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Biochemical Basis and Therapeutic Implications of Angiogenesis pp 285–311Cite as

Adipose Tissue-Derived Mesenchymal Stem Cell and Angiogenesis in Ischemic Heart Disease

Part of the Advances in Biochemistry in Health and Disease book series (ABHD,volume 6)

Abstract

Acute myocardial infarction is one of the most important causes of death and disability worldwide. The limited capacity of the adult heart to self-regenerate and revascularize the ischemic damaged tissue leads to tissue loss, ventricular remodeling, and persistent deterioration in cardiac performance increasing the frequency of heart failure. Over the last several years, adult stem cells have appeared as one of the novel promising therapeutic approaches for the treatment of ischemic heart disease. However, the quest for the best cell type is still ongoing. This ideal cell type should be capable of differentiating into functional cardiomyocytes and of forming new vessels to nourish the damaged area. Recent studies have shown that adipose tissue contains multipotent stem cells (the so-called adipose tissue-derived stem cells or ASC) that are capable of regenerating injured myocardium by differentiating into cardiac resident cells or by secreting multiple angiogenic growth factors (paracrine effects). Moreover, due to ease of harvesting these cells in large numbers and low immunogenicity, white adipose tissue has become an attractive stem cell source. In this chapter, we review the principal characteristics of ASC as well as their capacity to repair cardiac damage in the setting of ischemic heart disease as compared with other adult stem cells, with special attention to their pro-­angiogenic mechanisms of action.

Keywords

  • Cell therapy
  • Adipose tissue-derived stem cells
  • Myocardial ­infarction
  • Angiogenesis
  • Cytokines

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  • DOI: 10.1007/978-1-4614-5857-9_16
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Fig. 16.1
Fig. 16.2
Fig. 16.3

References

  1. Armstrong L, Lako M, Buckley N et al (2012) Editorial: our top 10 developments in stem cell biology over the last 30 years. Stem Cells 30:2–9

    PubMed  CAS  Google Scholar 

  2. Daher SR, Johnstone BH, Phinney DG, March KL (2008) Adipose stromal/stem cells: basic and translational advances: the IFATS collection. Stem Cells 26:2664–2665

    PubMed  Google Scholar 

  3. Uccelli A, Moretta L, Pistoia V (2008) Mesenchymal stem cells in health and disease. Nat Rev Immunol 8:726–736

    PubMed  CAS  Google Scholar 

  4. Bianco P, Robey PG, Simmons PJ (2008) Mesenchymal stem cells: revisiting history, ­concepts, and assays. Cell Stem Cell 2:313–319

    PubMed  CAS  Google Scholar 

  5. Ranganath SH, Levy O, Inamdar MS, Karp JM (2012) Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell 10:244–258

    PubMed  CAS  Google Scholar 

  6. Dominici M, Le Blanc K, Mueller I et al (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315–317

    PubMed  CAS  Google Scholar 

  7. Horwitz EM, Dominici M (2008) How do mesenchymal stromal cells exert their therapeutic benefit? Cytotherapy 10:771–774

    PubMed  CAS  Google Scholar 

  8. Nadri S, Soleimani M (2007) Comparative analysis of mesenchymal stromal cells from murine bone marrow and amniotic fluid. Cytotherapy 9:729–737

    PubMed  CAS  Google Scholar 

  9. Zuk PA, Zhu M, Ashjian P et al (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279–4295

    PubMed  CAS  Google Scholar 

  10. Shih DT, Lee DC, Chen SC et al (2005) Isolation and characterization of neurogenic mesenchymal stem cells in human scalp tissue. Stem Cells 23:1012–1020

    PubMed  CAS  Google Scholar 

  11. Sarugaser R, Lickorish D, Baksh D et al (2005) Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells 23:220–229

    PubMed  Google Scholar 

  12. Mazo M, Gavira JJ, Pelacho B, Prosper F (2011) Adipose-derived stem cells for myocardial infarction. J Cardiovasc Transl Res 4:145–153

    PubMed  Google Scholar 

  13. Fraser JK, Wulur I, Alfonso Z, Hedrick MH (2006) Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol 24:150–154

    PubMed  CAS  Google Scholar 

  14. Strawford A, Antelo F, Christiansen M, Hellerstein MK (2004) Adipose tissue triglyceride turnover, de novo lipogenesis, and cell proliferation in humans measured with 2H2O. Am J Physiol 286:E577–E588

    CAS  Google Scholar 

  15. Zuk PA, Zhu M, Mizuno H et al (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211–228

    PubMed  CAS  Google Scholar 

  16. Schaffler A, Buchler C (2007) Concise review: adipose tissue-derived stromal cells—basic and clinical implications for novel cell-based therapies. Stem Cells 25:818–827

    PubMed  CAS  Google Scholar 

  17. Miyahara Y, Nagaya N, Kataoka M et al (2006) Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 12:459–465

    PubMed  Google Scholar 

  18. Williams KJ, Picou AA, Kish SL et al (2008) Isolation and characterization of porcine adipose tissue-derived adult stem cells. Cells Tissues Organs 188:251–258

    PubMed  Google Scholar 

  19. De Ugarte DA, Alfonso Z, Zuk PA et al (2003) Differential expression of stem cell mobilization-associated molecules on multi-lineage cells from adipose tissue and bone marrow. Immunol Lett 89:267–270

    PubMed  CAS  Google Scholar 

  20. Puissant B, Barreau C, Bourin P et al (2005) Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol 129:118–129

    PubMed  Google Scholar 

  21. Rodriguez AM, Pisani D, Dechesne CA et al (2005) Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent mdx mouse. J Exp Med 201:1397–1405

    PubMed  CAS  Google Scholar 

  22. Jurgens WJ, Oedayrajsingh-Varma MJ, Helder MN et al (2008) Effect of tissue-harvesting site on yield of stem cells derived from adipose tissue: implications for cell-based therapies. Cell Tissue Res 332:415–426

    PubMed  CAS  Google Scholar 

  23. Fraser JK, Schreiber R, Strem B et al (2006) Plasticity of human adipose stem cells toward endothelial cells and cardiomyocytes. Nat Clin Pract Cardiovasc Med 3(suppl 1):S33–S37

    PubMed  CAS  Google Scholar 

  24. Nakagami H, Morishita R, Maeda K et al (2006) Adipose tissue-derived stromal cells as a novel option for regenerative cell therapy. J Atheroscler Thromb 13:77–81

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  26. Djouad F, Plence P, Bony C et al (2003) Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 102:3837–3844

    PubMed  Google Scholar 

  27. Nakagami H, Maeda K, Morishita R 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

    PubMed  Google Scholar 

  28. Bensinger W, Singer J, Appelbaum F et al (1993) Autologous transplantation with peripheral blood mononuclear cells collected after administration of recombinant granulocyte stimulating factor. Blood 81:3158–3163

    PubMed  CAS  Google Scholar 

  29. Asahara T, Murohara T, Sullivan A et al (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964–967

    PubMed  Google Scholar 

  30. Gronthos S, Franklin DM, Leddy HA et al (2001) Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 189:54–63

    PubMed  Google Scholar 

  31. Festy F, Hoareau L, Bes-Houtmann S et al (2005) Surface protein expression between human adipose tissue-derived stromal cells and mature adipocytes. Histochem Cell Biol 124:113–121

    PubMed  Google Scholar 

  32. Rehman J, Traktuev D, Li J et al (2004) Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 109:1292–1298

    PubMed  CAS  Google Scholar 

  33. Kern S, Eichler H, Stoeve J et al (2006) Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24:1294–1301

    PubMed  CAS  Google Scholar 

  34. Hombach-Klonisch S, Panigrahi S, Rashedi I et al (2008) Adult stem cells and their ­transdifferentiation potential-perspectives and therapeutic applications. J Mol Med 86(12):1301–1314

    PubMed  Google Scholar 

  35. Sanz-Ruiz R, Fernandez-Santos E, Dominguez-Munoa M et al (2009) Early translation of adipose-derived cell therapy for cardiovascular disease. Cell Transplant 18:245–254

    PubMed  CAS  Google Scholar 

  36. Casteilla L, Planat-Benard V, Cousin B et al (2005) Plasticity of adipose tissue: a promising therapeutic avenue in the treatment of cardiovascular and blood diseases? Arch Mal Coeur Vaiss 98:922–926

    PubMed  CAS  Google Scholar 

  37. Oedayrajsingh-Varma MJ, van Ham SM, Knippenberg M et al (2006) Adipose tissue-derived mesenchymal stem cell yield and growth characteristics are affected by the tissue-harvesting procedure. Cytotherapy 8:166–177

    PubMed  CAS  Google Scholar 

  38. Martínez-González J, Viñals M et al (1997) Mevalonate deprivation impairs IGF-I/insulin signaling in human vascular smooth cells. Atherosclerosis 135:213–223

    PubMed  CAS  Google Scholar 

  39. Bai X, Alt E (2010) Myocardial regeneration potential of adipose tissue-derived stem cells. Biochem Biophys Res Commun 401:321–326

    PubMed  CAS  Google Scholar 

  40. Sanz-Ruiz R, Santos ME, Munoa MD et al (2008) Adipose tissue-derived stem cells: the friendly side of a classic cardiovascular foe. J Cardiovasc Transl Res 1:55–63

    PubMed  Google Scholar 

  41. Rodriguez AM, Elabd C, Amri E-Z et al (2005) The human adipose tissue is a source of multipotent stem cells. Biochimie 87:125–128

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  43. Fuster V, Badimon L, Badimon JJ, Chesebro JH (1992) The pathogenesis of coronary artery disease and the acute coronary syndromes (1). N Engl J Med 326:242–250

    PubMed  CAS  Google Scholar 

  44. Fuster V, Badimon L, Badimon JJ, Chesebro JH (1992) The pathogenesis of coronary artery disease and the acute coronary syndromes (2). N Engl J Med 326:310–318

    PubMed  CAS  Google Scholar 

  45. Beltrami AP, Urbanek K, Kajstura J et al (2001) Evidence that human cardiac myocytes divide after myocardial infarction. N Engl J Med 344:1750–1757

    PubMed  CAS  Google Scholar 

  46. Condorelli G, Borello U, De Angelis L et al (2001) Cardiomyocytes induce endothelial cells to trans-differentiate into cardiac muscle: implications for myocardium regeneration. Proc Natl Acad Sci U S A 98:10733–10738

    PubMed  CAS  Google Scholar 

  47. Kudo M, Wang Y, Wani MA et al (2003) Implantation of bone marrow stem cells reduces the infarction and fibrosis in ischemic mouse heart. J Mol Cell Cardiol 35:1113–1119

    PubMed  CAS  Google Scholar 

  48. Smart N, Riley PR (2008) The stem cell movement. Circ Res 102:1155–1168

    PubMed  CAS  Google Scholar 

  49. Sanchez PL, Villa A, Sanz R et al (2007) Present and future of stem cells for cardiovascular therapy. Ann Med 39:412–427

    PubMed  CAS  Google Scholar 

  50. Orlic D, Kajstura J, Chimenti S et al (2001) Bone marrow cells regenerate infarcted myocardium. Nature 410:701–705

    PubMed  CAS  Google Scholar 

  51. Murry CE, Soonpaa MH, Reinecke H et al (2004) Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428:664–668

    PubMed  CAS  Google Scholar 

  52. Balsam LB, Wagers AJ, Christensen JL et al (2004) Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428:668–673

    PubMed  CAS  Google Scholar 

  53. Miller-Kasprzak E, Jagodzinski PP (2007) Endothelial progenitor cells as a new agent contributing to vascular repair. Arch Immunol Ther Exp 55:247–259

    CAS  Google Scholar 

  54. Rubart M, Field LJ (2006) Cardiac regeneration: repopulating the heart. Annu Rev Physiol 68:29–49

    PubMed  CAS  Google Scholar 

  55. Narmoneva DA, Vukmirovic R, Davis ME et al (2004) Endothelial cells promote cardiac myocyte survival and spatial reorganization: implications for cardiac regeneration. Circulation 110:962–968

    PubMed  Google Scholar 

  56. Makino S, Fukuda K, Miyoshi S et al (1999) Cardiomyocytes can be generated from marrow stromal cells in vitro. J Clin Invest 103:697–705

    PubMed  CAS  Google Scholar 

  57. Pittenger MF, Mackay AM, Beck SC et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147

    PubMed  CAS  Google Scholar 

  58. Murry CE, Field LJ, Menasche P (2005) Cell-based cardiac repair: reflections at the 10-year point. Circulation 112:3174–3183

    PubMed  Google Scholar 

  59. Menasche P (2007) Skeletal myoblasts as a therapeutic agent. Prog Cardiovasc Dis 50:7–17

    PubMed  Google Scholar 

  60. Shi X, Garry DJ (2006) Muscle stem cells in development, regeneration, and disease. Genes Dev 20:1692–1708

    PubMed  CAS  Google Scholar 

  61. Dowell JD, Rubart M, Pasumarthi KBS et al (2003) Myocyte and myogenic stem cell transplantation in the heart. Cardiovasc Res 58:336–350

    PubMed  CAS  Google Scholar 

  62. Laflamme MA, Murry CE (2005) Regenerating the heart. Nat Biotechnol 23:845–856

    PubMed  CAS  Google Scholar 

  63. Aicher A, Brenner W, Zuhayra M et al (2003) Assessment of the tissue distribution of ­transplanted human endothelial progenitor cells by radioactive labeling. Circulation 107:2134–2139

    PubMed  Google Scholar 

  64. Dimmeler S, Zeiher AM, Schneider MD (2005) Unchain my heart: the scientific foundations of cardiac repair. J Clin Invest 115:572–583

    PubMed  CAS  Google Scholar 

  65. Menasche P, Hagege AA, Vilquin JT et al (2003) Autologous skeletal myoblast transplantation for severe postinfarction left ventricular dysfunction. J Am Coll Cardiol 41:1078–1083

    PubMed  Google Scholar 

  66. Menasche P, Alfieri O, Janssens S et al (2008) The myoblast autologous grafting in ischemic cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantation. Circulation 117:1189–1200

    PubMed  Google Scholar 

  67. Barile L, Messina E, Giacomello A, Marban E (2007) Endogenous cardiac stem cells. Prog Cardiovasc Dis 50:31–48

    PubMed  CAS  Google Scholar 

  68. Oh H, Bradfute SB, Gallardo TD et al (2003) Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A 100:12313–12318

    PubMed  CAS  Google Scholar 

  69. Oettgen P (2006) Cardiac stem cell therapy: need for optimization of efficacy and safety monitoring. Circulation 114:353–358

    PubMed  Google Scholar 

  70. Wang JS, Shum-Tim D, Galipeau J et al (2000) Marrow stromal cells for cellular cardiomyoplasty: feasibility and potential clinical advantages. J Thorac Cardiovasc Surg 120:999–1005

    PubMed  CAS  Google Scholar 

  71. Wakitani S, Saito T, Caplan AI (1995) Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve 18:1417–1426

    PubMed  CAS  Google Scholar 

  72. Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71–74

    PubMed  CAS  Google Scholar 

  73. Nagaya N, Fujii T, Iwase T et al (2004) Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis. Am J Physiol Heart Circ Physiol 287:H2670–H2676

    PubMed  CAS  Google Scholar 

  74. Strem BM, Zhu M, Alfonso Z et al (2005) Expression of cardiomyocytic markers on adipose tissue-derived cells in a murine model of acute myocardial injury. Cytotherapy 7:282–291

    PubMed  CAS  Google Scholar 

  75. Strem BM, Jordan M, Kim J, Yang J, Anderson CD, Daniels E (2005) Adipose tissue-derived stem cells enhance cardiac function following surgically-induced myocardial infarction. Circulation 112(suppl II):274

    Google Scholar 

  76. Mazo M, Planat-Bénard V, Abizanda G et al (2008) Transplantation of adipose derived stromal cells is associated with functional improvement in a rat model of chronic myocardial infarction. Eur J Heart Fail 10:454–462

    PubMed  CAS  Google Scholar 

  77. Cai L, Johnstone BH, Cook TG et al (2009) IFATS collection: human adipose tissue-derived stem cells induce angiogenesis and nerve sprouting following myocardial infarction, in conjunction with potent preservation of cardiac function. Stem Cells 27:230–237

    PubMed  CAS  Google Scholar 

  78. Léobon B, Roncalli J, Joffre C et al (2009) Adipose-derived cardiomyogenic cells: in vitro expansion and functional improvement in a mouse model of myocardial infarction. Cardiovasc Res 83:757–767

    PubMed  CAS  Google Scholar 

  79. Schenke-Layland K, Strem BM, Jordan MC et al (2009) Adipose tissue-derived cells improve cardiac function following myocardial infarction. J Surg Res 153:217–223

    PubMed  CAS  Google Scholar 

  80. van der Bogt KE, Schrepfer S, Yu J et al (2009) Comparison of transplantation of adipose tissue- and bone marrow-derived mesenchymal stem cells in the infarcted heart. Transplantation 87:642–652

    PubMed  CAS  Google Scholar 

  81. Wang L, Deng J, Tian W et al (2009) Adipose-derived stem cells are an effective cell candidate for treatment of heart failure: an MR imaging study of rat hearts. Am J Physiol Heart Circ Physiol 297:H1020–H1031

    PubMed  CAS  Google Scholar 

  82. Zhu XY, Zhang XZ, Xu L et al (2009) Transplantation of adipose-derived stem cells overexpressing hHGF into cardiac tissue. Biochem Biophys Res Commun 379:1084–1090

    PubMed  CAS  Google Scholar 

  83. Bai X, Yan Y, Song YH et al (2010) Both cultured and freshly isolated adipose tissue-derived stem cells enhance cardiac function after acute myocardial infarction. Eur Heart J 31:489–501

    PubMed  CAS  Google Scholar 

  84. Bayes-Genis A, Soler-Botija C, Farré J et al (2010) Human progenitor cells derived from cardiac adipose tissue ameliorate myocardial infarction in rodents. J Mol Cell Cardiol 49:771–780

    PubMed  Google Scholar 

  85. Danoviz ME, Nakamuta JS, Marques FL et al (2010) Rat adipose tissue-derived stem cells transplantation attenuates cardiac dysfunction post infarction and biopolymers enhance cell retention. PLoS One 5:e12077

    PubMed  Google Scholar 

  86. Lin YC, Leu S, Sun CK et al (2010) Early combined treatment with sildenafil and adiposederived mesenchymal stem cells preserves heart function in rat dilated cardiomyopathy. J Transl Med 8:88

    PubMed  CAS  Google Scholar 

  87. Okura H, Matsuyama A, Lee CM et al (2010) Cardiomyoblast-like cells differentiated from human adipose tissue-derived mesenchymal stem cells improve left ventricular dysfunction and survival in a rat myocardial infarction model. Tissue Eng Part C Methods 16:417–425

    PubMed  CAS  Google Scholar 

  88. Zhang X, Wang H, Ma X et al (2010) Preservation of the cardiac function in infarcted rat hearts by the transplantation of adipose-derived stem cells with injectable fibrin scaffolds. Exp Biol Med (Maywood) 235:1505–1515

    PubMed  CAS  Google Scholar 

  89. Bai X, Yan Y, Caleman M et al (2011) Tracking long-term survival of intramyocardially delivered human adipose tissue-derived stem cells using bioluminescence imaging. Mol Imaging Biol 13:633–645

    PubMed  CAS  Google Scholar 

  90. Berardi GR, Rebelatto CK, Tavares HF et al (2011) Transplantation of SNAP-treated adipose tissue-derived stem cells improves cardiac function and induces neovascularization after myocardium infarct in rats. Exp Mol Pathol 90:149–156

    PubMed  CAS  Google Scholar 

  91. Cai A, Zheng D, Dong Y et al (2011) Efficacy of Atorvastatin combined with adipose-derived mesenchymal stem cell transplantation on cardiac function in rats with acute myocardial infarction. Acta Biochim Biophys Sin (Shanghai) 43:857–866

    PubMed  CAS  Google Scholar 

  92. Gaebel R, Furlani D, Sorg H et al (2011) Cell origin of human mesenchymal stem cells determines a different healing performance in cardiac regeneration. PLoS One 6:e15652

    PubMed  CAS  Google Scholar 

  93. Hamdi H, Planat-Benard V, Bel A et al (2011) Epicardial adipose stem cell sheets results in greater post-infarction survival than intramyocardial injections. Cardiovasc Res 91:483–491

    PubMed  CAS  Google Scholar 

  94. Ii M, Horii M, Yokoyama A et al (2011) Synergistic effect of adiposederived stem cell therapy and bone marrow progenitor recruitment in ischemic heart. Lab Invest 91:539–552

    PubMed  CAS  Google Scholar 

  95. Paul A, Srivastava S, Cheng G et al (2011) Functional assessment of adipose stem cells for xenotransplantation using myocardial. Infarction immunocompetent models: comparison with bone marrow stem cells. Cell Biochem Biophys [Epub ahead of print]

    PubMed  Google Scholar 

  96. van Dijk A, Naaijkens BA, Jurgens WJ et al (2011) Reduction of infarct size by intravenous injection of uncultured adipose derived stromal cells in a rat model is dependent on the time point of application. Stem Cell Res 7:219–229

    PubMed  CAS  Google Scholar 

  97. Bagno LL, Werneck-de-Castro JP, Oliveira PF et al (2012) Adipose-derived stromal cell therapy improves cardiac function after coronary occlusion in rats. Cell Transplant 21 (9):1985–1996

    PubMed  CAS  Google Scholar 

  98. Otto Beitnes J, Oie E, Shahdadfar A et al (2012) Intramyocardial injections of human mesenchymal stem cells following acute myocardial infarction modulate scar formation and improve left ventricular function. Cell Transplant 21:1697–1709

    PubMed  CAS  Google Scholar 

  99. Fang CH, Jin J, Joe JH et al (2012) In vivo differentiation of human amniotic epithelial cells into cardiomyocyte-like cells and cell transplantation effect on myocardial infarction in rats: comparison with cord blood and adipose tissue-derived mesenchymal stem cells. Cell Transplant 21:1687–1696

    PubMed  CAS  Google Scholar 

  100. Hoke NN, Salloum FN, Dakks DA et al (2012) Preconditioning by phosphodiesterase-5 inhibition improves therapeutic efficacy of adipose-derived stem cells following myocardial infarction in mice. Stem Cells 30:326–335

    PubMed  CAS  Google Scholar 

  101. Li TS, Cheng K, Malliaras K et al (2012) Direct comparison of different stem cell types and subpopulations reveals superior paracrine potency and myocardial repair efficacy with cardiosphere-­derived cells. J Am Coll Cardiol 59:942–953

    PubMed  CAS  Google Scholar 

  102. Liu Z, Wang H, Wang Y et al (2012) The influence of chitosan hydrogel on stem cell engraftment, survival and homing in the ischemic myocardial microenvironment. Biomaterials 33:3093–3106

    PubMed  CAS  Google Scholar 

  103. Paul A, Cheng G, Khan A et al (2012) Genipin-cross-linked microencapsulated human adipose stem cells augment transplant retention resulting in attenuation of chronically infarcted rat heart fibrosis and cardiac dysfunction. Cell Transplant 21:2735–2751

    PubMed  Google Scholar 

  104. Shi CZ, Zhang XP, Lv ZW et al (2012) Adipose tissue-derived stem cells embedded with eNOS restore cardiac function in acute myocardial infarction model. Int J Cardiol 154:2–8

    PubMed  Google Scholar 

  105. Zhang DZ, Gai LY, Liu HW et al (2007) Transplantation of autologous adipose-derived stem cells ameliorates cardiac function in rabbits with myocardial infarction. Chin Med J (Engl) 120:300–307

    Google Scholar 

  106. Yang JJ, Yang X, Liu ZQ et al (2012) Transplantation of adipose tissue-derived stem cells overexpressing heme oxygenase-1 improves functions and remodeling of infarcted myocardium in rabbits. Tohoku J Exp Med 226:231–241

    PubMed  Google Scholar 

  107. Watanabe C (2004) Intracoronary adipose tissue derived stem cells therapy preserves left ventricular function in a porcine infarct model. Paper presented at Transvascular Cardiovascular Therapeutics Annual Meeting, September 2004, Washington DC, USA

    PubMed  CAS  Google Scholar 

  108. Fotuhi P, Song YH, Alt E (2007) Electrophysiological consequence of adipose-derived stem cell transplantation in infarcted porcine myocardium. Europace 9:1218–1221

    PubMed  CAS  Google Scholar 

  109. Valina C, Pinkernell K, Song YH et al (2007) Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction. Eur Heart J 28:2667–2677

    PubMed  Google Scholar 

  110. Alt E, Pinkernell K, Scharlau M et al (2010) Effect of freshly isolated autologous tissue resident stromal cells on cardiac function and perfusion following acute myocardial infarction. Int J Cardiol 144:26–35

    PubMed  CAS  Google Scholar 

  111. Rigol M, Solanes N, Farre J et al (2010) Effects of adipose tissue-derived stem cell therapy after myocardial infarction: impact of the route of administration. J Card Fail 16:357–366

    PubMed  CAS  Google Scholar 

  112. Mazo M, Hernández S, Gavira JJ et al (2012) Treatment of reperfused ischemia with adiposederived stem cells in a preclinical Swine model of myocardial infarction. Cell Transplant 21:2723–2733

    PubMed  CAS  Google Scholar 

  113. Kim YM, Jeon ES, Kim MR et al (2008) Angiotensin II-induced differentiation of adipose tissue-derived mesenchymal stem cells to smooth muscle-like cells. Int J Biochem Cell Biol 40:2482–2491

    PubMed  CAS  Google Scholar 

  114. Rodriguez LV, Alfonso Z, Zhang R et al (2006) Clonogenic multipotent stem cells in human adipose tissue differentiate into functional smooth muscle cells. Proc Natl Acad Sci U S A 103:12167–12172

    PubMed  CAS  Google Scholar 

  115. Ning H, Liu G, Lin G et al (2009) Fibroblast growth factor 2 promotes endothelial differentiation of adipose tissue-derived stem cells. J Sex Med 6:967–979

    PubMed  CAS  Google Scholar 

  116. Jackson KA, Majka SM, Wang H et al (2001) Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 107:1395–1402

    PubMed  Google Scholar 

  117. Laflamme MA, Myerson D, Saffitz JE, Murry CE (2002) Evidence for cardiomyocyte repopulation by extracardiac progenitors in transplanted human hearts. Circ Res 90:634–640

    PubMed  CAS  Google Scholar 

  118. Gnecchi M, He H, Liang OD et al (2005) Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 11:367–368

    PubMed  CAS  Google Scholar 

  119. Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285:1182–1186

    PubMed  CAS  Google Scholar 

  120. Yanagisawa-Miwa A, Uchida Y, Nakamura F et al (1992) Salvage of infarcted myocardium by angiogenic action of basic fibroblast growth factor. Science 257:1401–1403

    PubMed  CAS  Google Scholar 

  121. Takeshita S, Zheng LP, Brogi E et al (1994) Therapeutic angiogenesis. A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb model. J Clin Invest 93:662–670

    PubMed  CAS  Google Scholar 

  122. Losordo DW, Dimmeler S (2004) Therapeutic angiogenesis and vasculogenesis for ischemic disease. Part I: angiogenic cytokines. Circulation 109:2487–2491

    PubMed  CAS  Google Scholar 

  123. Freedman SB, Isner JM (2002) Therapeutic angiogenesis for coronary artery disease. Ann Intern Med 136:54–71

    PubMed  CAS  Google Scholar 

  124. Losordo DW, Vale PR, Hendel RC et al (2002) Phase 1/2 placebo-controlled, double-blind, dose-escalating trial of myocardial vascular endothelial growth factor 2 gene transfer by catheter delivery in patients with chronic myocardial ischemia. Circulation 105:2012–2018

    PubMed  CAS  Google Scholar 

  125. Henry TD, Annex BH, McKendall GR et al (2003) The VIVA trial: vascular endothelial growth factor in ischemia for vascular angiogenesis. Circulation 107:1359–1365

    PubMed  CAS  Google Scholar 

  126. Lazarous DF, Shou M, Scheinowitz M et al (1996) Comparative effects of basic fibroblast growth factor and vascular endothelial growth factor on coronary collateral development and the arterial response to injury. Circulation 94:1074–1082

    PubMed  CAS  Google Scholar 

  127. Takahashi T, Kalka C, Masuda H et al (1999) Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 5:434–438

    PubMed  CAS  Google Scholar 

  128. Yamaguchi J, Kusano KF, Masuo O et al (2003) Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 107:1322–1328

    PubMed  CAS  Google Scholar 

  129. Wang M, Crisostomo PR, Herring C et al (2006) Human progenitor cells from bone marrow or adipose tissue produce VEGF, HGF, and IGF-I in response to TNF by a p38 MAPKdependent mechanism. Am J Physiol Regul Integr Comp Physiol 291:R880–R884

    PubMed  CAS  Google Scholar 

  130. Dernbach E, Urbich C, Brandes RP et al (2004) Antioxidative stress-associated genes in ­circulating progenitor cells: evidence for enhanced resistance against oxidative stress. Blood 104:3591–3597

    PubMed  CAS  Google Scholar 

  131. Kocher AA, Schuster MD, Szabolcs MJ et al (2001) Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 7:430–436

    PubMed  CAS  Google Scholar 

  132. Schuster MD, Kocher AA, Seki T et al (2004) Myocardial neovascularization by bone ­marrow angioblasts results in cardiomyocyte regeneration. Am J Physiol Heart Circ Physiol 287:H525–H532

    PubMed  CAS  Google Scholar 

  133. Murohara T (2009) Autologous adipose tissue as a new source of progenitor cells for therapeutic angiogenesis. J Cardiol 53:155–163

    PubMed  CAS  Google Scholar 

  134. Sadat S, Gehmert S, Song YH et al (2007) The cardioprotective effect of mesenchymal stem cells is mediated by IGF-I and VEGF. Biochem Biophys Res Commun 363:674–679

    PubMed  CAS  Google Scholar 

  135. Liles WC, Broxmeyer HE, Rodger E et al (2003) Mobilization of hematopoietic progenitor cells in healthy volunteers by AMD3100, a CXCR4 antagonist. Blood 102:2728–2730

    PubMed  CAS  Google Scholar 

  136. Tachibana K, Hirota S, Iizasa H et al (1998) The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393:591–594

    PubMed  CAS  Google Scholar 

  137. Rasmussen JG, Frobert O, Pilgaard L et al (2011) Prolonged hypoxic culture and trypsinization increase the pro-angiogenic potential of human adipose tissue-derived stem cells. Cytotherapy 13:318–328

    PubMed  CAS  Google Scholar 

  138. Suga H, Eto H, Aoi N et al (2010) Adipose tissue remodeling under ischemia: death of ­adipocytes and activation of stem/progenitor cells. Plast Reconstr Surg 126:1911–1923

    PubMed  CAS  Google Scholar 

  139. Stubbs SL, Hsiao ST, Peshavariya HM et al (2012) Hypoxic preconditioning enhances survival of human adipose-derived stem cells and conditions endothelial cells in vitro. Stem Cells Dev 21:1887–1896

    PubMed  CAS  Google Scholar 

  140. Tateishi-Yuyama E, Matsubara H, Murohara T et al (2002) Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Lancet 360:427–435

    PubMed  CAS  Google Scholar 

  141. Jay SM, Shepherd BR, Bertram JP et al (2008) Engineering of multifunctional gels integrating highly efficient growth factor delivery with endothelial cell transplantation. FASEB J 22:2949–2956

    PubMed  CAS  Google Scholar 

  142. Deuse T, Peter C, Fedak PW et al (2009) Hepatocyte growth factor or vascular endothelial growth factor gene transfer maximizes mesenchymal stem cell-based myocardial salvage after acute myocardial infarction. Circulation 120:S247–S254

    PubMed  CAS  Google Scholar 

  143. Fitzpatrick JR III, Frederick JR, McCormick RC et al (2010) Tissue-engineered proangiogenic fibroblast scaffold improves myocardial perfusion and function and limits ventricular remodeling after infarction. J Thorac Cardiovasc Surg 140:667–676

    PubMed  CAS  Google Scholar 

  144. Bhang SH, Cho SW, La WG et al (2011) Angiogenesis in ischemic tissue produced by spheroid grafting of human adipose-derived stromal cells. Biomaterials 32:2734–2747

    PubMed  CAS  Google Scholar 

  145. Amos PJ, Shang H, Bailey AM et al (2008) IFATS collection: the role of human adiposederived stromal cells in inflammatory microvascular remodeling and evidence of a perivascular phenotype. Stem Cells 26:2682–2690

    PubMed  CAS  Google Scholar 

  146. Zannettino AC, Paton S, Arthur A et al (2008) Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 214:413–421

    PubMed  CAS  Google Scholar 

  147. Efimenko A, Starostina E, Kalinina N, Stolzing A (2011) Angiogenic properties of aged adipose derived mesenchymal stem cells after hypoxic conditioning. J Transl Med 9:10

    PubMed  CAS  Google Scholar 

  148. Onate B, Vilahur G, Ferrer-Lorente R et al (2012) The subcutaneous adipose tissue reservoir of functionally active stem cells is reduced in obese patients. FASEB J 26(10):4327–4336

    PubMed  CAS  Google Scholar 

  149. Hwangbo S, Kim J, Her S et al (2010) Therapeutic potential of human adipose stem cells in a rat myocardial infarction model. Yonsei Med J. 51:69–76

    PubMed  CAS  Google Scholar 

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Acknowledgements 

This work was supported by grants TERCEL, SAF 2010-16549, CIBEROBN CB06/03 and by the ENCITE (European Network for Cell Imaging and Tracking Expertise) project Cooperation Health-2007-1.2-4 In Vivo Image-guidance for Cell Therapy, Large-scale Integrating Project (to LB). We thank Fundacion Jesus Serra-FIC, Barcelona, for their continuous support. BO is a recipient of a predoctoral fellowship from Instituto Salud Carlos III, Madrid, and GV is a recipient of a contract from the Innovation and Science Spanish Ministry (RyC-2009-5495).

Disclosure No competing financial interests exist.

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Authors and Affiliations

  1. Cardiovascular Research Center, CSIC-ICCC, Hospital de la Santa Creu i Sant Pau, IIB-Sant Pau, c/Sant Antoni MªClaret 167, 08025, Barcelona, Spain

    Lina Badimon (Cardiovascular Research Chair), Blanca Oñate & Gemma Vilahur

  2. CIBEROBN-Pathophysiology of Obesity and Nutrition, Barcelona, Spain

    Lina Badimon (Cardiovascular Research Chair), Blanca Oñate & Gemma Vilahur

  3. UAB, Barcelona, Spain

    Lina Badimon (Cardiovascular Research Chair)

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  1. Lina Badimon
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  2. Blanca Oñate
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  3. Gemma Vilahur
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Correspondence to Lina Badimon .

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Editors and Affiliations

  1. Div. of Cardiovascular Medicine, UAMS, Little Rock, AR, USA, 4301 W Markham, Little Rock, 72205, Arkansas, USA

    Jawahar L. Mehta

  2. Institute of Cardiovascular Sciences, St. Boniface Hosp. Research, Univ. of Ma, 351 Tache Avenue, Winnipeg, R2H 2A6, Manitoba, Canada

    Naranjan S. Dhalla

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Badimon, L., Oñate, B., Vilahur, G. (2013). Adipose Tissue-Derived Mesenchymal Stem Cell and Angiogenesis in Ischemic Heart Disease. In: Mehta, J., Dhalla, N. (eds) Biochemical Basis and Therapeutic Implications of Angiogenesis. Advances in Biochemistry in Health and Disease, vol 6. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5857-9_16

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