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Cellular and Molecular Life Sciences

, Volume 71, Issue 8, pp 1353–1374 | Cite as

Natural history of mesenchymal stem cells, from vessel walls to culture vessels

  • Iain R. Murray
  • Christopher C. West
  • Winters R. Hardy
  • Aaron W. James
  • Tea Soon Park
  • Alan Nguyen
  • Tulyapruek Tawonsawatruk
  • Lorenza Lazzari
  • Chia Soo
  • Bruno Péault
Review

Abstract

Mesenchymal stem/stromal cells (MSCs) can regenerate tissues by direct differentiation or indirectly by stimulating angiogenesis, limiting inflammation, and recruiting tissue-specific progenitor cells. MSCs emerge and multiply in long-term cultures of total cells from the bone marrow or multiple other organs. Such a derivation in vitro is simple and convenient, hence popular, but has long precluded understanding of the native identity, tissue distribution, frequency, and natural role of MSCs, which have been defined and validated exclusively in terms of surface marker expression and developmental potential in culture into bone, cartilage, and fat. Such simple, widely accepted criteria uniformly typify MSCs, even though some differences in potential exist, depending on tissue sources. Combined immunohistochemistry, flow cytometry, and cell culture have allowed tracking the artifactual cultured mesenchymal stem/stromal cells back to perivascular anatomical regions. Presently, both pericytes enveloping microvessels and adventitial cells surrounding larger arteries and veins have been described as possible MSC forerunners. While such a vascular association would explain why MSCs have been isolated from virtually all tissues tested, the origin of the MSCs grown from umbilical cord blood remains unknown. In fact, most aspects of the biology of perivascular MSCs are still obscure, from the emergence of these cells in the embryo to the molecular control of their activity in adult tissues. Such dark areas have not compromised intents to use these cells in clinical settings though, in which purified perivascular cells already exhibit decisive advantages over conventional MSCs, including purity, thorough characterization and, principally, total independence from in vitro culture. A growing body of experimental data is currently paving the way to the medical usage of autologous sorted perivascular cells for indications in which MSCs have been previously contemplated or actually used, such as bone regeneration and cardiovascular tissue repair.

Keywords

Blood vessels Stem cells Pericytes Cell therapy Tissue repair Mesenchymal stem cells 

Abbreviations

AGM

Aorta-gonad-mesonephros

BGP

β-glycerophosphate

BM

Bone marrow

BMP

Bone morphogenetic protein

CB

Cord blood

CD

Cluster of differentiation

CFU

Colony-forming unit

CPD

Cumulative population doubling

CSC

Cardiac stem cell

DLK-1

Delta-like 1

ECM

Extracellular matrix

EPC

Endothelial progenitor cell

FACS

Fluorescence-activated cell sorting

FDA

Food and Drug Administration

HGF

Hepatocyte growth factor

HLADR

Human leukocyte antigen-DR

HSC

Hematopoietic stem cell

IBMX

3-isobutyl-1-methylxanthine

IGF

Insulin-like growth factor

ISCT

International Society for Cellular Therapy

Lep-R

Leptin receptor

mAbs

Monoclonal antibodies

MAPC

Multipotent adult progenitor cell

MASC

Multipotent adult stem cell

MCAM

Melanoma cell adhesion molecule

MI

Myocardial infarction

MIAMI

Marrow-isolated adult multilineage inducible cell

MLPC

Multilineage progenitor cell

MSC

Mesenchymal stem cell

NELL1

Nel-like molecule 1

OVX

Ovariectomized

PDGFRβ

Platelet-derived growth factor receptor β

PSC

Perivascular stem cell

SCF

Stem cell factor

SVF

Stromal vascular fraction

SVP

Saphenous vein pericyte

USSC

Unrestricted somatic stem cell

VCAM

Vascular cell adhesion molecule

VEGF

Vascular endothelial growth factor

VESL

Very small embryonic-like stem cell

vWF

von Willebrand factor

Notes

Disclosure

B.P., and C.S. are inventors of perivascular stem cell-related patents filed from UCLA. Dr C.S. is a founder of Scarless Laboratories Inc. which sublicenses perivascular stem cell-related patents from the UC Regents, and who also hold equity in the company. Dr C.S. is also an officer of Scarless Laboratories, Inc. This work was supported by the CIRM Early Translational II Research Award TR2-01821.

References

  1. 1.
    Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276(5309):71–74PubMedGoogle Scholar
  2. 2.
    Friedenstein AJ, Chailakhjan RK, Lalykina KS (1970) The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 3(4):393–403PubMedGoogle Scholar
  3. 3.
    Friedenstein AJ, Chailakhyan RK, Latsinik NV et al (1974) Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 17(4):331–340PubMedGoogle Scholar
  4. 4.
    Friedenstein AJ, Piatetzky S II, Petrakova KV (1966) Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol 16(3):381–390PubMedGoogle Scholar
  5. 5.
    Owen M, Friedenstein AJ (1988) Stromal stem cells: marrow-derived osteogenic precursors. Ciba Found Symp 136:42–60PubMedGoogle Scholar
  6. 6.
    Bianco P, Robey PG, Simmons PJ (2008) Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell 2(4):313–319PubMedCentralPubMedGoogle Scholar
  7. 7.
    Pittenger MF, Mackay AM, Beck SC et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284(5411):143–147PubMedGoogle Scholar
  8. 8.
    Kolf CM, Cho E, Tuan RS (2007) Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation. Arthritis Res Ther 9(1):204PubMedCentralPubMedGoogle Scholar
  9. 9.
    Caplan AI (2007) Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 213(2):341–347PubMedGoogle Scholar
  10. 10.
    Diaz-Flores L, Gutierrez R, Gonzalez P et al (1991) Inducible perivascular cells contribute to the neochondrogenesis in grafted perichondrium. Anat Rec 229(1):1–8PubMedGoogle Scholar
  11. 11.
    Diaz-Flores L, Gutierrez R, Lopez-Alonso A et al (1992) Pericytes as a supplementary source of osteoblasts in periosteal osteogenesis. Clin Orthop Relat Res 275:280–286PubMedGoogle Scholar
  12. 12.
    Caplan AI (1991) Mesenchymal stem cells. J Orthop Res 9(5):641–650PubMedGoogle Scholar
  13. 13.
    Zuk PA, Zhu M, Ashjian P et al (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13(12):4279–4295PubMedCentralPubMedGoogle Scholar
  14. 14.
    Xu Y, Malladi P, Wagner DR et al (2005) Adipose-derived mesenchymal cells as a potential cell source for skeletal regeneration. Curr Opin Mol Ther 7(4):300–305PubMedGoogle Scholar
  15. 15.
    Shi S, Gronthos S (2003) Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 18(4):696–704PubMedGoogle Scholar
  16. 16.
    Seo BM, Miura M, Gronthos S et al (2004) Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 364(9429):149–155PubMedGoogle Scholar
  17. 17.
    Salingcarnboriboon R, Yoshitake H, Tsuji K et al (2003) Establishment of tendon-derived cell lines exhibiting pluripotent mesenchymal stem cell-like property. Exp Cell Res 287(2):289–300PubMedGoogle Scholar
  18. 18.
    Bi Y, Ehirchiou D, Kilts TM et al (2007) Identification of tendon stem/progenitor cells and the role of the extracellular matrix in their niche. Nat Med 13(10):1219–1227PubMedGoogle Scholar
  19. 19.
    Rogers I, Casper RF (2004) Umbilical cord blood stem cells. Best Pract Res Clin Obstet Gynaecol 18(6):893–908PubMedGoogle Scholar
  20. 20.
    Toma JG, Akhavan M, Fernandes KJ et al (2001) Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3(9):778–784PubMedGoogle Scholar
  21. 21.
    Igura K, Zhang X, Takahashi K et al (2004) Isolation and characterization of mesenchymal progenitor cells from chorionic villi of human placenta. Cytotherapy 6(6):543–553PubMedGoogle Scholar
  22. 22.
    Tsai MS, Lee JL, Chang YJ et al (2004) Isolation of human multipotent mesenchymal stem cells from second-trimester amniotic fluid using a novel two-stage culture protocol. Hum Reprod 19(6):1450–1456PubMedGoogle Scholar
  23. 23.
    De Bari C, Dell’Accio F, Tylzanowski P et al (2001) Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 44(8):1928–1942PubMedGoogle Scholar
  24. 24.
    Asakura A, Komaki M, Rudnicki M (2001) Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation 68(4–5):245–253PubMedGoogle Scholar
  25. 25.
    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(11):2204–2213Google Scholar
  26. 26.
    Covas DT, Panepucci RA, Fontes AM et al (2008) Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts. Exp Hematol 36(5):642–654PubMedGoogle Scholar
  27. 27.
    Crisan M (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301–313PubMedGoogle Scholar
  28. 28.
    Chen CW, Montelatici E, Crisan M et al (2009) Perivascular multi-lineage progenitor cells in human organs: regenerative units, cytokine sources or both? Cytokine Growth Factor Rev 20(5–6):429–434PubMedGoogle Scholar
  29. 29.
    Tsutsumi S, Shimazu A, Miyazaki K et al (2001) Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochem Biophys Res Commun 288(2):413–419PubMedGoogle Scholar
  30. 30.
    Kulterer B, Friedl G, Jandrositz A et al (2007) Gene expression profiling of human mesenchymal stem cells derived from bone marrow during expansion and osteoblast differentiation. BMC Genomics 8:70PubMedCentralPubMedGoogle Scholar
  31. 31.
    Pochampally RR, Smith JR, Ylostalo J et al (2004) Serum deprivation of human marrow stromal cells (hMSCs) selects for a subpopulation of early progenitor cells with enhanced expression of OCT-4 and other embryonic genes. Blood 103(5):1647–1652PubMedGoogle Scholar
  32. 32.
    Hishikawa K, Miura S, Marumo T et al (2004) Gene expression profile of human mesenchymal stem cells during osteogenesis in three-dimensional thermoreversible gelation polymer. Biochem Biophys Res Commun 317(4):1103–1107PubMedGoogle Scholar
  33. 33.
    Kratchmarova I, Blagoev B, Haack-Sorensen M et al (2005) Mechanism of divergent growth factor effects in mesenchymal stem cell differentiation. Science 308(5727):1472–1477PubMedGoogle Scholar
  34. 34.
    Song L, Webb NE, Song Y et al (2006) Identification and functional analysis of candidate genes regulating mesenchymal stem cell self-renewal and multipotency. Stem Cells 24(7):1707–1718PubMedGoogle Scholar
  35. 35.
    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(4):315–317PubMedGoogle Scholar
  36. 36.
    Peister A, Mellad JA, Larson BL et al (2004) Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103(5):1662–1668PubMedGoogle Scholar
  37. 37.
    Dexter TM, Allen TD, Lajtha LG (1977) Conditions controlling the proliferation of haemopoietic stem cells in vitro. J Cell Physiol 91(3):335–344PubMedGoogle Scholar
  38. 38.
    Simmons PJ, Torok-Storb B (1991) Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood 78(1):55–62PubMedGoogle Scholar
  39. 39.
    Dennis JE, Carbillet JP, Caplan AI et al (2002) The STRO-1+ marrow cell population is multipotential. Cells Tissues Organs 170(2–3):73–82PubMedGoogle Scholar
  40. 40.
    Devine SM, Bartholomew AM, Mahmud N et al (2001) Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Exp Hematol 29(2):244–255PubMedGoogle Scholar
  41. 41.
    In ‘t Anker PS, Scherjon SA, Kleijburg-van der Keur C et al (2003) Amniotic fluid as a novel source of mesenchymal stem cells for therapeutic transplantation. Blood 102(4):1548–1549PubMedGoogle Scholar
  42. 42.
    Bensidhoum M, Chapel A, Francois S et al (2004) Homing of in vitro expanded Stro-1− or Stro-1+ human mesenchymal stem cells into the NOD/SCID mouse and their role in supporting human CD34 cell engraftment. Blood 103(9):3313–3319PubMedGoogle Scholar
  43. 43.
    Farrington-Rock C, Crofts NJ, Doherty MJ et al (2004) Chondrogenic and adipogenic potential of microvascular pericytes. Circulation 110(15):2226–2232PubMedGoogle Scholar
  44. 44.
    Feng J, Mantesso A, De Bari C et al (2011) Dual origin of mesenchymal stem cells contributing to organ growth and repair. Proc Natl Acad Sci USA 108(16):6503–6508PubMedCentralPubMedGoogle Scholar
  45. 45.
    Sims DE (1986) The pericyte: a review. Tissue Cell 18(2):153–174PubMedGoogle Scholar
  46. 46.
    Diaz-Flores L, Martin Herrera AI, Garcia Montelongo R et al (1990) Role of pericytes and endothelial cells in tissue repair and related pathological processes. J Cutan Pathol 17(3):191–192PubMedGoogle Scholar
  47. 47.
    Savvatis K, van Linthout S, Miteva K et al (2012) Mesenchymal stromal cells but not cardiac fibroblasts exert beneficial systemic immunomodulatory effects in experimental myocarditis. Plos One 7(7):e41047PubMedCentralPubMedGoogle Scholar
  48. 48.
    Jia Z, Jiao C, Zhao S et al (2012) Immunomodulatory effects of mesenchymal stem cells in a rat corneal allograft rejection model. Exp Eye Res 102:44–49PubMedGoogle Scholar
  49. 49.
    Nauta AJ, Fibbe WE (2007) Immunomodulatory properties of mesenchymal stromal cells. Blood 110(10):3499–3506PubMedGoogle Scholar
  50. 50.
    Krampera M, Cosmi L, Angeli R et al (2006) Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 24(2):386–398PubMedGoogle Scholar
  51. 51.
    Caplan AI, Correa D (2011) The MSC: an injury drugstore. Cell Stem Cell 9(1):11–15PubMedCentralPubMedGoogle Scholar
  52. 52.
    Aggarwal S, Pittenger MF (2005) Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105(4):1815–1822PubMedGoogle Scholar
  53. 53.
    Jui HY, Lin CH, Hsu WT et al (2012) Autologous mesenchymal stem cells prevent transplant arteriosclerosis by enhancing local expression of interleukin-10, interferon-gamma, and indoleamine 2,3-dioxygenase. Cell Transplant 21(5):971–984PubMedGoogle Scholar
  54. 54.
    Caplan AI, Dennis JE (2006) Mesenchymal stem cells as trophic mediators. J Cell Biochem 98(5):1076–1084PubMedGoogle Scholar
  55. 55.
    Kuo YR, Chen CC, Shih HS et al (2011) Prolongation of composite tissue allotransplant survival by treatment with bone marrow mesenchymal stem cells is correlated with T-cell regulation in a swine hind-limb model. Plast Reconstr Surg 127(2):569–579PubMedGoogle Scholar
  56. 56.
    Ikeguchi R, Sacks JM, Unadkat JV et al (2008) Long-term survival of limb allografts induced by pharmacologically conditioned, donor alloantigen-pulsed dendritic cells without maintenance immunosuppression. Transplantation 85(2):237–246PubMedGoogle Scholar
  57. 57.
    Sarugaser R, Ennis J, Stanford WL et al (2009) Isolation, propagation, and characterization of human umbilical cord perivascular cells (HUCPVCs). Methods Mol Biol 482:269–279PubMedGoogle Scholar
  58. 58.
    Dai W, Hale SL, Martin BJ et al (2005) Allogeneic mesenchymal stem cell transplantation in postinfarcted rat myocardium: short- and long-term effects. Circulation 112(2):214–223PubMedGoogle Scholar
  59. 59.
    Noiseux N, Gnecchi M, Lopez-Ilasaca M et al (2006) Mesenchymal stem cells overexpressing Akt dramatically repair infarcted myocardium and improve cardiac function despite infrequent cellular fusion or differentiation. Mol Ther 14(6):840–850PubMedGoogle Scholar
  60. 60.
    Kinnaird T, Stabile E, Burnett MS et al (2004) Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 109(12):1543–1549PubMedGoogle Scholar
  61. 61.
    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(4):367–368PubMedGoogle Scholar
  62. 62.
    Baksh D, Song L, Tuan RS (2004) Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy. J Cell Mol Med 8(3):301–316PubMedGoogle Scholar
  63. 63.
    Schafer R, Dominici M, Muller I et al (2007) Progress in characterization, preparation and clinical applications of non-hematopoietic stem cells, 29–30 September 2006, Tubingen, Germany. Cytotherapy 9(4):397–405PubMedGoogle Scholar
  64. 64.
    Ratajczak MZ, Zuba-Surma EK, Wysoczynski M et al (2008) Hunt for pluripotent stem cell—regenerative medicine search for almighty cell. J Autoimmun 30(3):151–162PubMedCentralPubMedGoogle Scholar
  65. 65.
    Jiang Y, Jahagirdar BN, Reinhardt RL et al (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418(6893):41–49PubMedGoogle Scholar
  66. 66.
    D’Ippolito G, Diabira S, Howard GA 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(Pt 14):2971–2981PubMedGoogle Scholar
  67. 67.
    Beltrami AP, Cesselli D, Bergamin N et al (2007) Multipotent cells can be generated in vitro from several adult human organs (heart, liver, and bone marrow). Blood 110(9):3438–3446PubMedGoogle Scholar
  68. 68.
    Bosch J, Houben AP, Radke TF et al (2012) Distinct differentiation potential of “MSC” derived from cord blood and umbilical cord: are cord-derived cells true mesenchymal stromal cells? Stem Cells Dev 21(11):1977–1988PubMedGoogle Scholar
  69. 69.
    Kluth SM, Buchheiser A, Houben AP et al (2010) DLK-1 as a marker to distinguish unrestricted somatic stem cells and mesenchymal stromal cells in cord blood. Stem Cells Dev 19(10):1471–1483PubMedGoogle Scholar
  70. 70.
    Kucia M, Halasa M, Wysoczynski M et al (2007) Morphological and molecular characterization of novel population of CXCR4+ SSEA-4+ Oct-4+ very small embryonic-like cells purified from human cord blood: preliminary report. Leukemia 21(2):297–303PubMedGoogle Scholar
  71. 71.
    Ratajczak MZ, Zuba-Surma EK, Machalinski B et al (2007) Bone-marrow-derived stem cells—our key to longevity? J Appl Genet 48(4):307–319PubMedGoogle Scholar
  72. 72.
    Rojewski MT, Weber BM, Schrezenmeier H (2008) Phenotypic characterization of mesenchymal stem cells from various tissues. Transfus Med Hemother 35(3):168–184PubMedCentralPubMedGoogle Scholar
  73. 73.
    Lindner U, Kramer J, Behrends J et al (2010) Improved proliferation and differentiation capacity of human mesenchymal stromal cells cultured with basement-membrane extracellular matrix proteins. Cytotherapy 12(8):992–1005PubMedGoogle Scholar
  74. 74.
    Gronthos S, Zannettino AC, Hay SJ et al (2003) Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 116(Pt 9):1827–1835PubMedGoogle Scholar
  75. 75.
    Bianco P, Riminucci M, Gronthos S et al (2001) Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19(3):180–192PubMedGoogle Scholar
  76. 76.
    Sacchetti B, Funari A, Michienzi S et al (2007) Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131(2):324–336PubMedGoogle Scholar
  77. 77.
    Schipani E, Kronenberg HM (2008) Adult mesenchymal stem cells. Harvard Stem Cell Institute, CambridgeGoogle Scholar
  78. 78.
    Jones EA, Kinsey SE, English A et al (2002) Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum 46(12):3349–3360PubMedGoogle Scholar
  79. 79.
    Levi B, Wan DC, Glotzbach JP et al (2011) CD105 protein depletion enhances human adipose-derived stromal cell osteogenesis through reduction of transforming growth factor beta1 (TGF-beta1) signaling. J Biol Chem 286(45):39497–39509PubMedCentralPubMedGoogle Scholar
  80. 80.
    Quirici N, Soligo D, Bossolasco P et al (2002) Isolation of bone marrow mesenchymal stem cells by anti-nerve growth factor receptor antibodies. Exp Hematol 30(7):783–791PubMedGoogle Scholar
  81. 81.
    Meyerrose TE, De Ugarte DA, Hofling AA et al (2007) In vivo distribution of human adipose-derived mesenchymal stem cells in novel xenotransplantation models. Stem Cells 25(1):220–227PubMedGoogle Scholar
  82. 82.
    Daquinag AC, Zhang Y, Amaya-Manzanares F et al (2011) An isoform of decorin is a resistin receptor on the surface of adipose progenitor cells. Cell Stem Cell 9(1):74–86PubMedGoogle Scholar
  83. 83.
    Katz AJ, Tholpady A, Tholpady SS et al (2005) Cell surface and transcriptional characterization of human adipose-derived adherent stromal (hADAS) cells. Stem Cells 23(3):412–423PubMedGoogle Scholar
  84. 84.
    Mitchell JB, McIntosh K, Zvonic S et al (2006) Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem Cells 24(2):376–385PubMedGoogle Scholar
  85. 85.
    Kilroy GE, Foster SJ, Wu X et al (2007) Cytokine profile of human adipose-derived stem cells: expression of angiogenic, hematopoietic, and pro-inflammatory factors. J Cell Physiol 212(3):702–709PubMedGoogle Scholar
  86. 86.
    Muraglia A, Cancedda R, Quarto R (2000) Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci 113(Pt 7):1161–1166PubMedGoogle Scholar
  87. 87.
    Russell KC, Phinney DG, Lacey MR et al (2010) In vitro high-capacity assay to quantify the clonal heterogeneity in trilineage potential of mesenchymal stem cells reveals a complex hierarchy of lineage commitment. Stem Cells 28(4):788–798PubMedGoogle Scholar
  88. 88.
    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(2–3):267–270PubMedGoogle Scholar
  89. 89.
    Vogel W, Grunebach F, Messam CA et al (2003) Heterogeneity among human bone marrow-derived mesenchymal stem cells and neural progenitor cells. Haematologica 88(2):126–133PubMedGoogle Scholar
  90. 90.
    Mihu CM, Mihu D, Costin N et al (2008) Isolation and characterization of stem cells from the placenta and the umbilical cord. Rom J Morphol Embryol 49(4):441–446PubMedGoogle Scholar
  91. 91.
    Bottai D, Cigognini D, Nicora E et al (2012) Third-trimester amniotic fluid cells with the capacity to develop neural phenotypes and with heterogeneity among sub-populations. Restor Neurol Neurosci 30(1):55–68PubMedGoogle Scholar
  92. 92.
    Kuci S, Kuci Z, Kreyenberg H et al (2010) CD271 antigen defines a subset of multipotent stromal cells with immunosuppressive and lymphohematopoietic engraftment-promoting properties. Haematologica 95(4):651–659PubMedCentralPubMedGoogle Scholar
  93. 93.
    Battula VL, Treml S, Bareiss PM et al (2009) Isolation of functionally distinct mesenchymal stem cell subsets using antibodies against CD56, CD271, and mesenchymal stem cell antigen-1. Haematologica 94(2):173–184PubMedCentralPubMedGoogle Scholar
  94. 94.
    Nichols JE, Niles JA, Dewitt D et al (2013) Neurogenic and neuro-protective potential of a novel subpopulation of peripheral blood-derived CD133+ ABCG2+ CXCR4+ mesenchymal stem cells: development of autologous cell based therapeutics for traumatic brain injury. Stem Cell Res Ther 4(1):3PubMedCentralPubMedGoogle Scholar
  95. 95.
    Watt FM, Hogan BL (2000) Out of Eden: stem cells and their niches. Science 287(5457):1427–1430PubMedGoogle Scholar
  96. 96.
    Kunisaki Y, Frenette PS (2012) The secrets of the bone marrow niche: enigmatic niche brings challenge for HSC expansion. Nat Med 18(6):864–865PubMedGoogle Scholar
  97. 97.
    Braun KM, Niemann C, Jensen UB et al (2003) Manipulation of stem cell proliferation and lineage commitment: visualisation of label-retaining cells in wholemounts of mouse epidermis. Development 130(21):5241–5255PubMedGoogle Scholar
  98. 98.
    Gould E, Reeves AJ, Graziano MS et al (1999) Neurogenesis in the neocortex of adult primates. Science 286(5439):548–552PubMedGoogle Scholar
  99. 99.
    da Silva Meirelles L, Caplan AI, Nardi NB (2008) In search of the in vivo identity of mesenchymal stem cells. Stem Cells 26(9):2287–2299Google Scholar
  100. 100.
    Rochefort GY, Delorme B, Lopez A et al (2006) Multipotential mesenchymal stem cells are mobilized into peripheral blood by hypoxia. Stem Cells 24(10):2202–2208PubMedGoogle Scholar
  101. 101.
    Alm JJ, Koivu HM, Heino TJ et al (2010) Circulating plastic adherent mesenchymal stem cells in aged hip fracture patients. J Orthop Res 28(12):1634–1642Google Scholar
  102. 102.
    Lazarus HM, Haynesworth SE, Gerson SL et al (1997) Human bone marrow-derived mesenchymal (stromal) progenitor cells (MPCs) cannot be recovered from peripheral blood progenitor cell collections. J Hematother 6(5):447–455PubMedGoogle Scholar
  103. 103.
    Wexler SA, Donaldson C, Denning-Kendall P et al (2003) Adult bone marrow is a rich source of human mesenchymal ‘stem’ cells but umbilical cord and mobilized adult blood are not. Br J Haematol 121(2):368–374PubMedGoogle Scholar
  104. 104.
    James AW, Zara JN, Corselli M et al (2012) Use of human perivascular stem cells for bone regeneration. J Vis Exp: JoVE 63:e2952PubMedGoogle Scholar
  105. 105.
    James AW, Zara JN, Corselli M et al (2012) An abundant perivascular source of stem cells for bone tissue engineering. Stem Cells Transl Med 1(9):673–684PubMedCentralPubMedGoogle Scholar
  106. 106.
    Zimmerlin L, Donnenberg VS, Rubin JP et al (2013) Mesenchymal markers on human adipose stem/progenitor cells. Cytometry Part A: J Int Soc Anal Cytol 83:134–140Google Scholar
  107. 107.
    Crisan M, Chen CW, Corselli M et al (2009) Perivascular multipotent progenitor cells in human organs. Ann NY Acad Sci 1176:118–123PubMedGoogle Scholar
  108. 108.
    Park TS, Gavina M, Chen CW et al (2011) Placental perivascular cells for human muscle regeneration. Stem Cells Dev 20(3):451–463PubMedCentralPubMedGoogle Scholar
  109. 109.
    Tu Z, Li Y, Smith DS et al (2011) Retinal pericytes inhibit activated T cell proliferation. Invest Ophthalmol Vis Sci 52(12):9005–9010PubMedCentralPubMedGoogle Scholar
  110. 110.
    Maier CL, Pober JS (2011) Human placental pericytes poorly stimulate and actively regulate allogeneic CD4 T cell responses. Arterioscler Thromb Vasc Biol 31(1):183–189PubMedCentralPubMedGoogle Scholar
  111. 111.
    Tottey S, Corselli M, Jeffries EM et al (2011) Extracellular matrix degradation products and low-oxygen conditions enhance the regenerative potential of perivascular stem cells. Tissue Eng Part A 17(1–2):37–44PubMedCentralPubMedGoogle Scholar
  112. 112.
    Beck B, Driessens G, Goossens S et al (2011) A vascular niche and a VEGF-Nrp1 loop regulate the initiation and stemness of skin tumours. Nature 478(7369):399–403PubMedGoogle Scholar
  113. 113.
    Paul G, Ozen I, Christophersen NS et al (2012) The adult human brain harbors multipotent perivascular mesenchymal stem cells. Plos One 7(4):e35577PubMedCentralPubMedGoogle Scholar
  114. 114.
    Gerlach JC, Over P, Turner ME et al (2012) Perivascular mesenchymal progenitors in human fetal and adult liver. Stem Cells Dev 21(18):3258–3269PubMedGoogle Scholar
  115. 115.
    Dellavalle A, Sampaolesi M, Tonlorenzi R et al (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9(3):255–267PubMedGoogle Scholar
  116. 116.
    Davidoff MS, Middendorff R, Enikolopov G et al (2004) Progenitor cells of the testosterone-producing Leydig cells revealed. J Cell Biol 167(5):935–944PubMedCentralPubMedGoogle Scholar
  117. 117.
    Tang W, Zeve D, Suh JM et al (2008) White fat progenitor cells reside in the adipose vasculature. Science 322(5901):583–586PubMedCentralPubMedGoogle Scholar
  118. 118.
    Dellavalle A, Maroli G, Covarello D et al (2011) Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat Commun 2:499PubMedGoogle Scholar
  119. 119.
    Krautler NJ, Kana V, Kranich J et al (2012) Follicular dendritic cells emerge from ubiquitous perivascular precursors. Cell 150(1):194–206PubMedCentralPubMedGoogle Scholar
  120. 120.
    Bouacida A, Rosset P, Trichet V et al (2012) Pericyte-like progenitors show high immaturity and engraftment potential as compared with mesenchymal stem cells. Plos One 7(11):e48648PubMedCentralPubMedGoogle Scholar
  121. 121.
    Olson LE, Soriano P (2011) PDGFRbeta signaling regulates mural cell plasticity and inhibits fat development. Dev Cell 20(6):815–826PubMedCentralPubMedGoogle Scholar
  122. 122.
    Ceradini DJ, Kulkarni AR, Callaghan MJ et al (2004) Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10(8):858–864PubMedGoogle Scholar
  123. 123.
    Mendez-Ferrer S, Michurina TV, Ferraro F et al (2010) Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466(7308):829–834PubMedCentralPubMedGoogle Scholar
  124. 124.
    Ding L, Saunders TL, Enikolopov G et al (2012) Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481(7382):457–462PubMedCentralPubMedGoogle Scholar
  125. 125.
    Corselli M, Chin CJ, Parekh C et al (2013) Perivascular support of human hematopoietic cells. Blood 21:2891–2901Google Scholar
  126. 126.
    Tintut Y, Alfonso Z, Saini T et al (2003) Multilineage potential of cells from the artery wall. Circulation 108(20):2505–2510PubMedGoogle Scholar
  127. 127.
    Hoshino A, Chiba H, Nagai K et al (2008) Human vascular adventitial fibroblasts contain mesenchymal stem/progenitor cells. Biochem Biophys Res Commun 368(2):305–310PubMedGoogle Scholar
  128. 128.
    Sartore S, Chiavegato A, Faggin E et al (2001) Contribution of adventitial fibroblasts to neointima formation and vascular remodeling: from innocent bystander to active participant. Circ Res 89(12):1111–1121PubMedGoogle Scholar
  129. 129.
    Siow RC, Mallawaarachchi CM, Weissberg PL (2003) Migration of adventitial myofibroblasts following vascular balloon injury: insights from in vivo gene transfer to rat carotid arteries. Cardiovasc Res 59(1):212–221PubMedGoogle Scholar
  130. 130.
    Hu Y, Zhang Z, Torsney E et al (2004) Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J Clin Invest 113(9):1258–1265PubMedCentralPubMedGoogle Scholar
  131. 131.
    Haurani MJ, Pagano PJ (2007) Adventitial fibroblast reactive oxygen species as autacrine and paracrine mediators of remodeling: bellwether for vascular disease? Cardiovasc Res 75(4):679–689PubMedGoogle Scholar
  132. 132.
    Herrmann J, Samee S, Chade A et al (2005) Differential effect of experimental hypertension and hypercholesterolemia on adventitial remodeling. Arterioscler Thromb Vasc Biol 25(2):447–453PubMedGoogle Scholar
  133. 133.
    Stenmark KR, Davie N, Frid M et al (2006) Role of the adventitia in pulmonary vascular remodeling. Physiology (Bethesda) 21:134–145Google Scholar
  134. 134.
    Caplan AI (2008) All MSCs are pericytes? Cell Stem Cell 3(3):229–230PubMedGoogle Scholar
  135. 135.
    Corselli M, Chen CW, Sun B et al (2012) The tunica adventitia of human arteries and veins as a source of mesenchymal stem cells. Stem Cells Dev 21(8):1299–1308PubMedCentralPubMedGoogle Scholar
  136. 136.
    Rao M, Ahrlund-Richter L, Kaufman DS (2012) Concise review: cord blood banking, transplantation and induced pluripotent stem cell: success and opportunities. Stem Cells 30(1):55–60PubMedGoogle Scholar
  137. 137.
    Broxmeyer HE (2008) Cord blood hematopoietic stem cell transplantation. In: StemBook [Internet]. Harvard Stem Cell Institute, Cambridge. Available from: http://www.ncbi.nlm.nih.gov/books/NBK44751/
  138. 138.
    Morigi M, Rota C, Montemurro T et al (2010) Life-sparing effect of human cord blood-mesenchymal stem cells in experimental acute kidney injury. Stem Cells 28(3):513–522PubMedGoogle Scholar
  139. 139.
    Zanier ER, Montinaro M, Vigano M et al (2011) Human umbilical cord blood mesenchymal stem cells protect mice brain after trauma. Crit Care Med 39(11):2501–2510PubMedGoogle Scholar
  140. 140.
    Pierro M, Ionescu L, Montemurro T et al (2013) Short-term, long-term and paracrine effect of human umbilical cord-derived stem cells in lung injury prevention and repair in experimental bronchopulmonary dysplasia. Thorax 68(5):475–484PubMedGoogle Scholar
  141. 141.
    Zhang X, Hirai M, Cantero S et al (2011) Isolation and characterization of mesenchymal stem cells from human umbilical cord blood: re-evaluation of critical factors for successful isolation and high ability to proliferate and differentiate to chondrocytes as compared to mesenchymal stem cells from bone marrow and adipose tissue. J Cell Biochem 112(4):1206–1218PubMedGoogle Scholar
  142. 142.
    Avanzini MA, Bernardo ME, Cometa AM et al (2009) Generation of mesenchymal stromal cells in the presence of platelet lysate: a phenotypic and functional comparison of umbilical cord blood- and bone marrow-derived progenitors. Haematologica 94(12):1649–1660PubMedCentralPubMedGoogle Scholar
  143. 143.
    Zeddou M, Briquet A, Relic B et al (2010) The umbilical cord matrix is a better source of mesenchymal stem cells (MSC) than the umbilical cord blood. Cell Biol Int 34(7):693–701PubMedGoogle Scholar
  144. 144.
    Kogler G, Sensken S, Airey JA et al (2004) A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J Exp Med 200(2):123–135PubMedCentralPubMedGoogle Scholar
  145. 145.
    van de Ven C, Collins D, Bradley MB et al (2007) The potential of umbilical cord blood multipotent stem cells for non-hematopoietic tissue and cell regeneration. Exp Hematol 35(12):1753–1765PubMedGoogle Scholar
  146. 146.
    McGuckin C, Jurga M, Ali H et al (2008) Culture of embryonic-like stem cells from human umbilical cord blood and onward differentiation to neural cells in vitro. Nat Protoc 3(6):1046–1055PubMedGoogle Scholar
  147. 147.
    Bieback K, Kern S, Kluter H et al (2004) Critical parameters for the isolation of mesenchymal stem cells from umbilical cord blood. Stem Cells 22(4):625–634PubMedGoogle Scholar
  148. 148.
    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(5):1294–1301PubMedGoogle Scholar
  149. 149.
    Montesinos JJ, Flores-Figueroa E, Castillo-Medina S et al (2009) Human mesenchymal stromal cells from adult and neonatal sources: comparative analysis of their morphology, immunophenotype, differentiation patterns and neural protein expression. Cytotherapy 11(2):163–176PubMedGoogle Scholar
  150. 150.
    Takashima Y, Era T, Nakao K et al (2007) Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 129(7):1377–1388PubMedGoogle Scholar
  151. 151.
    LaBonne C, Bronner-Fraser M (1999) Molecular mechanisms of neural crest formation. Annu Rev Cell Dev Biol 15:81–112PubMedGoogle Scholar
  152. 152.
    Le Douarin NM, Creuzet S, Couly G et al (2004) Neural crest cell plasticity and its limits. Development 131(19):4637–4650PubMedGoogle Scholar
  153. 153.
    Dennis JE, Charbord P (2002) Origin and differentiation of human and murine stroma. Stem Cells 20(3):205–214PubMedGoogle Scholar
  154. 154.
    Hungerford JE, Little CD (1999) Developmental biology of the vascular smooth muscle cell: building a multilayered vessel wall. J Vasc Res 36(1):2–27PubMedGoogle Scholar
  155. 155.
    Vrancken Peeters MP, Gittenberger-de Groot AC, Mentink MM, Poelmann RE (1999) Smooth muscle cells and fibroblasts of the coronary arteries derive from epithelial–mesenchymal transformation of the epicardium. Anat Embryol (Berl) 199(4):367–378Google Scholar
  156. 156.
    Minasi MG, Riminucci M, De Angelis L et al (2002) The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development 129(11):2773–2783PubMedGoogle Scholar
  157. 157.
    Mendes SC, Robin C, Dzierzak E (2005) Mesenchymal progenitor cells localize within hematopoietic sites throughout ontogeny. Development 132(5):1127–1136PubMedGoogle Scholar
  158. 158.
    Morikawa S, Mabuchi Y, Niibe K et al (2009) Development of mesenchymal stem cells partially originate from the neural crest. Biochem Biophys Res Commun 379(4):1114–1119PubMedGoogle Scholar
  159. 159.
    Trentin A, Glavieux-Pardanaud C, Le Douarin NM et al (2004) Self-renewal capacity is a widespread property of various types of neural crest precursor cells. Proc Natl Acad Sci USA 101(13):4495–4500PubMedCentralPubMedGoogle Scholar
  160. 160.
    Korn J, Christ B, Kurz H (2002) Neuroectodermal origin of brain pericytes and vascular smooth muscle cells. J Comp Neurol 442(1):78–88PubMedGoogle Scholar
  161. 161.
    Etchevers HC, Vincent C, Le Douarin NM et al (2001) The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development 128(7):1059–1068PubMedGoogle Scholar
  162. 162.
    Dupin E, Coelho-Aguiar JM (2013) Isolation and differentiation properties of neural crest stem cells. Cytometry A 83(1):38–47PubMedGoogle Scholar
  163. 163.
    Shi H, Zhang T, Qiang L et al (2013) Mesenspheres of neural crest-derived cells enriched from bone marrow stromal cell subpopulation. Neurosci Lett 532:70–75PubMedGoogle Scholar
  164. 164.
    Kruger GM, Mosher JT, Bixby S et al (2002) Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron 35(4):657–669PubMedCentralPubMedGoogle Scholar
  165. 165.
    Morikawa S, Mabuchi Y, Kubota Y et al (2009) Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J Exp Med 206(11):2483–2496PubMedCentralPubMedGoogle Scholar
  166. 166.
    Morrison SJ, White PM, Zock C et al (1999) Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 96(5):737–749PubMedGoogle Scholar
  167. 167.
    Wislet-Gendebien S, Laudet E, Neirinckx V et al (2012) Mesenchymal stem cells and neural crest stem cells from adult bone marrow: characterization of their surprising similarities and differences. Cell Mol Life Sci 69(15):2593–2608PubMedGoogle Scholar
  168. 168.
    Lee G, Kim H, Elkabetz Y et al (2007) Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells. Nat Biotechnol 25(12):1468–1475PubMedGoogle Scholar
  169. 169.
    Nagoshi N, Shibata S, Nakamura M et al (2009) Neural crest-derived stem cells display a wide variety of characteristics. J Cell Biochem 107(6):1046–1052PubMedGoogle Scholar
  170. 170.
    Yamashita J, Itoh H, Hirashima M et al (2000) Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408(6808):92–96PubMedGoogle Scholar
  171. 171.
    Brachvogel B, Moch H, Pausch F et al (2005) Perivascular cells expressing annexin A5 define a novel mesenchymal stem cell-like population with the capacity to differentiate into multiple mesenchymal lineages. Development 132(11):2657–2668PubMedGoogle Scholar
  172. 172.
    Nelander S, Mostad P, Lindahl P (2003) Prediction of cell type-specific gene modules: identification and initial characterization of a core set of smooth muscle-specific genes. Genome Res 13(8):1838–1854PubMedCentralPubMedGoogle Scholar
  173. 173.
    Paredes B, Santana A, Arribas MI et al (2010) Phenotypic differences during the osteogenic differentiation of single cell-derived clones isolated from human lipoaspirates. J Tissue Eng Regen Med 5:589–599PubMedGoogle Scholar
  174. 174.
    Muller AM, Mehrkens A, Schafer DJ et al (2010) Towards an intraoperative engineering of osteogenic and vasculogenic grafts from the stromal vascular fraction of human adipose tissue. Eur Cell Mater 19:127–135PubMedGoogle Scholar
  175. 175.
    Cheung WK, Working DM, Galuppo LD et al (2010) Osteogenic comparison of expanded and uncultured adipose stromal cells. Cytotherapy 12(4):554–562PubMedGoogle Scholar
  176. 176.
    Rajashekhar G, Traktuev DO, Roell WC et al (2008) IFATS collection: adipose stromal cell differentiation is reduced by endothelial cell contact and paracrine communication: role of canonical Wnt signaling. Stem Cells 26(10):2674–2681PubMedGoogle Scholar
  177. 177.
    Meury T, Verrier S, Alini M (2006) Human endothelial cells inhibit BMSC differentiation into mature osteoblasts in vitro by interfering with osterix expression. J Cell Biochem 98(4):992–1006PubMedGoogle Scholar
  178. 178.
    Dahl JA, Duggal S, Coulston N et al (2008) Genetic and epigenetic instability of human bone marrow mesenchymal stem cells expanded in autologous serum or fetal bovine serum. Int J Dev Biol 52(8):1033–1042PubMedGoogle Scholar
  179. 179.
    Rosland GV, Svendsen A, Torsvik A et al (2009) Long-term cultures of bone marrow-derived human mesenchymal stem cells frequently undergo spontaneous malignant transformation. Cancer Res 69(13):5331–5339PubMedGoogle Scholar
  180. 180.
    Ren Z, Wang J, Zhu W et al (2011) Spontaneous transformation of adult mesenchymal stem cells from cynomolgus macaques in vitro. Exp Cell Res 317(20):2950–2957PubMedGoogle Scholar
  181. 181.
    Torsvik A, Rosland GV, Svendsen A et al (2010) Spontaneous malignant transformation of human mesenchymal stem cells reflects cross-contamination: putting the research field on track—letter. Cancer Res 70(15):6393–6396PubMedGoogle Scholar
  182. 182.
    Meliga E, Strem BM, Duckers HJ et al (2007) Adipose-derived cells. Cell Transplant 16(9):963–970PubMedGoogle Scholar
  183. 183.
    Tarnok A, Ulrich H, Bocsi J (2010) Phenotypes of stem cells from diverse origin. Cytometry A 77(1):6–10PubMedGoogle Scholar
  184. 184.
    Schaffler A, Buchler C (2007) Concise review: adipose tissue-derived stromal cells—basic and clinical implications for novel cell-based therapies. Stem Cells 25(4):818–827PubMedGoogle Scholar
  185. 185.
    James AW, Zara JN, Zhang X et al (2012) Perivascular stem cells: a prospectively purified mesenchymal stem cell population for bone tissue engineering. Stem Cells Transl Med 1(6):510–519PubMedCentralPubMedGoogle Scholar
  186. 186.
    Bruder SP, Jaiswal N, Ricalton NS et al (1998) Mesenchymal stem cells in osteobiology and applied bone regeneration. Clin Orthop Relat Res 355 Suppl:S247–S256PubMedGoogle Scholar
  187. 187.
    Kang SW, Bae JH, Park SA et al (2012) Combination therapy with BMP-2 and BMSCs enhances bone healing efficacy of PCL scaffold fabricated using the 3D plotting system in a large segmental defect model. Biotechnol Lett 34(7):1375–1384PubMedGoogle Scholar
  188. 188.
    Zhu S, Zhang B, Man C et al (2011) NEL-like molecule-1-modified bone marrow mesenchymal stem cells/poly lactic-co-glycolic acid composite improves repair of large osteochondral defects in mandibular condyle. Osteoarthritis Cartilage 19(6):743–750PubMedGoogle Scholar
  189. 189.
    Monteiro BS, Del Carlo RJ, Argolo-Neto NM et al (2012) Association of mesenchymal stem cells with platelet rich plasma on the repair of critical calvarial defects in mice. Acta Cir Bras 27(3):201–209PubMedGoogle Scholar
  190. 190.
    Monteiro BS, Argolo-Neto NM, Nardi NB et al (2012) Treatment of critical defects produced in calvaria of mice with mesenchymal stem cells. An Acad Bras Cienc 84(3):841–851PubMedGoogle Scholar
  191. 191.
    Koob S, Torio-Padron N, Stark GB et al (2011) Bone formation and neovascularization mediated by mesenchymal stem cells and endothelial cells in critical-sized calvarial defects. Tissue Eng Part A 17(3–4):311–321PubMedGoogle Scholar
  192. 192.
    Agacayak S, Gulsun B, Ucan MC et al (2012) Effects of mesenchymal stem cells in critical size bone defect. Eur Rev Med Pharmacol Sci 16(5):679–686PubMedGoogle Scholar
  193. 193.
    Osugi M, Katagiri W, Yoshimi R et al (2012) Conditioned media from mesenchymal stem cells enhanced bone regeneration in rat calvarial bone defects. Tissue Eng Part A 18(13–14):1479–1489PubMedCentralPubMedGoogle Scholar
  194. 194.
    Stephan SJ, Tholpady SS, Gross B et al (2010) Injectable tissue-engineered bone repair of a rat calvarial defect. Laryngoscope 120(5):895–901PubMedCentralPubMedGoogle Scholar
  195. 195.
    Yang Q, Peng J, Lu SB et al (2011) Evaluation of an extracellular matrix-derived acellular biphasic scaffold/cell construct in the repair of a large articular high-load-bearing osteochondral defect in a canine model. Chin Med J (Engl) 124(23):3930–3938Google Scholar
  196. 196.
    Mokbel A, El-Tookhy O, Shamaa AA et al (2011) Homing and efficacy of intra-articular injection of autologous mesenchymal stem cells in experimental chondral defects in dogs. Clin Exp Rheumatol 29(2):275–284PubMedGoogle Scholar
  197. 197.
    Field JR, McGee M, Stanley R et al (2011) The efficacy of allogeneic mesenchymal precursor cells for the repair of an ovine tibial segmental defect. Vet Comp Orthop Traumatol 24(2):113–121PubMedGoogle Scholar
  198. 198.
    Reichert JC, Cipitria A, Epari DR et al (2012) A tissue engineering solution for segmental defect regeneration in load-bearing long bones. Sci Transl Med 4(141):141ra93PubMedGoogle Scholar
  199. 199.
    Marquass B, Schulz R, Hepp P et al (2011) Matrix-associated implantation of predifferentiated mesenchymal stem cells versus articular chondrocytes: in vivo results of cartilage repair after 1 year. Am J Sports Med 39(7):1401–1412PubMedGoogle Scholar
  200. 200.
    Khojasteh A, Behnia H, Dashti SG et al (2012) Current trends in mesenchymal stem cell application in bone augmentation: a review of the literature. J Oral Maxillofac Surg 70(4):972–982PubMedGoogle Scholar
  201. 201.
    Bruder SP, Fink DJ, Caplan AI (1994) Mesenchymal stem cells in bone development, bone repair, and skeletal regeneration therapy. J Cell Biochem 56(3):283–294PubMedGoogle Scholar
  202. 202.
    Cao L, Liu G, Gan Y et al (2012) The use of autologous enriched bone marrow MSCs to enhance osteoporotic bone defect repair in long-term estrogen deficient goats. Biomaterials 33(20):5076–5084PubMedGoogle Scholar
  203. 203.
    Wang Z, Goh J, De Das S et al (2006) Efficacy of bone marrow-derived stem cells in strengthening osteoporotic bone in a rabbit model. Tissue Eng 12(7):1753–1761PubMedGoogle Scholar
  204. 204.
    Nde Ocarino M, Boeloni JN, Jorgetti V et al (2010) Intra-bone marrow injection of mesenchymal stem cells improves the femur bone mass of osteoporotic female rats. Connect Tissue Res 51(6):426–433Google Scholar
  205. 205.
    Turgeman G, Zilberman Y, Zhou S et al (2002) Systemically administered rhBMP-2 promotes MSC activity and reverses bone and cartilage loss in osteopenic mice. J Cell Biochem 86(3):461–474PubMedGoogle Scholar
  206. 206.
    Bragdon B, Moseychuk O, Saldanha S et al (2011) Bone morphogenetic proteins: a critical review. Cell Signal 23(4):609–620PubMedGoogle Scholar
  207. 207.
    Voumvourakis KI, Antonelou R, Kitsos DK et al (2011) TGF-beta/BMPs: crucial crossroad in neural autoimmune disorders. Neurochem Int 59(5):542–550PubMedGoogle Scholar
  208. 208.
    Tang YC, Tang W, Tian WD et al (2006) A study on repairing mandibular defect by means of tissue-engineering and human bone morphogenetic protein-2 gene transfection in osteoporotic rats. Zhonghua Kou Qiang Yi Xue Za Zhi 41(7):430–431PubMedGoogle Scholar
  209. 209.
    Turgeman G, Pittman DD, Muller R et al (2001) Engineered human mesenchymal stem cells: a novel platform for skeletal cell mediated gene therapy. J Gene Med 3(3):240–251PubMedGoogle Scholar
  210. 210.
    Egermann M, Baltzer AW, Adamaszek S et al (2006) Direct adenoviral transfer of bone morphogenetic protein-2 cDNA enhances fracture healing in osteoporotic sheep. Hum Gene Ther 17(5):507–517PubMedGoogle Scholar
  211. 211.
    Zhang XS, Linkhart TA, Chen ST et al (2004) Local ex vivo gene therapy with bone marrow stromal cells expressing human BMP4 promotes endosteal bone formation in mice. J Gene Med 6(1):4–15PubMedGoogle Scholar
  212. 212.
    Hu J, Qi MC, Zou SJ et al (2007) Callus formation enhanced by BMP-7 ex vivo gene therapy during distraction osteogenesis in rats. J Orthop Res 25(2):241–251PubMedGoogle Scholar
  213. 213.
    Askarinam A, James AW, Zara JN et al (2013) Human perivascular stem cells show enhanced osteogenesis and vasculogenesis with Nell-1 protein. Tissue Eng Part A 19:1386–1397PubMedGoogle Scholar
  214. 214.
    Zhao Y, Li T, Wei X et al (2012) Mesenchymal stem cell transplantation improves regional cardiac remodeling following ovine infarction. Stem Cells Transl Med 1(9):685–695PubMedCentralPubMedGoogle Scholar
  215. 215.
    Roura S, Bago JR, Soler-Botija C et al (2012) Human umbilical cord blood-derived mesenchymal stem cells promote vascular growth in vivo. Plos One 7(11):e49447PubMedCentralPubMedGoogle Scholar
  216. 216.
    Zheng SX, Weng YL, Zhou CQ et al (2012) Comparison of cardiac stem cells and mesenchymal stem cells transplantation on the cardiac electrophysiology in rats with myocardial infarction. Stem Cell Rev 9:339–349Google Scholar
  217. 217.
    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(4):e35685PubMedCentralPubMedGoogle Scholar
  218. 218.
    van den Akker F, Deddens JC, Doevendans PA et al (2012) Cardiac stem cell therapy to modulate inflammation upon myocardial infarction. Biochim Biophys Acta 830:2449–2458Google Scholar
  219. 219.
    Hu X, Yu SP, Fraser JL et al (2008) Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. J Thorac Cardiovasc Surg 135(4):799–808PubMedGoogle Scholar
  220. 220.
    Shabbir A, Zisa D, Suzuki G et al (2009) Heart failure therapy mediated by the trophic activities of bone marrow mesenchymal stem cells: a noninvasive therapeutic regimen. Am J Physiol Heart Circ Physiol 296(6):H1888–H1897PubMedCentralPubMedGoogle Scholar
  221. 221.
    Zhu K, Lai H, Guo C et al (2012) Novel vascular endothelial growth factor gene delivery system-manipulated mesenchymal stem cells repair infarcted myocardium. Exp Biol Med (Maywood) 237(6):678–687Google Scholar
  222. 222.
    Huang XP, Sun Z, Miyagi Y et al (2010) Differentiation of allogeneic mesenchymal stem cells induces immunogenicity and limits their long-term benefits for myocardial repair. Circulation 122(23):2419–2429PubMedGoogle Scholar
  223. 223.
    Gao XR, Tan YZ, Wang HJ (2011) Overexpression of Csx/Nkx2.5 and GATA-4 enhances the efficacy of mesenchymal stem cell transplantation after myocardial infarction. Circ J 75(11):2683–2691PubMedGoogle Scholar
  224. 224.
    Li XH, Fu YH, Lin QX et al (2012) Induced bone marrow mesenchymal stem cells improve cardiac performance of infarcted rat hearts. Mol Biol Rep 39(2):1333–1342PubMedGoogle Scholar
  225. 225.
    Tang JM, Wang JN, Zhang L et al (2011) VEGF/SDF-1 promotes cardiac stem cell mobilization and myocardial repair in the infarcted heart. Cardiovasc Res 91(3):402–411PubMedCentralPubMedGoogle Scholar
  226. 226.
    Katare R, Riu F, Mitchell K et al (2011) Transplantation of human pericyte progenitor cells improves the repair of infarcted heart through activation of an angiogenic program involving micro-RNA-132. Circ Res 109(8):894–906PubMedCentralPubMedGoogle Scholar
  227. 227.
    Chen CW, Okada M, Proto JD et al (2013) Human pericytes for ischemic heart repair. Stem Cells 31(2):305–316PubMedCentralPubMedGoogle Scholar
  228. 228.
    De Ugarte DA et al (2003) Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 174(3):101–109PubMedGoogle Scholar
  229. 229.
    Rodriguez AM et al (2005) The human adipose tissue is a source of multipotent stem cells. Biochimie 87(1):125–128PubMedGoogle Scholar
  230. 230.
    Lindroos B et al (2009) Serum-free, xeno-free culture media maintain the proliferation rate and multipotentiality of adipose stem cells in vitro. Cytotherapy 11(7):958–972PubMedGoogle Scholar
  231. 231.
    Schreml S et al (2009) Harvesting human adipose tissue-derived adult stem cells: resection versus liposuction. Cytotherapy 11(7):947–957PubMedGoogle Scholar
  232. 232.
    Sensebe L, Bourin P (2009) Mesenchymal stem cells for therapeutic purposes. Transplantation 87(9 Suppl):S49–S53PubMedGoogle Scholar
  233. 233.
    Franco Lambert AP et al (2009) Differentiation of human adipose-derived adult stem cells into neuronal tissue: does it work? Differentiation 77(3):221–228PubMedGoogle Scholar
  234. 234.
    Campagnoli C et al (2001) Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 98(8):2396–2402PubMedGoogle Scholar
  235. 235.
    Villaron EM et al (2004) Mesenchymal stem cells are present in peripheral blood and can engraft after allogeneic hematopoietic stem cell transplantation. Haematologica 89(12):1421–1427PubMedGoogle Scholar
  236. 236.
    Alsalameh S et al (2004) Identification of mesenchymal progenitor cells in normal and osteoarthritic human articular cartilage. Arthritis Rheum 50(5):1522–1532PubMedGoogle Scholar
  237. 237.
    Hiraoka K et al (2006) Mesenchymal progenitor cells in adult human articular cartilage. Biorheology 43(3–4):447–454PubMedGoogle Scholar
  238. 238.
    Erices A, Conget P, Minguell JJ (2000) Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 109(1):235–242PubMedGoogle Scholar
  239. 239.
    Secco M et al (2009) Gene expression profile of mesenchymal stem cells from paired umbilical cord units: cord is different from blood. Stem Cell Rev 5(4):387–401PubMedCentralPubMedGoogle Scholar
  240. 240.
    Jager M et al (2009) Cord blood—an alternative source for bone regeneration. Stem Cell Rev 5(3):266–277PubMedGoogle Scholar
  241. 241.
    Bieback K, Kluter H (2007) Mesenchymal stromal cells from umbilical cord blood. Curr Stem Cell Res Ther 2(4):310–323PubMedGoogle Scholar
  242. 242.
    Gronthos S et al (2000) Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA 97(25):13625–13630PubMedCentralPubMedGoogle Scholar
  243. 243.
    Nakamura S et al (2009) Stem cell proliferation pathways comparison between human exfoliated deciduous teeth and dental pulp stem cells by gene expression profile from promising dental pulp. J Endod 35(11):1536–1542PubMedGoogle Scholar
  244. 244.
    Huang GT, Gronthos S, Shi S (2009) Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. J Dent Res 88(9):792–806PubMedCentralPubMedGoogle Scholar
  245. 245.
    Valtieri M, Sorrentino A (2008) The mesenchymal stromal cell contribution to homeostasis. J Cell Physiol 217(2):296–300PubMedGoogle Scholar
  246. 246.
    Shi S et al (2005) The efficacy of mesenchymal stem cells to regenerate and repair dental structures. Orthod Craniofac Res 8(3):191–199PubMedGoogle Scholar
  247. 247.
    Schuring AN et al (2011) Characterization of endometrial mesenchymal stem-like cells obtained by endometrial biopsy during routine diagnostics. Fertil Steril 95(1):423–426PubMedGoogle Scholar
  248. 248.
    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(2):58PubMedCentralPubMedGoogle Scholar
  249. 249.
    Lanzoni G et al (2009) Isolation of stem cell populations with trophic and immunoregulatory functions from human intestinal tissues: potential for cell therapy in inflammatory bowel disease. Cytotherapy 11(8):1020–1031PubMedGoogle Scholar
  250. 250.
    Arai F et al (2002) Mesenchymal stem cells in perichondrium express activated leukocyte cell adhesion molecule and participate in bone marrow formation. J Exp Med 195(12):1549–1563PubMedCentralPubMedGoogle Scholar
  251. 251.
    O’Driscoll SW, Fitzsimmons JS (2001) The role of periosteum in cartilage repair. Clin Orthop Relat Res 391:S190–S207PubMedGoogle Scholar
  252. 252.
    In ‘t Anker PS (2004) Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 22(7):1338–1345PubMedGoogle Scholar
  253. 253.
    Rotter N et al (2008) Isolation and characterization of adult stem cells from human salivary glands. Stem Cells Dev 17(3):509–518PubMedGoogle Scholar
  254. 254.
    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(1):105–110PubMedGoogle Scholar
  255. 255.
    Campagnolo P et al (2010) Human adult vena saphena contains perivascular progenitor cells endowed with clonogenic and proangiogenic potential. Circulation 121(15):1735–1745PubMedCentralPubMedGoogle Scholar
  256. 256.
    Mariotti E, Mirabelli P, Abate G, Schiattarella M, Martinelli P, Fortunato G et al (2008) Comparative characteristics of mesenchymal stem cells from human bone marrow and placenta: CD10, CD49d, and CD56 make a difference. Stem Cells Dev 17(6):1039–1041PubMedGoogle Scholar
  257. 257.
    Gronthos S, Franklin DM, Leddy HA, Robey PG, Storms RW, Gimble JM (2001) Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 189(1):54–63PubMedGoogle Scholar
  258. 258.
    Niehage C, Steenblock C, Pursche T, Bornhäuser M, Corbeil D, Hoflack B (2011) The cell surface proteome of human mesenchymal stromal cells. Plos One 6(5):e20399PubMedCentralPubMedGoogle Scholar
  259. 259.
    Gimble JM, Katz AJ, Bunnell BA (2007) Adipose-derived stem cells for regenerative medicine. Circ Res 100(9):1249–1260PubMedGoogle Scholar
  260. 260.
    Dar A, Domev H, Ben-Yosef O, Tzukerman M, Zeevi-Levin N, Novak A et al (2012) Multipotent vasculogenic pericytes from human pluripotent stem cells promote recovery of murine ischemic limb. Circulation 125(1):87–99PubMedGoogle Scholar
  261. 261.
    Brooke G, Tong H, Levesque J-P, Atkinson K (2008) Molecular trafficking mechanisms of multipotent mesenchymal stem cells derived from human bone marrow and placenta. Stem Cells Dev 17(5):929–940PubMedGoogle Scholar
  262. 262.
    Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U et al (2005) Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 33(11):1402–1416PubMedGoogle Scholar
  263. 263.
    Tallone T, Realini C, Böhmler A, Kornfeld C, Vassalli G, Moccetti T et al (2011) Adult human adipose tissue contains several types of multipotent cells. J Cardiovasc Transl Res 4(2):200–210PubMedGoogle Scholar
  264. 264.
    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(2):161–176PubMedCentralPubMedGoogle Scholar
  265. 265.
    Zimmerlin L, Donnenberg VS, Pfeifer ME, Meyer EM, Péault B, Rubin JP et al (2009) Stromal vascular progenitors in adult human adipose tissue. Cytometry A 77(1):22–30Google Scholar
  266. 266.
    Campioni DD, Moretti SS, Ferrari LL, Punturieri MM, Castoldi GLG, Lanza FF (2006) Immunophenotypic heterogeneity of bone marrow-derived mesenchymal stromal cells from patients with hematologic disorders: correlation with bone marrow microenvironment. Haematologica 91(3):364–368PubMedGoogle Scholar
  267. 267.
    Bűhring H-J, Battula VL, Treml S, Schewe B, Kanz L, Vogel W (2007) Novel markers for the prospective isolation of human MSC. Ann NY Acad Sci 1106:262–271PubMedGoogle Scholar
  268. 268.
    Masuda H, Anwar SS, Bűhring H-J, Rao JR, Gargett CE (2012) A novel marker of human endometrial mesenchymal stem-like cells. Cell Transpl 21(10):2201–2214Google Scholar
  269. 269.
    Flores-Torales E, Orozco-Barocio A, Gonzalez-Ramella OR, Carrasco-Yalan A, Gazarian K, Cuneo-Pareto S (2010) The CD271 expression could be alone for establisher phenotypic marker in bone marrow-derived mesenchymal stem cells. Folia Histochem Cytobiol 48(4):682–686PubMedGoogle Scholar
  270. 270.
    Zimmerlin L et al (2010) Stromal vascular progenitors in adult human adipose tissue. Cytometry A 77(1):22–30PubMedGoogle Scholar
  271. 271.
    Djouad F, Fritz V, Apparailly F et al (2005) Reversal of the immunosuppressive properties of mesenchymal stem cells by tumor necrosis factor alpha in collagen-induced arthritis. Arthritis Rheum 52(5):1595–1603PubMedGoogle Scholar
  272. 272.
    Guillot PV, De Bari C, Dell’Accio F et al (2008) Comparative osteogenic transcription profiling of various fetal and adult mesenchymal stem cell sources. Differentiation 76(9):946–957PubMedGoogle Scholar
  273. 273.
    Murphy JM, Fink DJ, Hunziker EB et al (2003) Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum 48(12):3464–3474PubMedGoogle Scholar
  274. 274.
    Hillel AT, Taube JM, Cornish TC et al (2010) Characterization of human mesenchymal stem cell-engineered cartilage: analysis of its ultrastructure, cell density and chondrocyte phenotype compared to native adult and fetal cartilage. Cells Tissues Organs 191(1):12–20PubMedGoogle Scholar
  275. 275.
    Erickson IE, Huang AH, Chung C et al (2009) Differential maturation and structure-function relationships in mesenchymal stem cell- and chondrocyte-seeded hydrogels. Tissue Eng Part A 15(5):1041–1052PubMedCentralPubMedGoogle Scholar
  276. 276.
    Noth U, Steinert AF, Tuan RS (2008) Technology insight: adult mesenchymal stem cells for osteoarthritis therapy. Nat Clin Pract Rheumatol 4(7):371–380PubMedGoogle Scholar
  277. 277.
    Wang N, Ren GD, Zhou Z et al (2012) Cooperation of myocardin and Smad2 in inducing differentiation of mesenchymal stem cells into smooth muscle cells. IUBMB Life 64(4):331–339PubMedGoogle Scholar
  278. 278.
    Uysal AC, Mizuno H (2010) Tendon regeneration and repair with adipose derived stem cells. Curr Stem Cell Res Ther 5(2):161–167PubMedGoogle Scholar
  279. 279.
    Leroux L, Descamps B, Tojais NF et al (2010) Hypoxia preconditioned mesenchymal stem cells improve vascular and skeletal muscle fiber regeneration after ischemia through a Wnt4-dependent pathway. Mol Ther 18(8):1545–1552PubMedCentralPubMedGoogle Scholar
  280. 280.
    Chen J, Li Y, Katakowski M et al (2003) Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J Neurosci Res 73(6):778–786PubMedGoogle Scholar
  281. 281.
    Rosova I, Dao M, Capoccia B et al (2008) Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells 26(8):2173–2182PubMedCentralPubMedGoogle Scholar
  282. 282.
    Gupta PK, Chullikana A, Parakh R et al (2013) A double-blind randomized placebo controlled phase I/II study assessing the safety and efficacy of allogeneic bone marrow derived mesenchymal stem cell in critical limb ischemia. J Transl Med 11:143PubMedCentralPubMedGoogle Scholar
  283. 283.
    Serbeniuk TsV, Sychev VS, Lelekova TV (1976) Bilevel organization of the spinal center of the frog lymph heart. Nauchnye Doki Vyss Shkoly Biol Nauki 7:82–86PubMedGoogle Scholar
  284. 284.
    Laflamme MA, Murry CE (2005) Regenerating the heart. Nat Biotechnol 23(7):845–856PubMedGoogle Scholar
  285. 285.
    Burst V, Putsch F, Kubacki T et al (2013) Survival and distribution of injected haematopoietic stem cells in acute kidney injury. Nephrol Dial Transpl 28:1131–1139Google Scholar
  286. 286.
    Wise AF, Ricardo SD (2012) Mesenchymal stem cells in kidney inflammation and repair. Nephrology (Carlton) 17(1):1–10Google Scholar
  287. 287.
    Domínguez-Bendala J, Lanzoni G et al (2012) Concise review: mesenchymal stem cells for diabetes. Stem Cells Transl Med 1(1):59–63Google Scholar
  288. 288.
    Dai LJ, Li HY, Guan LX et al (2009) The therapeutic potential of bone marrow-derived mesenchymal stem cells on hepatic cirrhosis. Stem Cell Res 2(1):16–25PubMedGoogle Scholar
  289. 289.
    Ishikawa T, Banas A, Hagiwara K et al (2010) Stem cells for hepatic regeneration: the role of adipose tissue derived mesenchymal stem cells. Curr Stem Cell Res Ther 5(2):182–189PubMedGoogle Scholar
  290. 290.
    Aquino JB, Bolontrade MF, Garcia MG et al (2010) Mesenchymal stem cells as therapeutic tools and gene carriers in liver fibrosis and hepatocellular carcinoma. Gene Ther 17(6):692–708PubMedGoogle Scholar
  291. 291.
    Kim N, Im KI, Lim JY et al (2013) Mesenchymal stem cells for the treatment and prevention of graft-versus-host disease: experiments and practice. Ann Hematol 92(10):1295–1308Google Scholar
  292. 292.
    Silla L, Valim V, Amorin B et al (2013) A safety and feasibility study with platelet lysate expanded bone marrow mesenchymal stromal cells for the treatment of acute GVHD in Brazil. Leuk Lymphoma. doi: 10.3109/10428194.2013.823495
  293. 293.
    Xia Z, Zhang C, Zeng Y et al (2012) Transplantation of BMSCs expressing hVEGF(165)/hBD3 promotes wound healing in rats with combined radiation-wound injury. Int Wound J. doi: 10.1111/j.1742-481x.2012.01090.x
  294. 294.
    Kim SO, Na HS, Kwon D et al (2011) Bone-marrow-derived mesenchymal stem cell transplantation enhances closing pressure and leak point pressure in a female urinary incontinence rat model. Urol Int 86(1):110–116PubMedGoogle Scholar
  295. 295.
    Zannettino ACW, Paton S, Arthur A, Khor F, Itescu S, Gimble JM et al (2008) Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 214(2):413–421PubMedGoogle Scholar
  296. 296.
    Zhang R, Liu Y, Yan K et al (2013) Anti-inflammatory and immunomodulatory mechanisms of mesenchymal stem cell transplantation in experimental traumatic brain injury. J Neuroinflammation 10(1):106Google Scholar
  297. 297.
    Kumagai G, Tsoulfas P, Toh S et al (2013) Genetically modified mesenchymal stem cells (MSCs) promote axonal regeneration and prevent hypersensitivity after spinal cord injury. Exp Neurol 248:369–380Google Scholar
  298. 298.
    Jadasz JJ, Kremer D, Göttle P et al (2013) Mesenchymal stem cell conditioning promotes rat oligodendroglial cell maturation. PLoS One 8(8):e71814Google Scholar
  299. 299.
    Danielyan L, Schäfer R, von Ameln-Mayerhofer A et al (2011) Therapeutic efficacy of intranasally delivered mesenchymal stem cells in a rat model of Parkinson disease. Rejuvenation Res 14(1):3–16Google Scholar
  300. 300.
    Stemberger S, Jamnig A, Stefanova N et al (2011) Mesenchymal stem cells in a transgenic mouse model of multiple system atrophy: immunomodulation and neuroprotection. PLoS One 6(5):e19808Google Scholar
  301. 301.
    Hall SR, Tsoyi K, Ith B, Padera RF Jr et al (2013) Mesenchymal stromal cells improve survival during sepsis in the absence of heme oxygenase-1: the importance of neutrophils. Stem Cells 31(2):397–407Google Scholar
  302. 302.
    Curley GF, Ansari B, Hayes M et al (2013) Effects of intratracheal mesenchymal stromal cell therapy during recovery and resolution after ventilator-induced lung injury. Anesthesiology 118(4):924-932Google Scholar
  303. 303.
    Cheng K, Rai P, Plagov A et al (2013) Transplantation of bone marrow-derived MSCs improves cisplatinum-induced renal injury through paracrine mechanisms. Exp Mol Pathol 94(3):466–473Google Scholar

Copyright information

© Springer Basel 2013

Authors and Affiliations

  • Iain R. Murray
    • 1
    • 2
    • 3
  • Christopher C. West
    • 1
    • 2
  • Winters R. Hardy
    • 3
    • 4
  • Aaron W. James
    • 5
  • Tea Soon Park
    • 6
  • Alan Nguyen
    • 5
  • Tulyapruek Tawonsawatruk
    • 1
    • 2
  • Lorenza Lazzari
    • 7
  • Chia Soo
    • 8
  • Bruno Péault
    • 1
    • 2
    • 3
  1. 1.MRC Center for Regenerative MedicineUniversity of EdinburghEdinburghUK
  2. 2.BHF Center for Cardiovascular Science, Queens Medical Research InstituteUniversity of EdinburghEdinburghUK
  3. 3.Orthopedic Hospital Research Center and Broad Stem Cell Center, David Geffen School of MedicineUniversity of CaliforniaLos AngelesUSA
  4. 4.Indiana Center for Vascular Biology and MedicineIndianapolisUSA
  5. 5.Department of Pathology and Laboratory Medicine, David Geffen School of MedicineUniversity of CaliforniaLos AngelesUSA
  6. 6.Institute for Cell EngineeringJohns Hopkins School of MedicineBaltimoreUSA
  7. 7.Cell FactoryFondazione IRCCS Ca’ Granda Ospedale Maggiore PoliclinicoMilanItaly
  8. 8.Division of Plastic and Reconstructive Surgery, Departments of Surgery and Orthopedic Surgery, David Geffen School of MedicineUniversity of CaliforniaLos AngelesUSA

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