Biology of Blood and Marrow Transplantation
Volume 12, Issue 5 , Pages 585-593 , May 2006

Direct Comparison of Umbilical Cord Blood versus Bone Marrow–Derived Endothelial Precursor Cells in Mediating Neovascularization in Response to Vascular Ischemia

  • Marcie R. Finney

      Affiliations

    • Department of Medicine, Case Western Reserve University, School of Medicine, Case Comprehensive Cancer Center, Cleveland, Ohio
    • ,
  • Nicholas J. Greco

      Affiliations

    • Department of Medicine, Case Western Reserve University, School of Medicine, Case Comprehensive Cancer Center, Cleveland, Ohio
    • ,
  • Stephen E. Haynesworth

      Affiliations

    • Department of Biology, Case Western Reserve University, School of Medicine, Case Comprehensive Cancer Center, Cleveland, Ohio
    • ,
  • Joseph M. Martin

      Affiliations

    • Department of Medicine, Case Western Reserve University, School of Medicine, Case Comprehensive Cancer Center, Cleveland, Ohio
    • ,
  • David P. Hedrick

      Affiliations

    • Department of Medicine, Case Western Reserve University, School of Medicine, Case Comprehensive Cancer Center, Cleveland, Ohio
    • ,
  • Jimmy Z. Swan

      Affiliations

    • Department of Medicine, Case Western Reserve University, School of Medicine, Case Comprehensive Cancer Center, Cleveland, Ohio
    • ,
  • Daniel G. Winter

      Affiliations

    • Department of Medicine, Case Western Reserve University, School of Medicine, Case Comprehensive Cancer Center, Cleveland, Ohio
    • ,
  • Suzanne Kadereit

      Affiliations

    • Institute of Bioengineering and Nanotechnology, Singapore
    • ,
  • Matthew E. Joseph

      Affiliations

    • Department of Medicine, Case Western Reserve University, School of Medicine, Case Comprehensive Cancer Center, Cleveland, Ohio
    • ,
  • Pingfu Fu

      Affiliations

    • Department of Epidemiology and Biostatistics, Case Western Reserve University, School of Medicine, Case Comprehensive Cancer Center, Cleveland, Ohio
    • ,
  • Vincent J. Pompili

      Affiliations

    • Department of Medicine, Case Western Reserve University, School of Medicine, Case Comprehensive Cancer Center, Cleveland, Ohio
    • ,
  • Mary J. Laughlin

      Affiliations

    • Department of Medicine, Case Western Reserve University, School of Medicine, Case Comprehensive Cancer Center, Cleveland, Ohio
    • Department of Pathology, Case Western Reserve University, School of Medicine, Case Comprehensive Cancer Center, Cleveland, Ohio
    • Corresponding Author InformationCorrespondence and reprint requests: Mary J. Laughlin, MD, Department of Medicine, Case Western Reserve University, School of Medicine, 10900 Euclid Ave., WRB2-129, Cleveland, OH 44106-7284

Received 25 August 2005 ,Accepted 23 December 2005.

References 

  1. Jones EL , Weintraub WS . The importance of completeness of revascularization during long-term follow-up after coronary artery operations . J Thorac Cardiovasc Surg . 1996;112:227–237
  2. Kawamoto A , Gwon HC , Iwaguro H , et al.   Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia . Circulation . 2001;103:634–637
  3. 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
  4. Kocher AA , Schuster MD , Szabolcs MJ , et al.   Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function . Nat Med . 2001;7:430–436
  5. Orlic D , Kajstura J , Chimenti S , et al.   Bone marrow cells regenerate infarcted myocardium . Nature . 2001;410:701–705
  6. 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
  7. Kamihata H , Matsubara H , Nishiue T , et al.   Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines . Circulation . 2001;104:1046–1052
  8. Fuchs S , Baffour R , Zhou YF , et al.   Transendocardial delivery of autologous bone marrow enhances collateral perfusion and regional function in pigs with chronic experimental myocardial ischemia . J Am Coll Cardiol . 2001;37:1726–1732
  9. Strauer BE , Brehm M , Zeus T , et al.   Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans . Circulation . 2002;106:1913–1918
  10. 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
  11. Stamm C , Westphal B , Kleine HD , et al.   Autologous bone-marrow stem-cell transplantation for myocardial regeneration . Lancet . 2003;361:45–46
  12. 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
  13. Folkman J . Angiogenesis in cancer, vascular, rheumatoid and other disease . Nat Med . 1995;1:27–31
  14. Asahara T , Murohara T , Sullivan A , et al.   Isolation of putative progenitor endothelial cells for angiogenesis . Science . 1997;275:964–967
  15. Shi Q , Rafii S , Wu MH , et al.   Evidence for circulating bone marrow-derived endothelial cells . Blood . 1998;92:362–367
  16. Asahara T , Takahashi T , Masuda H , et al.   VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells . EMBO J . 1999;18:3964–3972
  17. Takahashi T , Kalka C , Masuda H , et al.   Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization . Nat Med . 1999;5:434–438
  18. Kalka C , Tehrani H , Laudenberg B , et al.   VEGF gene transfer mobilizes endothelial progenitor cells in patients with inoperable coronary disease . Ann Thorac Surg . 2000;70:829–834
  19. Gehling UM , Ergun S , Schumacher U , et al.   In vitro differentiation of endothelial cells from AC133-positive progenitor cells . Blood . 2000;95:3106–3112
  20. Crosby JR , Kaminski WE , Schatteman G , et al.   Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation . Circ Res . 2000;87:728–730
  21. Iwaguro H , Yamaguchi J , Kalka C , et al.   Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration . Circulation . 2002;105:732–738
  22. Isner JM , Asahara T . Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization . J Clin Invest . 1999;103:1231–1236
  23. Laughlin MJ , Eapen M , Rubinstein P , et al.   Outcomes after transplantation of cord blood or bone marrow from unrelated donors in adults with leukemia . N Engl J Med . 2004;351:2265–2275
  24. Mayani H , Lansdorp PM . Thy-1 expression is linked to functional properties of primitive hematopoietic progenitor cells from human umbilical cord blood . Blood . 1994;83:2410–2417
  25. Vaziri H , Dragowska W , Allsopp RC , et al.   Evidence for a mitotic clock in human hematopoietic stem cells (loss of telomeric DNA with age) . Proc Natl Acad Sci U S A . 1994;91:9857–9860
  26. Murohara T , Ikeda H , Duan J , et al.   Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization . J Clin Invest . 2000;105:1527–1536
  27. Hristov M , Weber C . Endothelial progenitor cells (characterization, pathophysiology, and possible clinical relevance) . J Cell Mol Med . 2004;8:498–508
  28. Lapidot T , Pflumio F , Doedens M , et al.   Cytokine stimulation of multilineage hematopoiesis from immature human cells engrafted in SCID mice . Science . 1992;255:1137–1141
  29. Takeshita S , Tsurumi Y , Couffinahl T , et al.   Gene transfer of naked DNA encoding for three isoforms of vascular endothelial growth factor stimulates collateral development in vivo . Lab Invest . 1996;75:487–501
  30. De Falco E , Porcelli D , Torella AR , et al.   SDF-1 involvement in endothelial phenotype and ischemia-induced recruitment of bone marrow progenitor cells . Blood . 2004;104:3472–3482
  31. Hiasa K , Ishibashi M , Ohtani K , et al.   Gene transfer of stromal cell-derived factor-1alpha enhances ischemic vasculogenesis and angiogenesis via vascular endothelial growth factor/endothelial nitric oxide synthase-related pathway (next-generation chemokine therapy for therapeutic neovascularization) . Circulation . 2004;109:2454–2461
  32. 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
  33. Salven P , Mustjoki S , Alitalo R , Alitalo K , Rafii S . VEGFR-3 and CD133 identify a population of CD34+ lymphatic/vascular endothelial precursor cells . Blood . 2003;101:168–172
  34. Aoki M , Yasutake M , Murohara T . Derivation of functional endothelial progenitor cells from human umbilical cord blood mononuclear cells isolated by a novel cell filtration device . Stem Cells . 2004;22:994–1002
  35. Hildbrand P , Cirulli V , Prinsen RC , et al.   The role of angiopoietins in the development of endothelial cells from cord blood CD34+ progenitors . Blood . 2004;104:2010–2019
  36. Le Ricousse-Roussanne S , Barateau V , Contreres JO , et al.   Ex vivo differentiated endothelial and smooth muscle cells from human cord blood progenitors home to the angiogenic tumor vasculature . Cardiovasc Res . 2004;62:176–184
  37. Beck L , D’Amore PA . Vascular development (cellular and molecular regulation) . FASEB J . 1997;11:365–373
  38. Daniel TO , Abrahamson D . Endothelial signal integration in vascular assembly . Annu Rev Physiol . 2000;62:649–671
  39. Ceradini DJ , Kulkarni AR , Callaghan MJ , et al.   Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1 . Nat Med . 2004;10:858–864
  40. Yamaguchi J , Kusano KF , Masuo O , et al.   Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization . Circulation . 2003;107:1322–1328
  41. Hiasa K , Ishibashi M , Ohtani K , et al.   Gene transfer of stromal cell-derived factor-1alpha enhances ischemic vasculogenesis and angiogenesis via vascular endothelial growth factor/endothelial nitric oxide synthase-related pathway (next-generation chemokine therapy for therapeutic neovascularization) . Circulation . 2004;109:2454–2461
  42. Salvucci O , Yao L , Villalba S , et al.   Regulation of endothelial cell branching morphogenesis by endogenous chemokine stromal-derived factor-1 . Blood . 2002;99:2703–2711
  43. Mirshahi F , Pourtau J , Li H , et al.   SDF-1 activity on microvascular endothelial cells (consequences on angiogenesis in in vitro and in vivo models) . Thromb Res . 2000;15:587–594
  44. Zhang XQ , Takakura N , Oike Y , et al.   Stromal cells expressing ephrin-B2 promote the growth and sprouting of ephrin-B2(+) endothelial cells . Blood . 2001;98:1028–1037
  45. Oike Y , Ito Y , Hamada K , et al.   Regulation of vasculogenesis and angiogenesis by EphB/ephrin-B2 signaling between endothelial cells and surrounding mesenchymal cells . Blood . 2002;100:1326–1333
  46. Arias E , MacDorman MF , Strobino DM , Guyer B . Annual summary of vital statistics—2002 . Pediatrics . 2003;112:1215–1230
  47. Van Zant G , Liang Y . The role of stem cells in aging . Exp Hematol . 2003;31:659–672
  48. Maslov AY , Barone TA , Plunkett RJ , Pruitt SC . Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice . J Neurosci . 2004;24:1726–1733
  49. Stenderup K , Justesen J , Clausen C , Kassem M . Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells . Bone . 2003;33:919–926
  50. Torella D , Rota M , Nurzynska D , et al.   Cardiac stem cell and myocyte aging, heart failure, and insulin-like growth factor-1 overexpression . Circ Res . 2004;94:514–524
  51. Almici C , Carlo-Stella C , Wagner JE , et al.   Biologic and phenotypic analysis of early hematopoietic progenitor cells in umbilical cord blood . Leukemia . 1997;11:2143–2149
  52. Rubinstein P , Carrier C , Scaradavou A , et al.   Outcomes among 562 recipients of placental-blood transplants from unrelated donors . N Engl J Med . 1998;339:1565–1577

 M.J.L. and V.J.P. share senior authorship.

PII: S1083-8791(05)01449-7

doi: 10.1016/j.bbmt.2005.12.037

Biology of Blood and Marrow Transplantation
Volume 12, Issue 5 , Pages 585-593 , May 2006

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