Progress in Pediatric Cardiology
Volume 25, Issue 1 , Pages 37-49 , April 2008

Stem cells in cardiopulmonary development: Implications for novel approaches to therapy for pediatric cardiopulmonary disease

  • Karen Young

      Affiliations

    • Departments of Pediatrics/Neonatology, The Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, USA
    • ,
  • Joshua M. Hare

      Affiliations

    • Departments of Internal Medicine/Cardiology, The Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, USA
    • Corresponding Author InformationCorresponding author. Leonard M Miller School of Medicine, Interdisciplinary Stem Cell Institute and Division of Cardiology, 1124 Clinical Research Building, 1120 NW 14th Street, Miami, FL 33136, USA. Tel.: +305 243 1998; fax: +305 585 5710.

References 

  1. Hoffman JI, Kaplan S. The incidence of congenital heart disease. J Am Coll Cardiol. 2002;39:1890–1900
  2. Bancalari E, Claure N, Sosenko IR. Bronchopulmonary dysplasia: changes in pathogenesis, epidemiology and definition. Semin Neonatol. 2003;8:63–71
  3. Kelly RG, Brown NA, Buckingham ME. The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev Cell. 2001;1:435–440
  4. Mjaatvedt CH, Nakaoka T, Moreno-Rodriguez R, et al. The outflow tract of the heart is recruited from a novel heart-forming field. Dev Biol. 2001;238:97–109
  5. Waldo KL, Kumiski DH, Wallis KT, et al. Conotruncal myocardium arises from a secondary heart field. Development. 2001;128:3179–3188
  6. Buckingham M, Meilhac S, Zaffran S. Building the mammalian heart from two sources of myocardial cells. Nat Rev Genet. 2005;6:826–835
  7. Cai CL, Liang X, Shi Y, et al. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell. 2003;5:877–889
  8. Christoffels VM, Mommersteeg MT, Trowe MO, et al. Formation of the venous pole of the heart from an Nkx2-5-negative precursor population requires Tbx18. Circ Res. 2006;98:1555–1563
  9. Rawles M. The heart-forming areas of the early chick blastoderm. Physiol Zoo. 1943;16:22–42
  10. Redkar A, Montgomery M, Litvin J. Fate map of early avian cardiac progenitor cells. Development. 2001;128:2269–2279
  11. Stalsberg H, DeHaan RL. The precardiac areas and formation of the tubular heart in the chick embryo. Dev Biol. 1969;19:128–159
  12. Eisenberg CA, Eisenberg LM. WNT11 promotes cardiac tissue formation of early mesoderm. Dev Dyn. 1999;216:45–58
  13. Brandon C, Eisenberg LM, Eisenberg CA. WNT signaling modulates the diversification of hematopoietic cells. Blood. 2000;96:4132–4141
  14. Kattman SJ, Huber TL, Keller GM. Multipotent flk-1+ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev Cell. 2006;11:723–732
  15. Meilhac SM, Esner M, Kelly RG, Nicolas JF, Buckingham ME. The clonal origin of myocardial cells in different regions of the embryonic mouse heart. Dev Cell. 2004;6:685–698
  16. 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
  17. 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
  18. Laugwitz KL, Moretti A, Lam J, et al. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature. 2005;433:647–653
  19. Beltrami AP, Barlucchi L, Torella D, et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell. 2003;114:763–776
  20. Oh H, Bradfute SB, Gallardo TD, et al. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A. 2003;100:12313–12318
  21. Matsuura K, Nagai T, Nishigaki N, et al. Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J Biol Chem. 2004;279:11384–11391
  22. Hierlihy AM, Seale P, Lobe CG, Rudnicki MA, Megeney LA. The post-natal heart contains a myocardial stem cell population. FEBS Lett. 2002;530:239–243
  23. Martin CM, Meeson AP, Robertson SM, et al. Persistent expression of the ATP-binding cassette transporter, Abcg2, identifies cardiac SP cells in the developing and adult heart. Dev Biol. 2004;265:262–275
  24. Messina E, De Angelis L, Frati G, et al. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res. 2004;95:911–921
  25. Schultheiss TM, Xydas S, Lassar AB. Induction of avian cardiac myogenesis by anterior endoderm. Development. 1995;121:4203–4214
  26. Gupta M, Gupta MP, Arcilla RA. Molecular regulation of cardiac myogenesis and morphology during development. Prog Pediatr Cardiol. 1998;9:155–170
  27. Foley A, Mercola M. Heart induction: embryology to cardiomyocyte regeneration. Trends Cardiovasc Med. 2004;14:121–125
  28. Brade T, Manner J, Kuhl M. The role of Wnt signalling in cardiac development and tissue remodelling in the mature heart. Cardiovasc Res. 2006;72:198–209
  29. Brand T. Heart development: molecular insights into cardiac specification and early morphogenesis. Dev Biol. 2003;258:1–19
  30. Bittner RE, Schofer C, Weipoltshammer K, et al. Recruitment of bone-marrow-derived cells by skeletal and cardiac muscle in adult dystrophic mdx mice. Anat Embryol (Berl). 1999;199:391–396
  31. Rafii S, Shapiro F, Rimarachin J, et al. Isolation and characterization of human bone marrow microvascular endothelial cells: hematopoietic progenitor cell adhesion. Blood. 1994;84:10–19
  32. Eglitis MA, Mezey E. Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc Natl Acad Sci U S A. 1997;94:4080–4085
  33. Brazelton TR, Rossi FM, Keshet GI, Blau HM. From marrow to brain: expression of neuronal phenotypes in adult mice. Science. 2000;290:1775–1779
  34. Mezey E, Chandross KJ, Harta G, Maki RA, McKercher SR. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science. 2000;290:1779–1782
  35. Petersen BE, Bowen WC, Patrene KD, et al. Bone marrow as a potential source of hepatic oval cells. Science. 1999;284:1168–1170
  36. Theise ND, Badve S, Saxena R, et al. Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology. 2000;31:235–240
  37. Theise ND, Nimmakayalu M, Gardner R, et al. Liver from bone marrow in humans. Hepatology. 2000;32:11–16
  38. Lagasse E, Connors H, Al-Dhalimy M, et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med. 2000;6:1229–1234
  39. Gussoni E, Soneoka Y, Strickland CD, et al. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature. 1999;401:390–394
  40. Mason RJ, Williams MC, Moses HL, Mohla S, Berberich MA. Stem cells in lung development, disease, and therapy. Am J Respir Cell Mol Biol. 1997;16:355–363
  41. Theise ND, Henegariu O, Grove J, et al. Radiation pneumonitis in mice: a severe injury model for pneumocyte engraftment from bone marrow. Exp Hematol. 2002;30:1333–1338
  42. Kotton DN, Ma BY, Cardoso WV, et al. Bone marrow-derived cells as progenitors of lung alveolar epithelium. Development. 2001;128:5181–5188
  43. Ortiz LA, Gambelli F, McBride C, et al. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci U S A. 2003;100:8407–8411
  44. Ianus A, Holz GG, Theise ND, Hussain MA. In vivo derivation of glucose-competent pancreatic endocrine cells from bone marrow without evidence of cell fusion. J Clin Invest. 2003;111:843–850
  45. Hess D, Li L, Martin M, et al. Bone marrow-derived stem cells initiate pancreatic regeneration. Nat Biotechnol. 2003;21:763–770
  46. Okamoto R, Yajima T, Yamazaki M, et al. Damaged epithelia regenerated by bone marrow-derived cells in the human gastrointestinal tract. Nat Med. 2002;8:1011–1017
  47. Brittan M, Hunt T, Jeffery R, et al. Bone marrow derivation of pericryptal myofibroblasts in the mouse and human small intestine and colon. Gut. 2002;50:752–757
  48. Pereira RF, Halford KW, O'Hara MD, et al. Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc Natl Acad Sci U S A. 1995;92:4857–4861
  49. Epperly MW, Guo H, Gretton JE, Greenberger JS. Bone marrow origin of myofibroblasts in irradiation pulmonary fibrosis. Am J Respir Cell Mol Biol. 2003;29:213–224
  50. Grove JE, Lutzko C, Priller J, et al. Marrow-derived cells as vehicles for delivery of gene therapy to pulmonary epithelium. Am J Respir Cell Mol Biol. 2002;27:645–651
  51. Trotman W, Beckett T, Goncz KK, Beatty BG, Weiss DJ. Dual Y chromosome painting and in situ cell-specific immunofluorescence staining in lung tissue: an improved method of identifying donor marrow cells in lung following bone marrow transplantation. Histochem Cell Biol. 2004;121:73–79
  52. Kondo M, Wagers AJ, Manz MG, et al. Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annu Rev Immunol. 2003;21:759–806
  53. Orlic D, Kajstura J, Chimenti S, et al. Bone marrow cells regenerate infarcted myocardium. Nature. 2001;410:701–705
  54. Murry CE, Soonpaa MH, Reinecke H, et al. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature. 2004;428:664–668
  55. Balsam LB, Wagers AJ, Christensen JL, Kofidis T, Weissman IL, Robbins RC. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature. 2004;428:668–673
  56. Nygren JM, Jovinge S, Breitbach M, et al. Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. Nat Med. 2004;10:494–501
  57. Orlic D, Kajstura J, Chimenti S, et al. Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci U S A. 2001;98:10344–10349
  58. Reyes M, Dudek A, Jahagirdar B, Koodie L, Marker PH, Verfaillie CM. Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest. 2002;109:337–346
  59. Tepper OM, Capla JM, Galiano RD, et al. Adult vasculogenesis occurs through in situ recruitment, proliferation, and tubulization of circulating bone marrow-derived cells. Blood. 2005;105:1068–1077
  60. Kalka C, Masuda H, Takahashi T, et al. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci U S A. 2000;97:3422–3427
  61. Hill JM, Zalos G, Halcox JP, et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med. 2003;348:593–600
  62. Schachinger V, Erbs S, Elsasser A, et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med. 2006;355:1210–1221
  63. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276:71–74
  64. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143–147
  65. Haynesworth SE, Baber MA, Caplan AI. Cell surface antigens on human marrow-derived mesenchymal cells are detected by monoclonal antibodies. Bone. 1992;13:69–80
  66. Makino S, Fukuda K, Miyoshi S, et al. Cardiomyocytes can be generated from marrow stromal cells in vitro. J Clin Invest. 1999;103:697–705
  67. Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation. 2002;105:93–98
  68. Shake JG, Gruber PJ, Baumgartner WA, et al. Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects. Ann Thorac Surg. 2002;73:1919–1925discussion 1926
  69. Amado LC, Saliaris AP, Schuleri KH, et al. Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. Proc Natl Acad Sci U S A. 2005;102:11474–11479
  70. Chen SL, Fang WW, Ye F, et al. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am J Cardiol. 2004;94:92–95
  71. Hare J, Dib N, Traverse JH, et al. A double-blind, randomized, placebo controlled clinical trial of allogeneic mesenchymal stem cells for the treatment of patients with acute myocardial infarction. J Am Coll Cardiol. 2007;49:2405-3A
  72. Menasche P. Skeletal muscle satellite cell transplantation. Cardiovasc Res. 2003;58:351–357
  73. Menasche P, Hagege AA, Vilquin JT, et al. Autologous skeletal myoblast transplantation for severe postinfarction left ventricular dysfunction. J Am Coll Cardiol. 2003;41:1078–1083
  74. Leobon B, Garcin I, Menasche P, Vilquin JT, Audinat E, Charpak S. Myoblasts transplanted into rat infarcted myocardium are functionally isolated from their host. Proc Natl Acad Sci U S A. 2003;100:7808–7811
  75. Siminiak T, Fiszer D, Jerzykowska O, et al. Percutaneous trans-coronary-venous transplantation of autologous skeletal myoblasts in the treatment of post-infarction myocardial contractility impairment: the POZNAN trial. Eur Heart J. 2005;26:1188–1195
  76. Dib N, Michler RE, Pagani FD, et al. Safety and feasibility of autologous myoblast transplantation in patients with ischemic cardiomyopathy: four-year follow-up. Circulation. 2005;112:1748–1755
  77. Reinecke H, Minami E, Poppa V, Murry CE. Evidence for fusion between cardiac and skeletal muscle cells. Circ Res. 2004;94:e56–e60
  78. Reinecke H, Poppa V, Murry CE. Skeletal muscle stem cells do not transdifferentiate into cardiomyocytes after cardiac grafting. J Mol Cell Cardiol. 2002;34:241–249
  79. Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol. 1985;87:27–45
  80. Fijnvandraat AC, van Ginneken AC, de Boer PA, et al. Cardiomyocytes derived from embryonic stem cells resemble cardiomyocytes of the embryonic heart tube. Cardiovasc Res. 2003;58:399–409
  81. Maltsev VA, Wobus AM, Rohwedel J, Bader M, Hescheler J. Cardiomyocytes differentiated in vitro from embryonic stem cells developmentally express cardiac-specific genes and ionic currents. Circ Res. 1994;75:233–244
  82. 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
  83. Kehat I, Khimovich L, Caspi O, et al. Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotechnol. 2004;22:1282–1289
  84. Laflamme MA, Gold J, Xu C, et al. Formation of human myocardium in the rat heart from human embryonic stem cells. Am J Pathol. 2005;167:663–671
  85. Steele A, Steele P. Stem cells for repair of the heart. Curr Opin Pediatr. 2006;18:518–523
  86. Kang HJ, Kim HS, Zhang SY, et al. Effects of intracoronary infusion of peripheral blood stem-cells mobilised with granulocyte-colony stimulating factor on left ventricular systolic function and restenosis after coronary stenting in myocardial infarction: the MAGIC cell randomised clinical trial. Lancet. 2004;363:751–756
  87. Balsam LB, Robbins RC. Haematopoietic stem cells and repair of the ischaemic heart. Clin Sci (Lond). 2005;109:483–492
  88. Oettgen P, Boyle AJ, Schulman SP, Hare JM. Cardiac stem cell therapy. Need for optimization of efficacy and safety monitoring. Circulation. 2006;114:353–358
  89. Flake AW. In utero stem cell transplantation. Best Pract Res Clin Obstet Gynaecol. 2004;18:941–958
  90. Liechty KW, MacKenzie TC, Shaaban AF, et al. Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med. 2000;6:1282–1286
  91. Fraidenraich D, Stillwell E, Romero E, et al. Rescue of cardiac defects in id knockout embryos by injection of embryonic stem cells. Science. 2004;306:247–252
  92. Chan J, Waddington SN, O'Donoghue K, et al. Widespread distribution and muscle differentiation of human fetal mesenchymal stem cells after intrauterine transplantation in dystrophic mdx mouse. Stem Cells. 2007;25:875–884
  93. Zimmermann WH, Melnychenko I, Wasmeier G, et al. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med. 2006;12:452–458
  94. Guo XM, Zhao YS, Chang HX, et al. Creation of engineered cardiac tissue in vitro from mouse embryonic stem cells. Circulation. 2006;113:2229–2237
  95. Kofidis T, Lebl DR, Martinez EC, Hoyt G, Tanaka M, Robbins RC. Novel injectable bioartificial tissue facilitates targeted, less invasive, large-scale tissue restoration on the beating heart after myocardial injury. Circulation. 2005;112:I173–I177
  96. Shin'oka T, Matsumura G, Hibino N, et al. Midterm clinical result of tissue-engineered vascular autografts seeded with autologous bone marrow cells. J Thorac Cardiovasc Surg. 2005;129:1330–1338
  97. Zimmermann WH, Didie M, Doker S, et al. Heart muscle engineering: an update on cardiac muscle replacement therapy. Cardiovasc Res. 2006;71:419–429
  98. Schmidt D, Hoerstrup SP. Tissue engineered heart valves based on human cells. Swiss Med Wkly. 2006;136:618–623
  99. Sutherland FW, Perry TE, Yu Y, et al. From stem cells to viable autologous semilunar heart valve. Circulation. 2005;111:2783–2791
  100. Cebotari S, Lichtenberg A, Tudorache I, et al. Clinical application of tissue engineered human heart valves using autologous progenitor cells. Circulation. 2006;114:I132–I137
  101. Schmidt D, Mol A, Breymann C, et al. Living autologous heart valves engineered from human prenatally harvested progenitors. Circulation. 2006;114:I125–I131
  102. Assmus B, Schachinger V, Teupe C, et al. Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI). Circulation. 2002;106:3009–3017
  103. Schachinger V, Assmus B, Britten MB, et al. Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction: final one-year results of the TOPCARE-AMI Trial. J Am Coll Cardiol. 2004;44:1690–1699
  104. Wollert KC, Meyer GP, Lotz J, et al. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet. 2004;364:141–148
  105. Meyer GP, Wollert KC, Lotz J, et al. Intracoronary bone marrow cell transfer after myocardial infarction: eighteen months' follow-up data from the randomized, controlled BOOST (BOne marrOw transfer to enhance ST-elevation infarct regeneration) trial. Circulation. 2006;113:1287–1294
  106. Pillekamp F, Reppel M, Brockmeier K, Hescheler J. Stem cells and their potential relevance to paediatric cardiology. Cardiol Young. 2006;16:117–124
  107. Agbulut O, Menot ML, Li Z, et al. Temporal patterns of bone marrow cell differentiation following transplantation in doxorubicin-induced cardiomyopathy. Cardiovasc Res. 2003;58:451–459
  108. Wang JF, Yang Y, Wang G, et al. Embryonic stem cells attenuate viral myocarditis in murine model. Cell Transplant. 2002;11:753–758
  109. Nagaya N, Kangawa K, Itoh T, et al. Transplantation of mesenchymal stem cells improves cardiac function in a rat model of dilated cardiomyopathy. Circulation. 2005;112:1128–1135
  110. Guarita-Souza LC, Carvalho KA, Woitowicz V, et al. Simultaneous autologous transplantation of cocultured mesenchymal stem cells and skeletal myoblasts improves ventricular function in a murine model of Chagas disease. Circulation. 2006;114:I120–I124
  111. Vinallonga X, Sanz N, Balaguer A, et al. Hypertrophic cardiomyopathy in mucopolysaccharidoses: regression after bone marrow transplantation. Pediatr Cardiol. 1992;13:107–109
  112. Peters C, Steward CG. Hematopoietic cell transplantation for inherited metabolic diseases: an overview of outcomes and practice guidelines. Bone Marrow Transplant. 2003;31:229–239
  113. Gatzoulis MA, Vellodi A, Redington AN. Cardiac involvement in mucopolysaccharidoses: effects of allogeneic bone marrow transplantation. Arch Dis Child. 1995;73:259–260
  114. Braunlin EA, Rose AG, Hopwood JJ, Candel RD, Krivit W. Coronary artery patency following long-term successful engraftment 14 years after bone marrow transplantation in the Hurler syndrome. Am J Cardiol. 2001;88:1075–1077
  115. Krivit W, Pierpont ME, Ayaz K, et al. Bone-marrow transplantation in the Maroteaux-Lamy syndrome (mucopolysaccharidosis type VI). Biochemical and clinical status 24 months after transplantation. N Engl J Med. 1984;311:1606–1611
  116. Klug MG, Soonpaa MH, Koh GY, Field LJ. Genetically selected cardiomyocytes from differentiating embronic stem cells form stable intracardiac grafts. J Clin Invest. 1996;98:216–224
  117. Payne TR, Oshima H, Sakai T, et al. Regeneration of dystrophin-expressing myocytes in the mdx heart by skeletal muscle stem cells. Gene Ther. 2005;12:1264–1274
  118. Davie NJ, Crossno JT, Frid MG, et al. Hypoxia-induced pulmonary artery adventitial remodeling and neovascularization: contribution of progenitor cells. Am J Physiol Lung Cell Mol Physiol. 2004;286:L668–L678
  119. Frid MG, Brunetti JA, Burke DL, et al. Hypoxia-induced pulmonary vascular remodeling requires recruitment of circulating mesenchymal precursors of a monocyte/macrophage lineage. Am J Pathol. 2006;168:659–669
  120. Baber SR, Deng W, Master RG, et al. Intratracheal mesenchymal stem cell administration attenuates monocrotaline-induced pulmonary hypertension and endothelial dysfunction. Am J Physiol Heart Circ Physiol. 2007;292:H1120–H1128
  121. Rochefort GY, Vaudin P, Bonnet N, et al. Influence of hypoxia on the domiciliation of mesenchymal stem cells after infusion into rats: possibilities of targeting pulmonary artery remodeling via cells therapies?. Respir Res. 2005;6:125
  122. Asahara T, Masuda H, Takahashi T, et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999;85:221–228
  123. Nagaya N, Kangawa K, Kanda M, et al. Hybrid cell-gene therapy for pulmonary hypertension based on phagocytosing action of endothelial progenitor cells. Circulation. 2003;108:889–895
  124. Takahashi M, Nakamura T, Toba T, Kajiwara N, Kato H, Shimizu Y. Transplantation of endothelial progenitor cells into the lung to alleviate pulmonary hypertension in dogs. Tissue Eng. 2004;10:771–779
  125. Zhao YD, Courtman DW, Deng Y, Kugathasan L, Zhang Q, Stewart DJ. Rescue of monocrotaline-induced pulmonary arterial hypertension using bone marrow-derived endothelial-like progenitor cells: efficacy of combined cell and eNOS gene therapy in established disease. Circ Res. 2005;96:442–450
  126. Wang XX, Zhang FR, Shang YP, et al. Transplantation of autologous endothelial progenitor cells may be beneficial in patients with idiopathic pulmonary arterial hypertension: a pilot randomized controlled trial. J Am Coll Cardiol. 2007;49:1566–1571

PII: S1058-9813(07)00165-8

doi: 10.1016/j.ppedcard.2007.11.005

Progress in Pediatric Cardiology
Volume 25, Issue 1 , Pages 37-49 , April 2008

Article Tools

* Image Usage & Resolution