metalloproteinases. Circulation 112:1618–1627

    Article  PubMed  Google Scholar 

  278. Bianco P (2011) Back to the future: moving beyond “mesenchymal stem cells”. J Cell Biochem 112:1713–1721

    Article  PubMed  CAS  Google Scholar 

  279. Caplan AI (1991) Mesenchymal stem cells. J Orthop Res 9:641–650

    Article  PubMed  CAS  Google Scholar 

  280. Vishnubalaji R et al (2012) In vitro differentiation of human skin-derived multipotent stromal cells into putative endothelial-like cells. BMC Dev Biol 12:7

    Article  PubMed  CAS  Google Scholar 

  281. Chen J et al (2008) Kidney-derived mesenchymal stem cells contribute to vasculogenesis, angiogenesis and endothelial repair. Kidney Int 74:879–889

    Article  PubMed  CAS  Google Scholar 

  282. Marchionni C et al (2009) Angiogenic potential of human dental pulp stromal (stem) cells. Int J Immunopathol Pharmacol 22:699–706

    PubMed  CAS  Google Scholar 

  283. Branski LK, Gauglitz GG, Herndon DN, Jeschke MG (2009) A review of gene and stem cell therapy in cutaneous wound healing. Burns 35:171–180

    Article  PubMed  Google Scholar 

  284. Romanov YA, Svintsitskaya VA, Smirnov VN (2003) Searching for alternative sources of postnatal human mesenchymal stem cells: candidate MSC-like cells from umbilical cord. Stem Cells 21:105–110

    Article  PubMed  Google Scholar 

  285. Zebardast N, Lickorish D, Davies JE (2010) Human umbilical cord perivascular cells (HUCPVC): a mesenchymal cell source for dermal wound healing. Organogenesis 6:197–203

    Article  PubMed  Google Scholar 

  286. Yang S, Huang S, Feng C, Fu X (2012) Umbilical cord-derived mesenchymal stem cells: strategies, challenges, and potential for cutaneous regeneration. Front Med 6:41–47

    Article  PubMed  Google Scholar 

  287. Anker PS I’t et al (2004) Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 22:1338–1345

    Article  Google Scholar 

  288. Spitzer TL et al (2012) Perivascular human endometrial mesenchymal stem cells express pathways relevant to self-renewal, lineage specification, and functional phenotype. Biol Reprod 86:58

    Article  PubMed  CAS  Google Scholar 

  289. Herdrich BJ, Lind RC, Liechty KW (2008) Multipotent adult progenitor cells: their role in wound healing and the treatment of dermal wounds. Cytotherapy 10:543–550

    Article  PubMed  CAS  Google Scholar 

  290. da Silva Meirelles L, Chagastelles PC, Nardi NB (2006) Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119:2204–2213

    Article  PubMed  CAS  Google Scholar 

  291. Otto WR, Wright NA (2011) Mesenchymal stem cells: from experiment to clinic. Fibrogenesis Tissue Repair 4:20

    Article  PubMed  CAS  Google Scholar 

  292. Natesan S, Wrice NL, Baer DG, Christy RJ (2011) Debrided skin as a source of autologous stem cells for wound repair. Stem Cells 29:1219–1230

    Article  PubMed  CAS  Google Scholar 

  293. Dominici M et al (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315–317

    Article  PubMed  CAS  Google Scholar 

  294. Fu X, Li H (2009) Mesenchymal stem cells and skin wound repair and regeneration: possibilities and questions. Cell Tissue Res 335:317–321

    Article  PubMed  Google Scholar 

  295. Chen L, Tredget EE, Wu PY, Wu Y (2008) Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 3:e1886

    Article  PubMed  CAS  Google Scholar 

  296. Hanson SE, Bentz ML, Hematti P (2010) Mesenchymal stem cell therapy for nonhealing cutaneous wounds. Plast Reconstr Surg 125:510–516

    Article  PubMed  CAS  Google Scholar 

  297. Hocking AM, Gibran NS (2010) Mesenchymal stem cells: paracrine signaling and differentiation during cutaneous wound repair. Exp Cell Res 316:2213–2219

    Article  PubMed  CAS  Google Scholar 

  298. Li H, Fu X (2012) Mechanisms of action of mesenchymal stem cells in cutaneous wound repair and regeneration. Cell Tissue Res 348:371–377

    Article  PubMed  Google Scholar 

  299. Sorrell JM, Caplan AI (2010) Topical delivery of mesenchymal stem cells and their function in wounds. Stem Cell Res Ther 1:30

    Article  PubMed  Google Scholar 

  300. Miura M et al (2006) Accumulated chromosomal instability in murine bone marrow mesenchymal stem cells leads to malignant transformation. Stem Cells 24:1095–1103

    Article  PubMed  Google Scholar 

  301. Rubio D et al (2005) Spontaneous human adult stem cell transformation. Cancer Res 65:3035–3039

    PubMed  CAS  Google Scholar 

  302. Tarte K et al (2010) Clinical-grade production of human mesenchymal stromal cells: occurrence of aneuploidy without transformation. Blood 115:1549–1553

    Article  PubMed  CAS  Google Scholar 

  303. Koc ON et al (2002) Allogeneic mesenchymal stem cell infusion for treatment of metachromatic leukodystrophy (MLD) and Hurler syndrome (MPS-IH). Bone Marrow Transplant 30:215–222

    Article  PubMed  CAS  Google Scholar 

  304. Bernardo ME, Locatelli F, Fibbe WE (2009) Mesenchymal stromal cells. Ann N Y Acad Sci 1176:101–117

    Article  PubMed  CAS  Google Scholar 

  305. Schallmoser K et al (2007) Human platelet lysate can replace fetal bovine serum for clinical-scale expansion of functional mesenchymal stromal cells. Transfusion 47:1436–1446

    Article  PubMed  CAS  Google Scholar 

  306. Cao Y et al (2005) Human adipose tissue-derived stem cells differentiate into endothelial cells in vitro and improve postnatal neovascularization in vivo. Biochem Biophys Res Commun 332:370–379

    Article  PubMed  CAS  Google Scholar 

  307. Miranville A et al (2004) Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation 110:349–355

    Article  PubMed  CAS  Google Scholar 

  308. Planat-Benard V et al (2004) Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 109:656–663

    Article  PubMed  Google Scholar 

  309. Sasaki M et al (2008) Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell type. J Immunol 180:2581–2587

    PubMed  CAS  Google Scholar 

  310. Wu KH et al (2007) In vitro and in vivo differentiation of human umbilical cord derived stem cells into endothelial cells. J Cell Biochem 100:608–616

    Article  PubMed  CAS  Google Scholar 

  311. Chen MY, Lie PC, Li ZL, Wei X (2009) Endothelial differentiation of Wharton’s jelly-derived mesenchymal stem cells in comparison with bone marrow-derived mesenchymal stem cells. Exp Hematol 37:629–640

    Article  PubMed  CAS  Google Scholar 

  312. Gang EJ et al (2006) In vitro endothelial potential of human UC blood-derived mesenchymal stem cells. Cytotherapy 8:215–227

    Article  PubMed  CAS  Google Scholar 

  313. Miao Z et al (2006) Isolation of mesenchymal stem cells from human placenta: comparison with human bone marrow mesenchymal stem cells. Cell Biol Int 30:681–687

    Article  PubMed  CAS  Google Scholar 

  314. Oswald J et al (2004) Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22:377–384

    Article  PubMed  Google Scholar 

  315. Cerqueira MT, Marques AP, Reis RL (2012) Using stem cells in skin regeneration: possibilities and reality. Stem Cells Dev 21:1201–1214

    Article  PubMed  CAS  Google Scholar 

  316. Colazzo F, Chester AH, Taylor PM, Yacoub MH (2010) Induction of mesenchymal to endothelial transformation of adipose-derived stem cells. J Heart Valve Dis 19:736–744

    PubMed  Google Scholar 

  317. Szoke K, Beckstrom KJ, Brinchmann JE (2012) Human adipose tissue as a source of cells with angiogenic potential. Cell Transplant 21:235–250

    PubMed  Google Scholar 

  318. Zimmerlin L et al (2010) Stromal vascular progenitors in adult human adipose tissue. Cytometry A 77:22–30

    PubMed  Google Scholar 

  319. Locke M, Feisst V, Dunbar PR (2011) Concise review: human adipose-derived stem cells: separating promise from clinical need. Stem Cells 29:404–411

    Article  PubMed  CAS  Google Scholar 

  320. Nakagami H et al (2005) Novel autologous cell therapy in ischemic limb disease through growth factor secretion by cultured adipose tissue-derived stromal cells. Arterioscler Thromb Vasc Biol 25:2542–2547

    Article  PubMed  CAS  Google Scholar 

  321. Moon MH et al (2006) Human adipose tissue-derived mesenchymal stem cells improve postnatal neovascularization in a mouse model of hindlimb ischemia. Cell Physiol Biochem 17:279–290

    Article  PubMed  CAS  Google Scholar 

  322. Schlosser S et al (2012) Paracrine effects of mesenchymal stem cells enhance vascular regeneration in ischemic murine skin. Microvasc Res 83:267–275

    Article  PubMed  CAS  Google Scholar 

  323. Roobrouck VD et al (2011) Differentiation potential of human postnatal mesenchymal stem cells, mesoangioblasts, and multipotent adult progenitor cells reflected in their transcriptome and partially influenced by the culture conditions. Stem Cells 29:871–882

    Article  PubMed  CAS  Google Scholar 

  324. Chamberlain G, Fox J, Ashton B, Middleton J (2007) Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25:2739–2749

    Article  PubMed  CAS  Google Scholar 

  325. Kinnaird T et al (2004) Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 94:678–685

    Article  PubMed  CAS  Google Scholar 

  326. Wu Y, Zhao RC, Tredget EE (2010) Concise review: bone marrow-derived stem/progenitor cells in cutaneous repair and regeneration. Stem Cells 28:905–915

    PubMed  CAS  Google Scholar 

  327. Yew TL et al (2011) Enhancement of wound healing by human multipotent stromal cell conditioned medium: the paracrine factors and p38 MAPK activation. Cell Transplant 20:693–706

    Article  PubMed  Google Scholar 

  328. Boomsma RA, Geenen DL (2012) Mesenchymal stem cells secrete multiple cytokines that promote angiogenesis and have contrasting effects on chemotaxis and apoptosis. PLoS One 7:e35685

    Article  PubMed  CAS  Google Scholar 

  329. Ghajar CM et al (2010) Mesenchymal cells stimulate capillary morphogenesis via distinct proteolytic mechanisms. Exp Cell Res 316:813–825

    Article  PubMed  CAS  Google Scholar 

  330. Kachgal S, Putnam AJ (2011) Mesenchymal stem cells from adipose and bone marrow promote angiogenesis via distinct cytokine and protease expression mechanisms. Angiogenesis 14:47–59

    Article  PubMed  CAS  Google Scholar 

  331. Lin RZ, Moreno-Luna R, Zhou B, Pu WT, Melero-Martin JM (2012) Equal modulation of endothelial cell function by four distinct tissue-specific mesenchymal stem cells. Angiogenesis 15:443–455

    Article  PubMed  Google Scholar 

  332. Amos PJ et al (2008) IFATS collection: the role of human adipose-derived stromal cells in inflammatory microvascular remodeling and evidence of a perivascular phenotype. Stem Cells 26:2682–2690

    Article  PubMed  CAS  Google Scholar 

  333. Crisan M et al (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301–313

    Article  PubMed  CAS  Google Scholar 

  334. Sacchetti B et al (2007) Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131:324–336

    Article  PubMed  CAS  Google Scholar 

  335. Traktuev DO et al (2008) A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res 102:77–85

    Article  PubMed  CAS  Google Scholar 

  336. Mulder GD, Lee DK, Jeppesen NS (2012) Comprehensive review of the clinical application of autologous mesenchymal stem cells in the treatment of chronic wounds and diabetic bone healing. Int Wound J 9:595–600

    Article  PubMed  Google Scholar 

  337. Brower J et al (2011) Mesenchymal stem cell therapy and delivery systems in nonhealing wounds. Adv Skin Wound Care 24:524–532; quiz 533–524

    Article  PubMed  Google Scholar 

  338. Falanga V et al (2007) Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. Tissue Eng 13:1299–1312

    Article  PubMed  CAS  Google Scholar 

  339. Kim EK, Li G, Lee TJ, Hong JP (2011) The effect of human adipose-derived stem cells on healing of ischemic wounds in a diabetic nude mouse model. Plast Reconstr Surg 128:387–394

    Article  PubMed  CAS  Google Scholar 

  340. Au P, Tam J, Fukumura D, Jain RK (2008) Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 111:4551–4558

    Article  PubMed  CAS  Google Scholar 

  341. Garcia-Olmo D et al (2005) A phase I clinical trial of the treatment of Crohn’s fistula by adipose mesenchymal stem cell transplantation. Dis Colon Rectum 48:1416–1423

    Article  PubMed  Google Scholar 

  342. Garcia-Olmo D et al (2009) Expanded adipose-derived stem cells for the treatment of complex perianal fistula: a phase II clinical trial. Dis Colon Rectum 52:79–86

    Article  PubMed  Google Scholar 

  343. Melero-Martin JM et al (2008) Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res 103:194–202

    Article  PubMed  CAS  Google Scholar 

  344. D’Ippolito G et al (2004) Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J Cell Sci 117:2971–2981

    Article  PubMed  CAS  Google Scholar 

  345. Jiang Y et al (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41–49

    Article  PubMed  CAS  Google Scholar 

  346. Yoon YS et al (2005) Clonally expanded novel multipotent stem cells from human bone marrow regenerate myocardium after myocardial infarction. J Clin Invest 115:326–338

    PubMed  CAS  Google Scholar 

  347. Sohni A, Verfaillie CM (2011) Multipotent adult progenitor cells. Best Pract Res Clin Haematol 24:3–11

    Article  PubMed  CAS  Google Scholar 

  348. Kogler G et al (2004) A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J Exp Med 200:123–135

    Article  PubMed  Google Scholar 

  349. Aranguren XL et al (2007) In vitro and in vivo arterial differentiation of human multipotent adult progenitor cells. Blood 109:2634–2642

    Article  PubMed  CAS  Google Scholar 

  350. Aranguren XL et al (2008) Multipotent adult progenitor cells sustain function of ischemic limbs in mice. J Clin Invest 118:505–514

    PubMed  CAS  Google Scholar 

  351. Reyes M et al (2002) Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest 109:337–346

    PubMed  CAS  Google Scholar 

  352. Ulloa-Montoya F et al (2007) Comparative transcriptome analysis of embryonic and adult stem cells with extended and limited differentiation capacity. Genome Biol 8:R163

    Article  PubMed  CAS  Google Scholar 

  353. Mahpatra S, Firpo MT, Bacanamwo M (2010) Inhibition of DNA methyltransferases and histone deacetylases induces bone marrow-derived multipotent adult progenitor cells to differentiate into endothelial cells. Ethn Dis 20:S1-60–S1-64

    Google Scholar 

  354. Highfill SL et al (2009) Multipotent adult progenitor cells can suppress graft-versus-host disease via prostaglandin E2 synthesis and only if localized to sites of allopriming. Blood 114:693–701

    Article  PubMed  CAS  Google Scholar 

  355. Luyckx A et al (2010) Mouse MAPC-mediated immunomodulation: cell-line dependent variation. Exp Hematol 38:1–2

    Article  PubMed  Google Scholar 

  356. Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154–156

    Article  PubMed  CAS  Google Scholar 

  357. Thomson JA et al (1998) Embryonic stem cell lines derived from human blastocysts. Science 282:1145–1147

    Article  PubMed  CAS  Google Scholar 

  358. Odorico JS, Kaufman DS, Thomson JA (2001) Multilineage differentiation from human embryonic stem cell lines. Stem Cells 19:193–204

    Article  PubMed  CAS  Google Scholar 

  359. Wang X et al (2012) MIF produced by bone marrow-derived macrophages contributes to teratoma progression after embryonic stem cell transplantation. Cancer Res 72:2867–2878

    Article  PubMed  CAS  Google Scholar 

  360. Moon SH et al (2011) A system for treating ischemic disease using human embryonic stem cell-derived endothelial cells without direct incorporation. Biomaterials 32:6445–6455

    Article  PubMed  CAS  Google Scholar 

  361. Jaenisch R (2004) Human cloning – the science and ethics of nuclear transplantation. N Engl J Med 351:2787–2791

    Article  PubMed  CAS  Google Scholar 

  362. Puymirat E et al (2009) Can mesenchymal stem cells induce tolerance to cotransplanted human embryonic stem cells? Mol Ther 17:176–182

    Article  PubMed  CAS  Google Scholar 

  363. Yamashita J et al (2000) Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408:92–96

    Article  PubMed  CAS  Google Scholar 

  364. Sone M et al (2007) Pathway for differentiation of human embryonic stem cells to vascular cell components and their potential for vascular regeneration. Arterioscler Thromb Vasc Biol 27:2127–2134

    Article  PubMed  CAS  Google Scholar 

  365. Yamahara K et al (2008) Augmentation of neovascularization [corrected] in hindlimb ischemia by combined transplantation of human embryonic stem cells-derived endothelial and mural cells. PLoS One 3:e1666

    Article  PubMed  CAS  Google Scholar 

  366. Descamps B, Emanueli C (2012) Vascular differentiation from embryonic stem cells: novel technologies and therapeutic promises. Vascul Pharmacol 56:267–279

    Article  PubMed  CAS  Google Scholar 

  367. Li Z, Han Z, Wu JC (2009) Transplantation of human embryonic stem cell-derived endothelial cells for vascular diseases. J Cell Biochem 106:194–199

    Article  PubMed  CAS  Google Scholar 

  368. Volz KS, Miljan E, Khoo A, Cooke JP (2012) Development of pluripotent stem cells for vascular therapy. Vascul Pharmacol 56:288–296

    Article  PubMed  CAS  Google Scholar 

  369. Hsiai TK, Wu JC (2008) Hemodynamic forces regulate embryonic stem cell commitment to vascular progenitors. Curr Cardiol Rev 4:269–274

    Article  PubMed  CAS  Google Scholar 

  370. Kane NM et al (2010) Derivation of endothelial cells from human embryonic stem cells by directed differentiation: analysis of microRNA and angiogenesis in vitro and in vivo. Arterioscler Thromb Vasc Biol 30:1389–1397

    Article  PubMed  CAS  Google Scholar 

  371. Lee AS et al (2009) Effects of cell number on teratoma formation by human embryonic stem cells. Cell Cycle 8:2608–2612

    Article  PubMed  CAS  Google Scholar 

  372. Tang C et al (2011) An antibody against SSEA-5 glycan on human pluripotent stem cells enables removal of teratoma-forming cells. Nat Biotechnol 29:829–834

    Article  PubMed  CAS  Google Scholar 

  373. Kalka C et al (2000) Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci USA 97:3422–3427

    Article  PubMed  CAS  Google Scholar 

  374. Yang C et al (2004) Enhancement of neovascularization with cord blood CD133+ cell-derived endothelial progenitor cell transplantation. Thromb Haemost 91:1202–1212

    PubMed  CAS  Google Scholar 

  375. Vatansever HS, Uluer ET, Aydede H, Ozbilgin MK (2013) Analysis of transferred keratinocyte-like cells derived from mouse embryonic stem cells on experimental surgical skin wounds of mouse. Acta Histochem 115:32–41

    Article  PubMed  Google Scholar 

  376. Lee MJ et al (2011) Enhancement of wound healing by secretory factors of endothelial precursor cells derived from human embryonic stem cells. Cytotherapy 13:165–178

    Article  PubMed  CAS  Google Scholar 

  377. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676

    Article  PubMed  CAS  Google Scholar 

  378. Yu J et al (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917–1920

    Article  PubMed  CAS  Google Scholar 

  379. Rolletschek A, Wobus AM (2009) Induced human pluripotent stem cells: promises and open questions. Biol Chem 390:845–849

    Article  PubMed  CAS  Google Scholar 

  380. Jia F et al (2010) A nonviral minicircle vector for deriving human iPS cells. Nat Methods 7:197–199

    Article  PubMed  CAS  Google Scholar 

  381. Li M, Chen M, Han W, Fu X (2010) How far are induced pluripotent stem cells from the clinic? Ageing Res Rev 9:257–264

    Article  PubMed  CAS  Google Scholar 

  382. Choi KD et al (2009) Hematopoietic and endothelial differentiation of human induced pluripotent stem cells. Stem Cells 27:559–567

    PubMed  CAS  Google Scholar 

  383. Narazaki G et al (2008) Directed and systematic differentiation of cardiovascular cells from mouse induced pluripotent stem cells. Circulation 118:498–506

    Article  PubMed  Google Scholar 

  384. Taura D et al (2009) Induction and isolation of vascular cells from human induced pluripotent stem cells – brief report. Arterioscler Thromb Vasc Biol 29:1100–1103

    Article  PubMed  CAS  Google Scholar 

  385. Rufaihah AJ et al (2011) Endothelial cells derived from human iPSCS increase capillary density and improve perfusion in a mouse model of peripheral arterial disease. Arterioscler Thromb Vasc Biol 31:e72–e79

    Article  PubMed  CAS  Google Scholar 

  386. Suzuki H et al (2010) Therapeutic angiogenesis by transplantation of induced pluripotent stem cell-derived Flk-1 positive cells. BMC Cell Biol 11:72

    Article  PubMed  CAS  Google Scholar 

  387. Iwaguro H et al (2002) Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation 105:732–738

    Article  PubMed  CAS  Google Scholar 

  388. Aranguren XL, Verfaillie CM, Luttun A (2009) Emerging hurdles in stem cell therapy for peripheral vascular disease. J Mol Med (Berl) 87(3–16)

    Google Scholar 

  389. Choudhery MS et al (2012) Bone marrow derived mesenchymal stem cells from aged mice have reduced wound healing, angiogenesis, proliferation and anti-apoptosis capabilities. Cell Biol Int 36:747–753

    Article  PubMed  CAS  Google Scholar 

  390. Di Rocco G et al (2010) Enhanced healing of diabetic wounds by topical administration of adipose tissue-derived stromal cells overexpressing stromal-derived factor-1: biodistribution and engraftment analysis by bioluminescent imaging. Stem Cells Int 2011:304562

    PubMed  Google Scholar 

  391. Pasha Z et al (2008) Preconditioning enhances cell survival and differentiation of stem cells during transplantation in infarcted myocardium. Cardiovasc Res 77:134–142

    Article  PubMed  CAS  Google Scholar 

  392. Marrotte EJ, Chen DD, Hakim JS, Chen AF (2010) Manganese superoxide dismutase expression in endothelial progenitor cells accelerates wound healing in diabetic mice. J Clin Invest 120:4207–4219

    Article  PubMed  CAS  Google Scholar 

  393. Song SH et al (2012) Genetic modification of human adipose-derived stem cells for promoting wound healing. J Dermatol Sci 66:98–107

    Article  PubMed  CAS  Google Scholar 

  394. Lu D et al (2012) Peroxisome proliferator-activated receptor-gamma coactivator-1alpha (PGC-1alpha) enhances engraftment and angiogenesis of mesenchymal stem cells in diabetic hindlimb ischemia. Diabetes 61:1153–1159

    Article  PubMed  CAS  Google Scholar 

  395. Barzilay R, Melamed E, Offen D (2009) Introducing transcription factors to multipotent mesenchymal stem cells: making transdifferentiation possible. Stem Cells 27:2509–2515

    Article  PubMed  CAS  Google Scholar 

  396. Duffy GP et al (2010) Mesenchymal stem cells overexpressing ephrin-b2 rapidly adopt an early endothelial phenotype with simultaneous reduction of osteogenic potential. Tissue Eng Part A 16:2755–2768

    Article  PubMed  CAS  Google Scholar 

  397. Dufourcq P et al (2008) Secreted frizzled-related protein-1 enhances mesenchymal stem cell function in angiogenesis and contributes to neovessel maturation. Stem Cells 26:2991–3001

    Article  PubMed  CAS  Google Scholar 

  398. Moues CM, Heule F, Hovius SE (2011) A review of topical negative pressure therapy in wound healing: sufficient evidence? Am J Surg 201:544–556

    Article  PubMed  CAS  Google Scholar 

  399. Labler L et al (2009) Vacuum-assisted closure therapy increases local interleukin-8 and vascular endothelial growth factor levels in traumatic wounds. J Trauma 66:749–757

    Article  PubMed  CAS  Google Scholar 

  400. Labanaris AP, Polykandriotis E, Horch RE (2009) The effect of vacuum-assisted closure on lymph vessels in chronic wounds. J Plast Reconstr Aesthet Surg 62:1068–1075

    Article  PubMed  Google Scholar 

  401. Costin GE, Birlea SA, Norris DA (2012) Trends in wound repair: cellular and molecular basis of regenerative therapy using electromagnetic fields. Curr Mol Med 12:14–26

    Article  PubMed  CAS  Google Scholar 

  402. Callaghan MJ et al (2008) Pulsed electromagnetic fields accelerate normal and diabetic wound healing by increasing endogenous FGF-2 release. Plast Reconstr Surg 121:130–141

    Article  PubMed  CAS  Google Scholar 

  403. Sebastian A et al (2011) Acceleration of cutaneous healing by electrical stimulation: degenerate electrical waveform down-regulates inflammation, up-regulates angiogenesis and advances remodeling in temporal punch biopsies in a human volunteer study. Wound Repair Regen 19:693–708

    Article  PubMed  Google Scholar 

  404. MacNeil S (2007) Progress and opportunities for tissue-engineered skin. Nature 445:874–880

    Article  PubMed  CAS  Google Scholar 

  405. Groeber F, Holeiter M, Hampel M, Hinderer S, Schenke-Layland K (2011) Skin tissue engineering – in vivo and in vitro applications. Adv Drug Deliv Rev 63:352–366

    Article  PubMed  CAS  Google Scholar 

  406. Griffith CK et al (2005) Diffusion limits of an in vitro thick prevascularized tissue. Tissue Eng 11:257–266

    Article  PubMed  CAS  Google Scholar 

  407. Papavasiliou G, Cheng MH, Brey EM (2010) Strategies for vascularization of polymer scaffolds. J Investig Med 58:838–844

    PubMed  CAS  Google Scholar 

  408. Glotzbach JP, Wong VW, Gurtner GC, Longaker MT (2011) Regenerative medicine. Curr Probl Surg 48:148–212

    Article  PubMed  Google Scholar 

  409. Phelps EA, Garcia AJ (2010) Engineering more than a cell: vascularization strategies in tissue engineering. Curr Opin Biotechnol 21:704–709

    Article  PubMed  CAS  Google Scholar 

  410. Sarkar A, Tatlidede S, Scherer SS, Orgill DP, Berthiaume F (2011) Combination of stromal cell-derived factor-1 and collagen-glycosaminoglycan scaffold delays contraction and accelerates reepithelialization of dermal wounds in wild-type mice. Wound Repair Regen 19:71–79

    Article  PubMed  Google Scholar 

  411. Lugo LM, Lei P, Andreadis ST (2011) Vascularization of the dermal support enhances wound re-epithelialization by in situ delivery of epidermal keratinocytes. Tissue Eng Part A 17:665–675

    Article  PubMed  CAS  Google Scholar 

  412. Supp DM, Boyce ST (2002) Overexpression of vascular endothelial growth factor accelerates early vascularization and improves healing of genetically modified cultured skin substitutes. J Burn Care Rehabil 23:10–20

    Article  PubMed  Google Scholar 

  413. Erdag G, Medalie DA, Rakhorst H, Krueger GG, Morgan JR (2004) FGF-7 expression enhances the performance of bioengineered skin. Mol Ther 10:76–85

    Article  PubMed  CAS  Google Scholar 

  414. Tremblay PL, Hudon V, Berthod F, Germain L, Auger FA (2005) Inosculation of tissue-engineered capillaries with the host’s vasculature in a reconstructed skin transplanted on mice. Am J Transplant 5:1002–1010

    Article  PubMed  Google Scholar 

  415. Halbleib M, Skurk T, de Luca C, von Heimburg D, Hauner H (2003) Tissue engineering of white adipose tissue using hyaluronic acid-based scaffolds. I: in vitro differentiation of human adipocyte precursor cells on scaffolds. Biomaterials 24:3125–3132

    Article  PubMed  CAS  Google Scholar 

  416. Burg KJ et al (2000) Comparative study of seeding methods for three-dimensional polymeric scaffolds. J Biomed Mater Res 52:576

    Article  PubMed  CAS  Google Scholar 

  417. Lawrence BJ, Madihally SV (2008) Cell colonization in degradable 3D porous matrices. Cell Adh Migr 2:9–16

    Article  PubMed  Google Scholar 

  418. Kannan RY, Salacinski HJ, Sales K, Butler P, Seifalian AM (2005) The roles of tissue engineering and vascularisation in the development of micro-vascular networks: a review. Biomaterials 26:1857–1875

    Article  PubMed  CAS  Google Scholar 

  419. Calcagni M et al (2011) In vivo visualization of the origination of skin graft vasculature in a wild-type/GFP crossover model. Microvasc Res 82:237–245

    PubMed  Google Scholar 

  420. Tonello C et al (2003) In vitro reconstruction of human dermal equivalent enriched with endothelial cells. Biomaterials 24:1205–1211

    Article  PubMed  CAS  Google Scholar 

  421. Black AF, Berthod F, L’Heureux N, Germain L, Auger FA (1998) In vitro reconstruction of a human capillary-like network in a tissue-engineered skin equivalent. FASEB J 12:1331–1340

    PubMed  CAS  Google Scholar 

  422. Hudon V et al (2003) A tissue-engineered endothelialized dermis to study the modulation of angiogenic and angiostatic molecules on capillary-like tube formation in vitro. Br J Dermatol 148:1094–1104

    Article  PubMed  CAS  Google Scholar 

  423. Schechner JS et al (2003) Engraftment of a vascularized human skin equivalent. FASEB J 17:2250–2256

    Article  PubMed  CAS  Google Scholar 

  424. Sarkanen JR et al (2012) Adipose stromal cell tubule network model provides a versatile tool for vascular research and tissue engineering. Cells Tissues Organs 196:385–397

    Article  PubMed  CAS  Google Scholar 

  425. Verseijden F et al (2012) Vascularization of prevascularized and non-prevascularized fibrin-based human adipose tissue constructs after implantation in nude mice. J Tissue Eng Regen Med 6:169–178

    Article  PubMed  CAS  Google Scholar 

  426. Frerich B, Winter K, Scheller K, Braumann UD (2012) Comparison of different fabrication techniques for human adipose tissue engineering in severe combined immunodeficient mice. Artif Organs 36:227–237

    Article  PubMed  CAS  Google Scholar 

  427. Wu X et al (2004) Tissue-engineered microvessels on three-dimensional biodegradable scaffolds using human endothelial progenitor cells. Am J Physiol Heart Circ Physiol 287:H480–H487

    Article  PubMed  CAS  Google Scholar 

  428. Sieminski AL, Hebbel RP, Gooch KJ (2005) Improved microvascular network in vitro by human blood outgrowth endothelial cells relative to vessel-derived endothelial cells. Tissue Eng 11:1332–1345

    Article  PubMed  CAS  Google Scholar 

  429. Melero-Martin JM et al (2007) In vivo vasculogenic potential of human blood-derived endothelial progenitor cells. Blood 109:4761–4768

    Article  PubMed  CAS  Google Scholar 

  430. Thebaud NB et al (2010) Human progenitor-derived endothelial cells vs. venous endothelial cells for vascular tissue engineering: an in vitro study. J Tissue Eng Regen Med 4:473–484

    PubMed  CAS  Google Scholar 

  431. Kung EF, Wang F, Schechner JS (2008) In vivo perfusion of human skin substitutes with microvessels formed by adult circulating endothelial progenitor cells. Dermatol Surg 34:137–146

    Article  PubMed  CAS  Google Scholar 

  432. Mujaj S, Manton K, Upton Z, Richards S (2010) Serum-free primary human fibroblast and keratinocyte coculture. Tissue Eng Part A 16:1407–1420

    Article  PubMed  CAS  Google Scholar 

  433. Markowicz M et al (2006) Human bone marrow mesenchymal stem cells seeded on modified collagen improved dermal regeneration in vivo. Cell Transplant 15:723–732

    Article  PubMed  Google Scholar 

  434. Liu P et al (2008) Tissue-engineered skin containing mesenchymal stem cells improves burn wounds. Artif Organs 32:925–931

    Article  PubMed  Google Scholar 

  435. Liu S et al (2011) Synergistic angiogenesis promoting effects of extracellular matrix scaffolds and adipose-derived stem cells during wound repair. Tissue Eng Part A 17:725–739

    Article  PubMed  CAS  Google Scholar 

  436. Zografou A et al (2011) Improvement of skin-graft survival after autologous transplantation of adipose-derived stem cells in rats. J Plast Reconstr Aesthet Surg 64:1647–1656

    Article  PubMed  CAS  Google Scholar 

  437. Altman AM et al (2008) Dermal matrix as a carrier for in vivo delivery of human adipose-derived stem cells. Biomaterials 29:1431–1442

    Article  PubMed  CAS  Google Scholar 

  438. Altman AM et al (2009) IFATS collection: human adipose-derived stem cells seeded on a silk fibroin-chitosan scaffold enhance wound repair in a murine soft tissue injury model. Stem Cells 27:250–258

    Article  PubMed  CAS  Google Scholar 

  439. Rustad KC et al (2012) Enhancement of mesenchymal stem cell angiogenic capacity and stemness by a biomimetic hydrogel scaffold. Biomaterials 33:80–90

    Article  PubMed  CAS  Google Scholar 

  440. Inoue H et al (2008) Bioimaging assessment and effect of skin wound healing using bone-marrow-derived mesenchymal stromal cells with the artificial dermis in diabetic rats. J Biomed Opt 13:064036

    Article  PubMed  CAS  Google Scholar 

  441. Vojtassak J et al (2006) Autologous biograft and mesenchymal stem cells in treatment of the diabetic foot. Neuro Endocrinol Lett 27(Suppl 2):134–137

    PubMed  Google Scholar 

  442. Levenberg S, Golub JS, Amit M, Itskovitz-Eldor J, Langer R (2002) Endothelial cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 99:4391–4396

    Article  PubMed  CAS  Google Scholar 

  443. Levenberg S et al (2005) Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23:879–884

    Article  PubMed  CAS  Google Scholar 

  444. Shen G et al (2003) Tissue engineering of blood vessels with endothelial cells differentiated from mouse embryonic stem cells. Cell Res 13:335–341

    Article  PubMed  Google Scholar 

  445. Huang H et al (2005) Differentiation from embryonic stem cells to vascular wall cells under in vitro pulsatile flow loading. J Artif Organs 8:110–118

    Article  PubMed  Google Scholar 

  446. Nourse MB et al (2010) VEGF induces differentiation of functional endothelium from human embryonic stem cells: implications for tissue engineering. Arterioscler Thromb Vasc Biol 30:80–89

    Article  PubMed  CAS  Google Scholar 

  447. Kraehenbuehl TP et al (2011) Human embryonic stem cell-derived microvascular grafts for cardiac tissue preservation after myocardial infarction. Biomaterials 32:1102–1109

    Article  PubMed  CAS  Google Scholar 

  448. Lammers G et al (2011) An overview of methods for the in vivo evaluation of tissue-engineered skin constructs. Tissue Eng Part B Rev 17:33–55

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cardiovascular Sciences, Molecular and Vascular Biology Research Unit, KU Leuven, Leuven, Belgium

    Benoit Hendrickx MD, PhD & Kristoff Verdonck MD

  2. Department of Development and Regeneration, Cell and Gene Therapy Applications Research Unit, Katholieke Universiteit Leuven, University Hospitals, Herestraat 49, Leuven, B-3000, Belgium

    Benoit Hendrickx MD, PhD, Margot Den Hondt MD & Jan J. Vranckx MD, PhD

  3. Department of Cardiovascular Sciences, Molecular and Vascular Biology Research Unit, Endothelial Cell Biology Unit, Katholieke Universiteit Leuven, Campus Gasthuisberg, Onderwijs & Navorsing 1, Herestraat 49, B-3000, Leuven, Belgium

    Aernout Luttun PhD

Authors
  1. Benoit Hendrickx MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Margot Den Hondt MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kristoff Verdonck MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jan J. Vranckx MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aernout Luttun PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jan J. Vranckx MD, PhD or Aernout Luttun PhD .

Editor information

Editors and Affiliations

  1. Pharmaceutical Sciences, Douglas Hall 206, Chicago State University, S. King Drive 9501, Chicago, 60628, Illinois, USA

    Michael K. Danquah

  2. Health Science Center, Dept. Pharmaceutical &, University of Tennessee, S. Manassas 19, Memphis, 38103, Tennessee, USA

    Ram I. Mahato

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Hendrickx, B., Hondt, M.D., Verdonck, K., Vranckx, J.J., Luttun, A. (2013). Cell and Gene Transfer Strategies for Vascularization During Skin Wound Healing. In: Danquah, M., Mahato, R. (eds) Emerging Trends in Cell and Gene Therapy. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-62703-417-3_26

Download citation

Publish with us

Policies and ethics

Search

Navigation