Experimental Hematology
Volume 38, Issue 3 , Pages 246-257.e1 , March 2010

Human embryonic stem cell−derived vascular progenitor cells capable of endothelial and smooth muscle cell function

  • Katherine L. Hill

      Affiliations

    • Stem Cell Institute and Department of Medicine, University of Minnesota, Minneapolis, Minn., USA
    • Drs. Hill and Obrtlikova contributed equally to this work as co−first authors.
  • ,
  • Petra Obrtlikova

      Affiliations

    • Stem Cell Institute and Department of Medicine, University of Minnesota, Minneapolis, Minn., USA
    • Clinical Department of Hematology of First Faculty of Medicine and General Teaching Hospital, Charles University, Prague, Czech Republic
    • Drs. Hill and Obrtlikova contributed equally to this work as co−first authors.
  • ,
  • Diego F. Alvarez

      Affiliations

    • Department of Internal Medicine, Pharmacology, Center for Lung Biology, University of South Alabama College of Medicine, Mobile, Ala., USA
  • ,
  • Judy A. King

      Affiliations

    • Department of Internal Medicine, Pharmacology, Center for Lung Biology, University of South Alabama College of Medicine, Mobile, Ala., USA
  • ,
  • Susan A. Keirstead

      Affiliations

    • Stem Cell Institute and Department of Medicine, University of Minnesota, Minneapolis, Minn., USA
  • ,
  • Jeremy R. Allred

      Affiliations

    • Stem Cell Institute and Department of Medicine, University of Minnesota, Minneapolis, Minn., USA
  • ,
  • Dan S. Kaufman

      Affiliations

    • Stem Cell Institute and Department of Medicine, University of Minnesota, Minneapolis, Minn., USA
    • Corresponding Author InformationOffprint requests to: Dan S. Kaufman, M.D., Ph.D., Stem Cell Institute and Department of Medicine, University of Minnesota, Masonic Cancer Center, 525 East River Parkway, Minneapolis, MN 55455

Received 13 September 2009 ,Revised 31 December 2009 ,Accepted 4 January 2010.

References 

  1. Kaufman DS, Lewis RL, Hanson ET, Auerbach R, Plendl J, Thomson JA. Functional endothelial cells derived from rhesus monkey embryonic stem cells. Blood. 2004;103:1325–1332
  2. Fennie C, Cheng J, Dowbenko D, Young P, Lasky LA. CD34+ endothelial cell lines derived from murine yolk sac induce the proliferation and differentiation of yolk sac CD34+ hematopoietic progenitors. Blood. 1995;86:4454–4467
  3. Wang ZZ, Au P, Chen T, et al. Endothelial cells derived from human embryonic stem cells form durable blood vessels in vivo. Nat Biotechnol. 2007;25:317–318
  4. Levenberg S, Zoldan J, Basevitch Y, Langer R. Endothelial potential of human embryonic stem cells. Blood. 2007;110:806–814
  5. Mariappan D, Winkler J, Chen S, Schulz H, Hescheler J, Sachinidis A. Transcriptional profiling of CD31(+) cells isolated from murine embryonic stem cells. Genes Cells. 2009;14:243–260
  6. Saeki K, Yogiashi Y, Nakahara M, et al. Highly efficient and feeder-free production of subculturable vascular endothelial cells from primate embryonic stem cells. J Cell Physiol. 2008;217:261–280
  7. Yamashita J, Itoh H, Hirashima M, et al. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature. 2000;408:92–96
  8. Ferreira LS, Gerecht S, Shieh HF, et al. Vascular progenitor cells isolated from human embryonic stem cells give rise to endothelial and smooth muscle like cells and form vascular networks in vivo. Circ Res. 2007;101:286–294
  9. Vodyanik MA, Bork JA, Thomson JA, Slukvin . Human embryonic stem cell-derived CD34+ cells: efficient production in the coculture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood. 2005;105:617–626
  10. Levenberg S, Golub JS, Amit M, Itskovitz-Eldor J, Langer R. Endothelial cells derived from human embryonic stem cells. Proc Natl Acad Sci U S A. 2002;99:4391–4396
  11. Kaufman DS, Hanson ET, Lewis RL, Auerbach R, Thomson JA. Hematopoietic colony-forming cells derived from human embryonic stem cells. Proc Natl Acad Sci U S A. 2001;98:10716–10721
  12. Wang L, Li L, Shojaei F, et al. Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity. 2004;21:31–41
  13. Gerecht-Nir S, Ziskind A, Cohen S, Itskovitz-Eldor J. Human embryonic stem cells as an in vitro model for human vascular development and the induction of vascular differentiation. Lab Invest. 2003;83:1811–1820
  14. Zambidis ET, Peault B, Park TS, Bunz F, Civin CI. Hematopoietic differentiation of human embryonic stem cells progresses through sequential hematoendothelial, primitive, and definitive stages resembling human yolk sac development. Blood. 2005;106:860–870
  15. Sone M, Itoh H, Yamahara K, et al. Pathway for differentiation of human embryonic stem cells to vascular cell components and their potential for vascular regeneration. Arterioscler Thromb Vasc Biol. 2007;27:2127–2134
  16. Lu SJ, Ivanova Y, Feng Q, Luo C, Lanza R. Hemangioblasts from human embryonic stem cells generate multilayered blood vessels with functional smooth muscle cells. Regen Med. 2009;4:37–47
  17. Huang H, Zhao X, Chen L, et al. Differentiation of human embryonic stem cells into smooth muscle cells in adherent monolayer culture. Biochem Biophys Res Commun. 2006;351:321–327
  18. Drab M, Haller H, Bychkov R, et al. From totipotent embryonic stem cells to spontaneously contracting smooth muscle cells: a retinoic acid and db-cAMP in vitro differentiation model. FASEB J. 1997;11:905–915
  19. Ross JJ, Hong Z, Willenbring B, et al. Cytokine-induced differentiation of multipotent adult progenitor cells into functional smooth muscle cells. J Clin Invest. 2006;116:3139–3149
  20. Cho SW, Moon SH, Lee SH, et al. Improvement of postnatal neovascularization by human embryonic stem cell derived endothelial-like cell transplantation in a mouse model of hindlimb ischemia. Circulation. 2007;116:2409–2419
  21. Hanjaya-Putra D, Gerecht S. Vascular engineering using human embryonic stem cells. Biotechnol Prog. 2009;25:2–9
  22. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282:1145–1147
  23. Tian X, Kaufman DS. Hematopoietic development of human embryonic stem cells in culture. Methods Mol Biol. 2008;430:119–133
  24. Hill KL, Kaufman DS. Hematopoietic differentiation of human embryonic stem cells by cocultivation with stromal layers. Curr Protoc Stem Cell Biol. 2008;6:1F.6.1-1F.6.12.
  25. Woll PS, Morris JK, Painschab MS, et al. Wnt signaling promotes hematoendothelial cell development from human embryonic stem cells. Blood. 2008;111:122–131
  26. Jimenez JJ, Jy W, Mauro LM, Soderland C, Horstman LL, Ahn YS. Endothelial cells release phenotypically and quantitatively distinct microparticles in activation and apoptosis. Thromb Res. 2003;109:175–180
  27. Berckmans RJ, Neiuwland R, Boing AN, Romijn FP, Hack CE, Sturk A. Cell-derived microparticles circulate in healthy humans and support low grade thrombin generation. Thromb Haemost. 2001;85:639–646
  28. Freyssinet JM. Cellular microparticles: what are they bad or good for?. J Thromb Haemost. 2003;1:1655–1662
  29. Kirschenlohr HL, Metcalfe JC, Weissberg PL, Grainger DJ. Proliferation of human aortic vascular smooth muscle cells in culture is modulated by active TGF beta. Cardiovasc Res. 1995;29:848–855
  30. Hirst SJ, Barnes PJ, Twort CH. PDGF isoform-induced proliferation and receptor expression in human cultured airway smooth muscle cells. Am J Physiol. 1996;270(3 Pt 1):L415–L428
  31. Mummery CL, Ward D, Passier R. Differentiation of human embryonic stem cells to cardiomyocytes by coculture with endoderm in serum-free medium. Curr Protoc Stem Cell Biol. 2007;2:1F.2.1-1F.2.14.
  32. Vodyanik MA, Slukvin . Directed differentiation of human embryonic stem cells to dendritic cells. Methods Mol Biol. 2007;407:275–293
  33. Sone M, Itoh H, Yamashita J, et al. Different differentiation kinetics of vascular progenitor cells in primate and mouse embryonic stem cells. Circulation. 2003;107:2085–2088
  34. Kaufman DS, Lewis RL, Hanson ET, Auerbach R, Plendl J, Thomson JA. Functional endothelial cells derived from rhesus monkey embryonic stem cells. Blood. 2004;103:1325–1332
  35. Cai X, Lin Y, Friedrich CC, et al. Bone marrow derived pluripotent cells are pericytes which contribute to vascularization. Stem Cell Rev. 2009;5:437–445
  36. Lozito TP, Taboas JM, Kuo CK, Tuan RS. Mesenchymal stem cell modification of endothelial matrix regulates their vascular differentiation. J Cell Biochem. 2009;107:706–713
  37. Covas DT, Panepucci RA, Fontes AM, et al. Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts. Exp Hematol. 2008;36:642–654
  38. Ema M, Faloon P, Zhang WJ, et al. Combinatorial effects of Flk1 and Tal1 on vascular and hematopoietic development in the mouse. Genes Dev. 2003;17:380–393
  39. Christoforou N, Miller RA, Hill CM, Jie CC, McCallion AS, Gearhart JD. Mouse ES cell-derived cardiac precursor cells are multipotent and facilitate identification of novel cardiac genes. J Clin Invest. 2008;118:894–903
  40. Moretti A, Caron L, Nakano A, et al. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell. 2006;127:1151–1165
  41. Wu SM, Fujiwara Y, Cibulsky SM, et al. Developmental origin of a bipotential myocardial and smooth muscle cell precursor in the mammalian heart. Cell. 2006;127:1137–1150
  42. Chung YS, Zhang WJ, Arentson E, Kingsley PD, Palis J, Choi K. Lineage analysis of the hemangioblast as defined by FLK1 and SCL expression. Development. 2002;129:5511–5520
  43. Kawai Y, Hosaka K, Kaidoh M, Minami T, Kodama T, Ohhashi T. Heterogeneity in immunohistochemical, genomic, and biological properties of human lymphatic endothelial cells between initial and collecting lymph vessels. Lymphat Res Biol. 2008;6:15–27
  44. Mellgren AM, Smith CL, Olsen GS, et al. Platelet-derived growth factor receptor beta signaling is required for efficient epicardial cell migration and development of two distinct coronary vascular smooth muscle cell populations. Circ Res. 2008;103:1393–1401
  45. Garlanda C, Dejana E. Heterogeneity of endothelial cells. Specific markers. Arterioscler Thromb Vasc Biol. 1997;17:1193–1202
  46. Stevens KR, Pabon L, Muskheli V, Murry CE. Scaffold-free human cardiac tissue patch created from embryonic stem cells. Tissue Eng Part A. 2009;15:1211–1222
  47. Laflamme MA, Zbinden S, Epstein SE, Murry CE. Cell-based therapy for myocardial ischemia and infarction: pathophysiological mechanisms. Annu Rev Pathol Mech Dis. 2007;2:307–339
  48. van Laake LW, Passier R, Monshouwer-Kloots J, et al. Human embryonic stem cell-derived cardiomyocytes survive and mature in the mouse heart and transiently improve function after myocardial infarction. Stem Cell Res. 2007;1:9–24
  49. Leor J, Gerecht S, Cohen S, et al. Human embryonic stem cell transplantation to repair the infarcted myocardium. Heart. 2007;93:1278–1284
  50. Dai W, Field LJ, Rubart M, et al. Survival and maturation of human embryonic stem cell-derived cardiomyocytes in rat hearts. J Mol Cell Cardiol. 2007;43:504–516
  51. Caspi O, Huber I, Kehat I, et al. Transplantation of human embryonic stem cell-derived cardiomyocytes improves myocardial performance in infarcted rat hearts. J Am Coll Cardiol. 2007;50:1884–1893
  52. Passier R, van Laake LW, Mummery CL. Stem-cell-based therapy and lessons from the heart. Nature. 2008;453:322–329
  53. Tendera M, Wojakowski W. Cell therapy—success does not come easy. Eur Heart J. 2009;30:640–641
  54. Rosenzweig A. Cardiac cell therapy—mixed results from mixed cells. N Engl J Med. 2006;355:1274–1277
  55. Kehat I, Kenyagin-Karsenti D, Snir M, et al. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest. 2001;108:407–414
  56. Laflamme MA, Chen KY, Naumova AV, et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol. 2007;25:1015–1024
  57. Mummery C, Ward-van Oostwaard D, Doevendans P, et al. Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation. 2003;107:2733–2740
  58. He JQ, Ma Y, Lee Y, Thomson JA, Kamp TJ. Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization. Circ Res. 2003;93:32–39
  59. Wilber A, Linehan JL, Tian X, et al. Efficient and stable transgene expression in human embryonic stem cells using transposon-mediated gene transfer. Stem Cells. 2007;25:2919–2927
  60. Park IH, Zhao R, West JA, et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature. 2007;451:141–146
  61. Choi KD, Yu J, Smuga-Otto K, et al. Hematopoietic and endothelial differentiation of human induced pluripotent stem cells. Stem Cells. 2009;27:559–567
  62. Zhang J, Wilson GF, Soerens AG, et al. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res. 2009;104:e30–e41

PII: S0301-472X(10)00002-0

doi: 10.1016/j.exphem.2010.01.001

Experimental Hematology
Volume 38, Issue 3 , Pages 246-257.e1 , March 2010