International Journal of Gerontology
Volume 1, Issue 1 , Pages 10-21 , March 2007

Therapeutic Application of Bone Marrow-derived Progenitor Cells for Vascular Diseases: Magicbullets Having the Good Without the Bad?

  • Kimie Tanaka

      Affiliations

    • Department of Cardiovascular Medicine, University of Tokyo Graduate School of Medicine, Tokyo, Japan
    • ,
  • Masataka Sata

      Affiliations

    • Department of Cardiovascular Medicine, University of Tokyo Graduate School of Medicine, Tokyo, Japan
    • Department of Advanced Clinical Science and Therapeutics, University of Tokyo Graduate School of Medicine, Tokyo, Japan
    • Corresponding Author InformationCorrespondence to: Dr Masataka Sata, Department of Cardiovascular Medicine, University of Tokyo Graduate School of Medicine, 7-3-1 Hongo Bunkyo-ku, Tokyo 113-8655, Japan

,Accepted 28 November 2006.

References 

  1. Asahara T , Murohara T , Sullivan A , Silver M , van der Zee R , Li T , et al.   Isolation of putative progenitor endothelial cells for angiogenesis . Science . 1997;275:964–967
  2. Khakoo AY , Finkel T . Endothelial progenitor cells . Annu Rev Med . 2005;56:79–101
  3. Sata M , Saiura A , Kunisato A , Tojo A , Okada S , Tokuhisa T , et al.   Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis . Nat Med . 2002;8:403–409
  4. Sata M . Circulating vascular progenitor cells contribute to vascular repair, remodeling, and lesion formation . Trends Cardiovasc Med . 2003;13:249–253
  5. Saiura A , Sata M , Hirata Y , Nagai R , Makuuchi M . Circulating smooth muscle progenitor cells contribute to atherosclerosis . Nat Med . 2001;7:382–383
  6. Sarjeant JM , Rabinovitch M . Understanding and treating vein graft atherosclerosis . Cardiovasc Pathol . 2002;11:263–271
  7. Billingham ME . Cardiac transplant atherosclerosis . Transplant Proc . 1987;19:19–25
  8. Ross R . Atherosclerosis: a defense mechanism gone awry . Am J Pathol . 1993;143:985–1002
  9. Sata M , Maejima Y , Adachi F , Fukino K , Saiura A , Sugiura S , et al.   A mouse model of vascular injury that induces rapid onset of medial cell apoptosis followed by reproducible neointimal hyperplasia . J Mol Cell Cardiol . 2000;32:2097–2104
  10. Furukawa Y , Matsumori A , Ohashi N , Shioi T , Ono K , Harada A , et al.   Anti-monocyte chemoattractant protein-1/monocyte chemotactic and activating factor antibody inhibits neointimal hyperplasia in injured rat carotid arteries . Circ Res . 1999;84:306–314
  11. Hayashi S , Watanabe N , Nakazawa K , Suzuki J , Tsushima K , Tamatani T , et al.   Roles of P-selectin in inflammation, neointimal formation, and vascular remodeling in balloon-injured rat carotid arteries . Circulation . 2000;102:1710–1717
  12. Zohlnhofer D , Klein CA , Richter T , Brandl R , Murr A , Nuhrenberg T , et al.   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;103:1396–1402
  13. Tanaka K , Sata M , Hirata Y , Nagai R . Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries . Circ Res . 2003;93:783–790
  14. 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;107:1411–1422
  15. Shimizu K , Sugiyama S , Aikawa M , Fukumoto Y , Rabkin E , Libby P , et al.   Host bone-marrow cells are a source of donor intimal smooth-muscle-like cells in murine aortic transplant arteriopathy . Nat Med . 2001;7:738–741
  16. Hu Y , Davison F , Ludewig B , Erdel M , Mayr M , Url M , et al.   Smooth muscle cells in transplant atherosclerotic lesions are originated from recipients, but not bone marrow progenitor cells . Circulation . 2002;106:1834–1839
  17. Grimm PC , Nickerson P , Jeffery J , Savani RC , Gough J , McKenna RM , et al.   Neointimal and tubulointerstitial infiltration by recipient mesenchymal cells in chronic renal-allograft rejection . N Engl J Med . 2001;345:93–97
  18. Lagaaij EL , Cramer-Knijnenburg GF , van Kemenade FJ , van Es LA , Bruijn JA , van Krieken JH . Endothelial cell chimerism after renal transplantation and vascular rejection . Lancet . 2001;357:33–37
  19. Caplice NM , Bunch TJ , Stalboerger PG , Wang S , Simper D , Miller DV , et al.   Smooth muscle cells in human coronary atherosclerosis can originate from cells administered at marrow transplantation . Proc Natl Acad Sci USA . 2003;100:4754–4759
  20. Plump AS , Smith JD , Hayek T , Aalto-Setela K , Walsh A , Verstuyft JG , et al.   Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells . Cell . 1992;71:343–353
  21. Folkman J . Clinical applications of research on angiogenesis . N Engl J Med . 1995;333:1757–1763
  22. Ferrara N . Vascular endothelial growth factor and the regulation of angiogenesis . Recent Prog Horm Res . 2000;55:15–35
  23. Moulton KS , Vakili K , Zurakowski D , Soliman M , Butterfield C , Sylvin E , et al.   Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis . Proc Natl Acad Sci USA . 2003;100:4736–4741
  24. 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;99:1726–1732
  25. 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
  26. Asahara T , Masuda H , Takahashi T , Kalka C , Pastore C , Silver M , et al.   Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization . Circ Res . 1999;85:221–228
  27. Kaplan RN , Riba RD , Zacharoulis S , Bramley AH , Vincent L , Costa C , et al.   VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche . Nature . 2005;438:820–827
  28. Otani A , Kinder K , Ewalt K , Otero FJ , Schimmel P , Friedlander M . Bone marrow-derived stem cells target retinal astrocytes and can promote or inhibit retinal angiogenesis . Nat Med . 2002;8:1004–1010
  29. Hu Y , Davison F , Zhang Z , Xu Q . Endothelial replacement and angiogenesis in arteriosclerotic lesions of allografts are contributed by circulating progenitor cells . Circulation . 2003;108:3122–3127
  30. 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
  31. Krause DS , Theise ND , Collector MI , Henegariu O , Hwang S , Gardner R , et al.   Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell . Cell . 2001;105:369–377
  32. Orlic D , Kajstura J , Chimenti S , Jakoniuk I , Anderson SM , Li B , et al.   Bone marrow cells regenerate infarcted myocardium . Nature . 2001;410:701–705
  33. Lagasse E , Connors H , Al-Dhalimy M , Reitsma M , Dohse M , Osborne L , et al.   Purified hematopoietic stem cells can differentiate into hepatocytes in vivo . Nat Med . 2000;6:1229–1234
  34. Sata M , Maejima Y , Adachi F , Fukino K , Saiura A , Sugiura S , et al.   A mouse model of vascular injury that induces rapid onset of medial cell apoptosis followed by reproducible neointimal hyperplasia . J Mol Cell Cardiol . 2000;32:2097–2104
  35. Wagers AJ , Sherwood RI , Christensen JL , Weissman IL . Little evidence for developmental plasticity of adult hematopoietic stem cells . Science . 2002;297:2256–2259
  36. 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
  37. Sahara M , Sata M , Matsuzaki Y , Tanaka K , Morita T , Hirata Y , et al.   Comparison of various bone marrow fractions in the ability to participate in vascular remodeling after mechanical injury . Stem Cells . 2005;23:874–878
  38. Jiang Y , Jahagirdar BN , Reinhardt RL , Schwartz RE , Keene CD , Ortiz-Gonzalez XR , et al.   Pluripotency of mesenchymal stem cells derived from adult marrow . Nature . 2002;418:41–49
  39. Sata M , Nagai R . Inflammation, angiogenesis, and endothelial progenitor cells: how do endothelial progenitor cells find their place? . J Mol Cell Cardiol . 2004;36:459–463
  40. Hill JM , Zalos G , Halcox JP , Schenke WH , Waclawiw MA , Quyyumi AA , et al.   Circulating endothelial progenitor cells, vascular function, and cardiovascular risk . N Engl J Med . 2003;348:593–600
  41. 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;108:2511–2516
  42. Shintani S , Murohara T , Ikeda H , Ueno T , Honma T , Katoh A , et al.   Mobilization of endothelial progenitor cells in patients with acute myocardial infarction . Circulation . 2001;103:2776–2779
  43. Rauscher FM , Goldschmidt-Clermont PJ , Davis BH , Wang T , Gregg D , Ramaswami P , et al.   Aging, progenitor cell exhaustion, and atherosclerosis . Circulation . 2003;108:457–463
  44. Gill M , Dias S , Hattori K , Rivera ML , Hicklin D , Witte L , et al.   Vascular trauma induces rapid but transient mobilization of VEGFR2(+)AC133(+) endothelial precursor cells . Circ Res . 2001;88:167–174
  45. 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
  46. Amano K , Okigaki M , Adachi Y , Fujiyama S , Mori Y , Kosaki A , et al.   Mechanism for IL-1 beta-mediated neovascularization unmasked by IL-1 beta knock-out mice . J Mol Cell Cardiol . 2004;36:469–480
  47. Friedrich EB , Walenta K , Scharlau J , Nickenig G , Werner N . CD34-/CD133+/VEGFR-2+ endothelial progenitor cell subpopulation with potent vasoregenerative capacities . Circ Res . 2006;98:e20–e25
  48. Luttun A , Tjwa M , Moons L , Wu Y , Angelillo-Scherrer A , Liao F , et al.   Revascularization of ischemic tissues by PlGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1 . Nat Med . 2002;8:831–840
  49. Rafii S , Lyden D . Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration . Nat Med . 2003;9:702–712
  50. Paunescu V , Suciu E , Tatu C , Plesa A , Herman D , Siska IR , et al.   Endothelial cells from hematopoietic stem cells are functionally different from those of human umbilical vein . J Cell Mol Med . 2003;7:455–460
  51. Liu C , Nath KA , Katusic ZS , Caplice NM . Smooth muscle progenitor cells in vascular disease . Trends Cardiovasc Med . 2004;14:288–293
  52. 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;110:2673–2677
  53. Zalewski A , Shi Y , Johnson AG . Diverse origin of intimal cells: smooth muscle cells, myofibroblasts, fibroblasts, and beyond? . Circ Res . 2002;91:652–655
  54. Tanaka K , Sata M , Hirata Y , Nagai R . Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries . Circ Res . 2003;93:783–790
  55. Hu Y , Zhang Z , Torsney E , Afzal AR , Davison F , Metzler B , et al.   Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoEdeficient mice . J Clin Invest . 2004;113:1258–1265
  56. Korbling M , Katz RL , Khanna A , Ruifrok AC , Rondon G , Albitar M , et al.   Hepatocytes and epithelial cells of donor origin in recipients of peripheral-blood stem cells . N Engl J Med . 2002;346:738–746
  57. Korbling M , Estrov Z . Adult stem cells for tissue repair— a new therapeutic concept? . N Engl J Med . 2003;349:570–582
  58. 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
  59. Terada N , Hamazaki T , Oka M , Hoki M , Mastalerz DM , Nakano Y , et al.   Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion . Nature . 2002;416:542–545
  60. Ying QL , Nichols J , Evans EP , Smith AG . Changing potency by spontaneous fusion . Nature . 2002;416:545–548
  61. Wang X , Willenbring H , Akkari Y , Torimaru Y , Foster M , Al-Dhalimy M , et al.   Cell fusion is the principal source of bone-marrow-derived hepatocytes . Nature . 2003;422:897–901
  62. Vassilopoulos G , Wang PR , Russell DW . Transplanted bone marrow regenerates liver by cell fusion . Nature . 2003;422:901–904
  63. Campbell JH , Tachas G , Black MJ , Cockerill G , Campbell GR . Molecular biology of vascular hypertrophy . Basic Res Cardiol . 1991;86:3–11
  64. Saiura A , Sata M , Washida M , Sugawara Y , Hirata Y , Nagai R , et al.   Little evidence for cell fusion between recipient and donor-derived cells . J Surg Res . 2003;113:222–227
  65. Oh H , Bradfute SB , Gallardo TD , Nakamura T , Gaussin V , Mishina Y , et al.   Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction . Proc Natl Acad Sci USA . 2003;100:12313–12318
  66. 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;49:838–850
  67. Jacobs AK . Coronary stents—have they fulfilled their promise? . N Engl J Med . 1999;341:2005–2006
  68. Moses JW , Leon MB , Popma JJ , Fitzgerald PJ , Holmes DR , O'Shaughnessy C , et al.   Sirolimus-eluting stents versus standard stents in patients with stenosis in a native coronary artery . N Engl J Med . 2003;349:1315–1323
  69. Daemen J , Ong AT , Stefanini GG , Tsuchida K , Spindler H , Sianos G , et al.   Three-year clinical follow-up of the unrestricted use of sirolimus-eluting stents as part of the Rapamycin-Eluting Stent Evaluated at Rotterdam Cardiology Hospital (RESEARCH) Registry . Am J Cardiol . 2006;98:895–901
  70. Marks AR . Sirolimus for the prevention of in-stent restenosis in a coronary artery . N Engl J Med . 2003;349:1307–1309
  71. Fukuda D , Sata M , Tanaka K , Nagai R . Potent inhibitory effect of sirolimus on circulating vascular progenitor cells . Circulation . 2005;111:926–931
  72. McFadden EP , Stabile E , Regar E , Cheneau E , Ong AT , Kinnaird T , et al.   Late thrombosis in drug-eluting coronary stents after discontinuation of antiplatelet therapy . Lancet . 2004;364:1519–1521
  73. Walsh K , Sata M . Is extravasation a Fas-regulated process? . Mol Med Today . 1999;7:61–67
  74. Walsh K , Sata M . Negative regulation of inflammation by Fas ligand expression on the vascular endothelium . Trends Cardiovasc Med . 1999;9:34–41
  75. Nagata S , Golstein P . The Fas death factor . Science . 1995;267:1449–1456
  76. Nagata S . Apoptosis by death factor . Cell . 1997;88:355–365
  77. Sata M , Perlman H , Muruve DA , Silver M , Ikebe M , Libermann TA , et al.   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;95:1213–1217
  78. Sata M , Luo Z , Walsh K . Fas ligand overexpression on allograft endothelium inhibits inflammatory cell infiltration and transplant-associated intimal hyperplasia . J Immunol . 2001;66:6964–6971
  79. 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;99:1776–1779
  80. Sata M , Walsh K . TNFα regulation of Fas ligand expression on the vascular endothelium modulates leukocyte extravasation . Nat Med . 1998;4:415–420
  81. Richardson BC , Lalwani ND , Johnson KJ , Marks RM . Fas ligation triggers apoptosis in macrophages but not endothelial cells . Eur J Immunol . 1994;24:2640–2645
  82. 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;20:309–316
  83. 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;8:474–487
  84. 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
  85. Reya T , Morrison SJ , Clarke MF , Weissman IL . Stem cells, cancer, and cancer stem cells . Nature . 2001;414:105–111
  86. Sata M , Saiura A , Kunisato A , Tojo A , Okada S , Tokuhisa T , et al.   Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis . Nat Med . 2002;8:403–409
  87. Saiura A , Sata M , Hirata Y , Nagai R , Makuuchi M . Circulating smooth muscle progenitor cells contribute to atherosclerosis . Nat Med . 2001;7:382–383
  88. Tateishi-Yuyama E , Matsubara H , Murohara T , Ikeda U , Shintani S , Masaki H , et al.   Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomized controlled trial . Lancet . 2002;360:427–435
  89. Assmus B , Schachinger V , Teupe C , Britten M , Lehmann R , Dobert N , et al.   Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI) . Circulation . 2002;106:3009–3017
  90. Strauer BE , Brehm M , Zeus T , Kostering M , Hernandez A , Sorg RV , et al.   Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans . Circulation . 2002;106:1913–1918
  91. Meyer GP , Wollert KC , Lotz J , Steffens J , Lippolt P , Fichtner S , et al.   Intracoronary bone marrow cell transfer after myocardial infarction: eighteen months' followup data from the randomized, controlled BOOST (BOne marrOw transfer to enhance ST-elevation infarct regeneration) trial . Circulation . 2006;113:1287–1294
  92. Ziegelhoeffer T , Fernandez B , Kostin S , Heil M , Voswinckel R , Helisch A , et al.   Bone marrow-derived cells do not incorporate into the adult growing vasculature . Circ Res . 2004;94:230–238
  93. Urbich C , Dimmeler S . Endothelial progenitor cells: characterization and role in vascular biology . Circ Res . 2004;95:343–353
  94. O'Neill TJT , Wamhoff BR , Owens GK , Skalak TC . Mobilization of bone marrow-derived cells enhances the angiogenic response to hypoxia without transdifferentiation into endothelial cells . Circ Res . 2005;97:1027–1035
  95. Kinnaird T , Stabile E , Burnett MS , Epstein SE . Bonemarrow-derived cells for enhancing collateral development: mechanisms, animal data, and initial clinical experiences . Circ Res . 2004;95:354–363
  96. Kang HJ , Kim HS , Zhang SY , Park KW , Cho HJ , Koo BK , 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 randomized clinical trial . Lancet . 2004;363:751–756
  97. Silvestre JS , Gojova A , Brun V , Potteaux S , Esposito B , Duriez M , et al.   Transplantation of bone marrowderived mononuclear cells in ischemic apolipoprotein E-knockout mice accelerates atherosclerosis without altering plaque composition . Circulation . 2003;108:2839–2842
  98. Assmus B , Honold J , Schachinger V , Britten MB , Fischer-Rasokat U , Lehmann R , et al.   Transcoronary transplantation of progenitor cells after myocardial infarction . N Engl J Med . 2006;355:1222–1232
  99. Schachinger V , Erbs S , Elsasser A , Haberbosch W , Hambrecht R , Holschermann H , et al.   Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction . N Engl J Med . 2006;355:1210–1221
  100. Lunde K , Solheim S , Aakhus S , Arnesen H , Abdelnoor M , Egeland T , et al.   Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction . N Engl J Med . 2006;355:1199–1209

PII: S1873-9598(08)70019-X

doi: 10.1016/S1873-9598(08)70019-X

International Journal of Gerontology
Volume 1, Issue 1 , Pages 10-21 , March 2007

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