Skip to main content
NCBI home page
Journal of Cellular and Molecular Medicine logoLink to Journal of Cellular and Molecular Medicine
. 2007 May 1;9(3):557–568. doi: 10.1111/j.1582-4934.2005.tb00488.x

The role of circulating precursors in vascular repair and lesion formation

Masataka Sata 1,2,3,✉, Daiju Fukuda 1, Kimie Tanaka 1, Yukari Kaneda 1,3, Hisako Yashiro 1, Ibuki Shirakawa 1,3
PMCID: PMC6741295  PMID: 16202205

Abstract

The accumulation of smooth muscle cells (SMCs) plays a principal role in atherogenesis, post‐angioplasty restenosis and transplantation‐associated vasculopathy. Therefore, much effort has been expended in targeting the migration and proliferation of medial smooth muscle cells to prevent occlusive vascular remodeling. Recent evidence suggests that bone marrow‐derived circulating precursors can also give rise to endothelial cells and smooth muscle cells that contribute to vascular repair, remodeling, and lesion formation under physiological and pathological conditions. This article overviews recent findings on circulating vascular progenitor cells and describes potential therapeutic strategies that target these cells to treat occlusive vascular diseases.

Keywords: smooth muscle cell, atherosclerosis, bone marrow, progenitor cell, regeneration

References

  • 1. Ross R. Atherosclerosis‐An inflammatory disease. N Eng J Med. 1999; 340: 115–26. [DOI] [PubMed] [Google Scholar]
  • 2. Nobuyoshi M, Kimura T, Nosaka H, Mioka S, Ueno K, Yokoi H, Hamasaki N, Horiuchi H, Ohishi H. Restenosis after successful percutaneous transluminal coronary angioplasty: serial angiographic follow‐up of 229 patients. J Am Coll Cardiol. 1988; 12: 616–23. [DOI] [PubMed] [Google Scholar]
  • 3. Kearney M, Pieczek A, Haley L, Losordo DW, Andres V, Schainfeld R, Rosenfield K, Isner JM. Histopathology of in‐stent restenosis in patients with peripheral artery disease. Circulation 1997; 95: 1998–2002. [DOI] [PubMed] [Google Scholar]
  • 4. Sarjeant JM, Rabinovitch M. Understanding and treating vein graft atherosclerosis. Cardiovasc Pathol. 2002; 11: 263–71. [DOI] [PubMed] [Google Scholar]
  • 5. Billingham ME. Cardiac transplant atherosclerosis. Transplant Proc. 1987; 19: 19–25. [PubMed] [Google Scholar]
  • 6. Sata M, Perlman H, Muruve DA, Silver M, Ikebe M, Libermann TA, Oettgen P, Walsh K. Fas ligand gene transfer to the vessel wall inhibits neointima formation and overrides the adenovirus‐mediated T cell response. Proc Natl Acad Sci USA. 1998; 95: 1213–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med. 2002; 8: 403–9. [DOI] [PubMed] [Google Scholar]
  • 8. Sata M. Circulating vascular progenitor cells contribute to vascular repair, remodeling, and lesion formation. Trends Cardiovasc Med. 2003; 13: 249–53. [DOI] [PubMed] [Google Scholar]
  • 9. Sata M. Molecular strategies to treat vascular diseases. Circ J. 2003; 67: 983–91. [DOI] [PubMed] [Google Scholar]
  • 10. Saiura A, Sata M, Hirata Y, Nagai R, Makuuchi M. Circulating smooth muscle progenitor cells contribute to atherosclerosis. Nat Med. 2001; 7: 382–3. [DOI] [PubMed] [Google Scholar]
  • 11. Ross R Rous‐Whipple Award Lecture. Atherosclerosis: a defense mechanism gone awry. Am J Pathol. 1993; 143: 987–1002. [PMC free article] [PubMed] [Google Scholar]
  • 12. Pollman MJ, Hall JL, Mann MJ, Zhang L, Gibbons GH. Inhibition of neointimal cell bcl‐x expression induces apoptosis and regression of vascular disease. Nature Med. 1998; 4: 222–7. [DOI] [PubMed] [Google Scholar]
  • 13. Sata M, Maejima Y, Adachi F, Fukino K, Saiura A, Sugiura S, Aoyagi T, Imai Y, Kurihara H, Kimura K, Omata M, Makuuchi M, Hirata Y, Nagai R. A mouse model of vascular injury that induces rapid onset of medial cell apoptosis followed by reproducible neointimal hyperplasia. J Mol Cell Cardiol. 2000; 32: 2097–104. [DOI] [PubMed] [Google Scholar]
  • 14. Furukawa Y, Matsumori A, Ohashi N, Shioi T, Ono K, Harada A, Matsushima K, Sasayama S. Anti‐monocyte chemoattractant protein‐1/monocyte chemotactic and activating factor antibody inhibits neointimal hyperplasia in injured rat carotid arteries. Circ Res. 1999; 84: 306–14. [DOI] [PubMed] [Google Scholar]
  • 15. Hayashi S, Watanabe N, Nakazawa K, Suzuki J, Tsushima K, Tamatani T, Sakamoto S, Isobe M. Roles of P‐selectin in inflammation, neointimal formation, and vascular remodeling in balloon‐injured rat carotid arteries. Circulation 2000; 102: 1710–7. [DOI] [PubMed] [Google Scholar]
  • 16. Zohlnhofer D, Klein CA, Richter T, Brandl R, Murr A, Nuhrenberg T, Schomig A, Baeuerle PA, Neumann FJ. Gene expression profiling of human stent‐induced neointima by cDNA array analysis of microscopic specimens retrieved by helix cutter atherectomy: Detection of FK506‐binding protein 12 upregulation. Circulation 2001; 103: 1396–402. [DOI] [PubMed] [Google Scholar]
  • 17. Tanaka K, Sata M, Hirata Y, Nagai R. Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries. Circ Res. 2003; 93: 783–90. [DOI] [PubMed] [Google Scholar]
  • 18. Hillebrands JL, Klatter FA, van Den Hurk BM, Popa ER, Nieuwenhuis P, Rozing J. Origin of neointimal endothelium and alpha‐actin‐positive smooth muscle cells in transplant arteriosclerosis. J Clin Invest. 2001; 107: 1411–22. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19. Hillebrands J, van den Hurk BM, Klatter FA, Popa ER, Nieuwenhuis P, Rozing J. Recipient origin of neointimal vascular smooth muscle cells in cardiac allografts with transplant arteriosclerosis. J Heart Lung Transplant 2000; 19: 1183–92. [DOI] [PubMed] [Google Scholar]
  • 20. Shimizu K, Sugiyama S, Aikawa M, Fukumoto Y, Rabkin E, Libby P, Mitchell RN. Host bone‐marrow cells are a source of donor intimal smooth‐muscle‐like cells in murine aortic transplant arteriopathy. Nat Med. 2001; 7: 738–41. [DOI] [PubMed] [Google Scholar]
  • 21. Hu Y, Davison F, Ludewig B, Erdel M, Mayr M, Url M, Dietrich H, Xu Q. Smooth muscle cells in transplant atherosclerotic lesions are originated from recipients, but not bone marrow progenitor cells. Circulation 2002; 106: 1834–9. [DOI] [PubMed] [Google Scholar]
  • 22. Grimm PC, Nickerson P, Jeffery J, Savani RC, Gough J, McKenna RM, Stern E, Rush DN. Neointimal and tubulointerstitial infiltration by recipient mesenchymal cells in chronic renal‐allograft rejection. N Engl J Med. 2001; 345: 93–7. [DOI] [PubMed] [Google Scholar]
  • 23. Lagaaij EL, Cramer‐Knijnenburg GF, van Kemenade FJ, van Es LA, Bruijn JA, and van Krieken JH. Endothelial cell chimerism after renal transplantation and vascular rejection. Lancet 2001; 357: 33–7. [DOI] [PubMed] [Google Scholar]
  • 24. Li S, Fan YS, Chow LH, Van Den Diepstraten C, van Der Veer E, Sims SM, Pickering JG. Innate diversity of adult human arterial smooth muscle cells: cloning of distinct subtypes from the internal thoracic artery. Circ Res. 2001; 89: 517–25. [DOI] [PubMed] [Google Scholar]
  • 25. Zalewski A, Shi Y, Johnson AG. Diverse origin of intimal cells: smooth muscle cells, myofibroblasts, fibroblasts, and beyond Circ Res. 2002; 91: 652–5. [DOI] [PubMed] [Google Scholar]
  • 26. Sata M, Sugiura S, Yoshizumi M, Ouchi Y, Hirata Y, Nagai R. Acute and chronic smooth muscle cell apoptosis after mechanical vascular injury can occur independently of the Fas‐death pathway. Arterioscler Thromb Vasc Biol. 2001; 21: 1733–7. [DOI] [PubMed] [Google Scholar]
  • 27. Sata M, Tanaka K, Ishizaka N, Hirata Y, Nagai R. Absence of p53 leads to accelerated neointimal hyperplasia after vascular injury. Arterioscler Thromb Vasc Biol. 2003; 23: 1548–52. [DOI] [PubMed] [Google Scholar]
  • 28. Caplice NM, Bunch TJ, Stalboerger PG, Wang S, Simper D, Miller DV, Russell SJ, Litzow MR, Edwards WD. Smooth muscle cells in human coronary atherosclerosis can originate from cells administered at marrow transplantation. Proc Natl Acad Sci USA. 2003; 100: 4754–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29. Plump AS, Smith JD, Hayek T, Aalto‐Setala K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL. Severe hypercholesterolemia and atherosclerosis in apolipoprotein Edeficient mice created by homologous recombination in ES cells. Cell 1992; 71: 343–53. [DOI] [PubMed] [Google Scholar]
  • 30. Ferrara N. Vascular endothelial growth factor and the regulation of angiogenesis. Recent Prog Horm Res. 2000; 55: 15–35. [PubMed] [Google Scholar]
  • 31. Folkman J. Seminars in medicine of the Beth Israel Hospital, Boston. Clinical applications of research on angiogenesis. N Engl J Med. 1995; 333: 1757–63. [DOI] [PubMed] [Google Scholar]
  • 32. Moulton KS, Vakili K, Zurakowski D, Soliman M, Butterfield C, Sylvin E, Lo KM, Gillies S, Javaherian K, Folkman J. Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis. Proc Natl Acad Sci USA. 2003; 100: 4736–41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33. Moulton KS, Heller E, Konerding MA, Flynn E, Palinski W, Folkman J. Angiogenesis inhibitors endostatin or TNP‐470 reduce intimal neovascularization and plaque growth in apolipoprotein E‐deficient mice. Circulation 1999; 99: 1726–32. [DOI] [PubMed] [Google Scholar]
  • 34. Rundhaug JE. Matrix metalloproteinases and angiogenesis. J Cell Mol Med. 2005; 9: 267–85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35. Staton CA, Lewis CE. Angiogenesis inhibitors found within the haemostasis pathway. J Cell Mol Med. 2005; 9: 286–302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997; 275: 964–7. [DOI] [PubMed] [Google Scholar]
  • 37. Peichev M, Naiyer AJ, Pereira D, Zhu Z, Lane WJ, Williams M, Oz MC, Hicklin DJ, Witte L, Moore MA. Rafii S. Expression of VEGFR‐2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 2000; 95: 952–8. [PubMed] [Google Scholar]
  • 38. Iwami Y, Masuda H, Asahara T. Endothelial progenitor cells: past, state of the art, and future. J Cell Mol Med. 2004; 8: 488–97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39. Schatteman GC, Awad O. In vivo and in vitro properties of CD34+ and CD14+ endothelial cell precursors. Adv Exp Med Biol 2003; 522: 9–16. [DOI] [PubMed] [Google Scholar]
  • 40. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999; 85: 221–8. [DOI] [PubMed] [Google Scholar]
  • 41. Hristov M, Weber C. Endothelial progenitor cells: characterization, pathophysiology, and possible clinical relevance. J Cell Mol Med. 2004; 8: 498–508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42. Jansen J, Hanks S, Thompson JM, Dugan MJ, Akard LP. Transplantation of hematopoietic stem cells from the peripheral blood. J Cell Mol Med. 2005; 9: 37–50. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43. Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, Neutzel S, Sharkis SJ. Multiorgan, multi‐lineage engraftment by a single bone marrow‐derived stem cell. Cell 2001; 105: 369–77. [DOI] [PubMed] [Google Scholar]
  • 44. Lagasse E, Connors H, Al‐Dhalimy M, Reitsma M, Dohse M, Osborne L, Wang X, Finegold M, Weissman IL, Grompe M. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo . Nat Med. 2000; 6: 1229–34. [DOI] [PubMed] [Google Scholar]
  • 45. Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson, SM , Li B, Pickel J, McKay R, Nadal‐Ginard B, Bodine, DM , Leri A, Anversa P. Bone marrow cells regenerate infarcted myocardium. Nature 2001; 410: 701–5. [DOI] [PubMed] [Google Scholar]
  • 46. Wagers AJ, Sherwood RI, Christensen JL, Weissman IL. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 2002; 297: 2256–9. [DOI] [PubMed] [Google Scholar]
  • 47. Balsam LB, Wagers AJ, Christensen JL, Kofidis T, Weissman IL, Robbins RC. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature, 2004. [DOI] [PubMed]
  • 48. Sahara M, Sata M, Matsuzaki Y, Tanaka K, Morita T, Hirata Y, Okano H, Nagai R. Comparison of various bone marrow fractions in the ability to participate in vascular remodeling after mechanical injury. Stem Cells 2005; 23: 874–8. [DOI] [PubMed] [Google Scholar]
  • 49. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz‐Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002; 418: 41–9. [DOI] [PubMed] [Google Scholar]
  • 50. Sata M, Nagai R. Inflammation, angiogenesis, and endothelial progenitor cells: how do endothelial progenitor cells find their place J Mol Cell Cardiol. 2004; 36: 459–63. [DOI] [PubMed] [Google Scholar]
  • 51. Gehling UM, Ergun S, Schumacher U, Wagener C, Pantel K, Otte M, Schuch G, Schafhausen P, Mende T, Kilic N, Kluge K, Schafer B, Hossfeld DK, Fiedler W. In vitro differentiation of endothelial cells from AC133‐positive progenitor cells. Blood 2000; 95: 3106–112. [PubMed] [Google Scholar]
  • 52. Kalka C, Masuda H, Takahashi T, Gordon R, Tepper O, Gravereaux E, Pieczek A, Iwaguro H, Hayashi SI, Isner JM, Asahara T. Vascular endothelial growth factor(165) gene transfer augments circulating endothelial progenitor cells in human subjects. Circ Res. 2000; 86: 1198–202. [DOI] [PubMed] [Google Scholar]
  • 53. Simper D, Stalboerger PG, Panetta CJ, Wang S, Caplice NM. Smooth muscle progenitor cells in human blood. Circulation 2002; 106: 1199–204. [DOI] [PubMed] [Google Scholar]
  • 54. Vasa M, Fichtlscherer S, Adler K, Aicher A, Martin H, Zeiher AM, Dimmeler S. Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease. Circulation 2001; 103: 2885–90. [DOI] [PubMed] [Google Scholar]
  • 55. Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM, Dimmeler S. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res. 2001; 89: E1–7. [DOI] [PubMed] [Google Scholar]
  • 56. Shintani S, Murohara T, Ikeda H, Ueno T, Honma T, Katoh A, Sasaki K, Shimada T, Oike Y, Imaizumi T. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 2001; 103: 2776–9. [DOI] [PubMed] [Google Scholar]
  • 57. Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med. 2003; 348: 593–600. [DOI] [PubMed] [Google Scholar]
  • 58. Gulati R, Jevremovic D, Peterson TE, Witt TA, Kleppe LS, Mueske CS, Lerman A, Vile RG, Simari RD. Autologous culture‐modified mononuclear cells confer vascular protection after arterial injury. Circulation 2003; 108: 1520–6. [DOI] [PubMed] [Google Scholar]
  • 59. Urbich C, Heeschen C, Aicher A, Dernbach E, Zeiher AM, Dimmeler S. Relevance of monocytic features for neovascularization capacity of circulating endothelial progenitor cells. Circulation 2003; 108: 2511–6. [DOI] [PubMed] [Google Scholar]
  • 60. Gill M, Dias S, Hattori K, Rivera ML, Hicklin D, Witte L, Girardi L, Yurt R, Himel H, Rafii S. Vascular trauma induces rapid but transient mobilization of VEGFR2(+) AC133(+) endothelial precursor cells. Circ Res. 2001; 88: 167–74. [DOI] [PubMed] [Google Scholar]
  • 61. Rauscher FM, Goldschmidt‐Clermont PJ, Davis BH, Wang T, Gregg D, Ramaswami P, Pippen AM, Annex BH, Dong C, Taylor DA. Aging, progenitor cell exhaustion, and atherosclerosis. Circulation 2003; 108: 457–63. [DOI] [PubMed] [Google Scholar]
  • 62. 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: 337–46. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63. Luttun A, Tjwa M, Moons L, Wu Y, Angelillo‐Scherrer A, Liao F, Nagy JA, Hooper A, Priller J, De Klerck B, Compernolle V, Daci E, Bohlen P, Dewerchin M, Herbert JM, Fava R, Matthys P, Carmeliet G, Collen D, Dvorak HF, Hicklin DJ, Carmeliet P. Revascularization of ischemic tissues by P1GF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti‐F1t1. Nat Med. 2002; 8: 831–40. [DOI] [PubMed] [Google Scholar]
  • 64. Amano K, Okigaki M, Adachi Y, Fujiyama S, Mori Y, Kosaki A, Iwasaka T, Matsubara H. Mechanism for IL‐1 beta‐mediated neovascularization unmasked by IL‐1 beta knock‐out mice. J Mol Cell Cardiol. 2004; 36: 469–80. [DOI] [PubMed] [Google Scholar]
  • 65. Moldovan NI. Functional adaptation: the key to plasticity of cardiovascular “stem” cells Stem Cells Dev. 2005; 14: 111–21. [DOI] [PubMed] [Google Scholar]
  • 66. Paunescu V, Suciu E, Tatu C, Plesa A, Herman D, Siska IR, Suciu C, Crisnic D, Nistor D, Tanasie G, Bunu C, Raica M. Endothelial cells from hematopoietic stem cells are functionally different from those of human umbilical vein. J Cell Mol Med. 2003; 7: 455–60. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 67. Liu C, Nath KA, Katusic ZS, Caplice NM. Smooth muscle progenitor cells in vascular disease. Trends Cardiovasc Med. 2004; 14: 288–93. [DOI] [PubMed] [Google Scholar]
  • 68. Deb A, Skelding KA, Wang S, Reeder M, Simper D, Caplice NM. Integrin profile and in vivo homing of human smooth muscle progenitor cells. Circulation 2004; 110: 2673–7. [DOI] [PubMed] [Google Scholar]
  • 69. Hu Y, Zhang Z, Torsney E, Afzal AR, Davison F, Metzler B, Xu Q. Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE‐deficient mice. J Clin Invest. 2004; 113: 1258–65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 70. Korbling M, Katz RL, Khanna A, Ruifrok AC, Rondon G, Albitar M, Champlin RE, Estrov Z. Hepatocytes and epithelial cells of donor origin in recipients of peripheral blood stem cells. N Engl J Med 2002; 346: 738–46. [DOI] [PubMed] [Google Scholar]
  • 71. Korbling M, Estrov Z. Adult stem cells for tissue repair ‐ a new therapeutic concept N Engl J Med. 2003; 349: 570–82. [DOI] [PubMed] [Google Scholar]
  • 72. LaBarge MA, Blau HM. Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell 2002; 111: 589–601. [DOI] [PubMed] [Google Scholar]
  • 73. Terada N, Hamazaki T, Oka M, Hoki M, Mastalerz DM, Nakano Y, Meyer EM, Morel L, Petersen BE, Scott EW. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 2002; 416: 542–5. [DOI] [PubMed] [Google Scholar]
  • 74. Ying QL, Nichols J, Evans EP, Smith AG. Changing potency by spontaneous fusion. Nature 2002; 416: 545–8. [DOI] [PubMed] [Google Scholar]
  • 75. Wang X, Willenbring H, Akkari Y, Torimaru Y, Foster M, Al‐Dhalimy M, Lagasse E, Finegold M, Olson S, Grompe M. Cell fusion is the principal source of bone‐marrow‐derived hepatocytes. Nature 2003; 422: 897–901. [DOI] [PubMed] [Google Scholar]
  • 76. Vassilopoulos G, Wang PR, Russell DW. Transplanted bone marrow regenerates liver by cell fusion. Nature 2003; 422: 901–4. [DOI] [PubMed] [Google Scholar]
  • 77. Campbell JH, Tachas G, Black MJ, Cockerill G, Campbell GR. Molecular biology of vascular hypertrophy. Basic Res Cardiol. 1991; 86: 3–11. [PubMed] [Google Scholar]
  • 78. Saiura A, Sata M, Washida M, Sugawara Y, Hirata Y, Nagai R, Makuuchi M. Little evidence for cell fusion between recipient and donor‐derived cells. J Surg Res. 2003; 113: 222–7. [DOI] [PubMed] [Google Scholar]
  • 79. Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y, Pocius J, Michael LH, Behringer RR, Garry DJ, Entman ML, Schneider MD. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 2003; 100: 12313–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 80. Miller AM, McPhaden AR, Wadsworth RM, Wainwright CL. Inhibition by leukocyte depletion of neointima formation after balloon angioplasty in a rabbit model of restenosis. Cardiovasc Res. 2001; 49: 838–50. [DOI] [PubMed] [Google Scholar]
  • 81. Jacobs AK. Coronary stents‐have they fulfilled their promise N Engl J Med. 1999; 341: 2005–6. [DOI] [PubMed] [Google Scholar]
  • 82. Moses JW, Leon MB, Popma JJ, Fitzgerald PJ, Holmes DR, O'Shaughnessy C, Caputo RP, Kereiakes DJ, Williams DO, Teirstein PS, Jaeger JL, Kuntz RE. Sirolimus‐eluting stents versus standard stents in patients with stenosis in a native coronary artery. N Engl J Med. 2003; 349: 1315–23. [DOI] [PubMed] [Google Scholar]
  • 83. Marks AR. Sirolimus for the prevention of in‐stent restenosis in a coronary artery. N Engl J Med. 2003; 349: 1307–9. [DOI] [PubMed] [Google Scholar]
  • 84. Fukuda D, Sata M, Tanaka K, Nagai R. Potent inhibitory effect of sirolimus on circulating vascular progenitor cells. Circulation 2005; 111: 926–31. [DOI] [PubMed] [Google Scholar]
  • 85. McFadden EP, Stabile E, Regar E, Cheneau E, Ong AT, Kinnaird T, Suddath WO, Weissman NJ, Torguson R, Kent KM, Pichard AD, Satler LF, Waksman R, Serruys PW. Late thrombosis in drug‐eluting coronary stents after discontinuation of antiplatelet therapy. Lancet 2004; 364: 1519–21. [DOI] [PubMed] [Google Scholar]
  • 86. Walsh K, Sata M. Is extravasation a Fas‐regulated process Mol. Med. Today 1999; 7: 61–7. [DOI] [PubMed] [Google Scholar]
  • 87. Walsh K, Sata M. Negative regulation of inflammation by Fas ligand expression on the vascular endothelium. Trends Cardiovasc Med. 1999; 9: 34–41. [DOI] [PubMed] [Google Scholar]
  • 88. Nagata S, Golstein P. The Fas death factor. Science 1995; 267: 1449–56. [DOI] [PubMed] [Google Scholar]
  • 89. Nagata S. Apoptosis by death factor. Cell 1997; 88: 355–65. [DOI] [PubMed] [Google Scholar]
  • 90. Sata M, Luo Z, Walsh K. Fas ligand overexpression on allograft endothelium inhibits inflammatory cell infiltration and transplant‐associated intimal hyperplasia. J Immunol. 2001; 66: 6964–71. [DOI] [PubMed] [Google Scholar]
  • 91. Luo Z, Sata M, Nguyen T, Kaplan JM, Akita GY, Walsh K. Adenovirus‐mediated delivery of Fas ligand inhibits intimal hyperplasia after balloon injury in immunologically primed animals. Circulation 1999; 99: 1776–9. [DOI] [PubMed] [Google Scholar]
  • 92. Sata M, Walsh K. TNFα Regulation of Fas ligand expression on the vascular endothelium modulates leukocyte extravasation. Nat Med. 1998; 4: 415–20. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 93. Richardson BC, Lalwani ND, Johnson KJ, Marks RM. Fas ligation triggers apoptosis in macrophages but not endothelial cells. Eur J Immunol. 1994; 24: 2640–5. [DOI] [PubMed] [Google Scholar]
  • 94. Sata M, Suhara T, Walsh K. Vascular endothelial cells and smooth muscle cells differ in expression of Fas and Fas ligand and in sensitivity to Fas Ligand induced cell death: Implications for vascular disease and therapy. Arterioscler Thromb Vasc Biol. 2000; 20: 309–16. [DOI] [PubMed] [Google Scholar]
  • 95. Yang J, Sato K, Aprahamian T, Brown NJ, Hutcheson J, Bialik A, Perlman H, Walsh K. Endothelial overexpression of Fas ligand decreases atherosclerosis in apolipoprotein E‐deficient mice. Arterioscler Thromb Vasc Biol. 2004; 24: 1466–73. [DOI] [PubMed] [Google Scholar]
  • 96. Anglani F, Forino M, Del Prete D, Tosetto E, Torregrossa R, D'Angelo A. In search of adult renal stem cells. J Cell Mol Med. 2004; 8: 474–87. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 97. Smits AM, van Vliet P, Hassink RJ, Goumans MJ, Doevendans PA. The role of stem cells in cardiac regeneration. J Cell Mol Med. 2005; 9: 25–36. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 98. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105–11. [DOI] [PubMed] [Google Scholar]
  • 99. Kang HJ, Kim HS, Zhang SY, Park KW, Cho HJ, Koo BK, Kim YJ, Soo Lee D, Sohn DW, Han KS, Oh BH, Lee MM, Park YB. Effects of intracoronary infusion of peripheral blood stem‐cells mobilised with granulocytecolony stimulating factor on left ventricular systolic function and restenosis after coronary stenting in myocardial infarction: the MAGIC cell randomised clinical trial. Lancet 2004; 363: 751–6. [DOI] [PubMed] [Google Scholar]
  • 100. Silvestre JS, Gojova A, Brun V, Potteaux S, Esposito B, Duriez M, Clergue M, Le Ricousse‐Roussanne S, Barateau V, Merval R, Groux H, Tobelem G, Levy B, Tedgui A, Mallat Z. Transplantation of bone marrowderived mononuclear cells in ischemic apolipoprotein E‐knockout mice accelerates atherosclerosis without altering plaque composition. Circulation 2003; 108: 2839–42. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Cellular and Molecular Medicine are provided here courtesy of Blackwell Publishing

RESOURCES