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Neovascularization and Hematopoietic Stem Cells

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Abstract

Vasculogenesis and angiogenesis are the major forms of blood vessel formation. Angiogenesis is the process where new vessels grow from pre-existing blood vessels, and is very important in the functional recovery of pathological conditions, such as wound healing and ischemic heart diseases. The development of better animal model and imaging technologies in past decades has greatly enriched our understanding on vasculogenesis and angiogenesis processes. Hypoxia turned out to be an important driving force for angiogenesis in various ischemic conditions. It stimulates expression of many growth factors like vascular endothelial growth factor, platelet-derived growth factor, insulin-like growth factor, and fibroblast growth factor, which play critical role in induction of angiogenesis. Other cellular components like monocytes, T cells, neutrophils, and platelets also play significant role in induction and regulation of angiogenesis. Various stem/progenitor cells also being recruited to the ischemic sites play crucial role in the angiogenesis process. Pre-clinical studies showed that stem/progenitor cells with/without combination of growth factors induce neovascularization in the ischemic tissues in various animal models. In this review, we will discuss about the fundamental factors that regulate the angiogenesis process and the use of stem cells as therapeutic regime for the treatment of ischemic diseases.

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References

  1. Lloyd-Jones, D., Adams, R., Carnethon, M., De Simone, G., Ferguson, T. B., Flegal, K., et al. (2009). Heart disease and stroke statistics–2009 update: a report from the American heart association statistics committee and stroke statistics subcommittee. Circulation, 119(3), 480–486.

    PubMed  Google Scholar 

  2. Cha, K. S., Schwartz, R. S., & Henry, T. D. (2005). Myocardial angiogenesis protein growth factors. In R. J. Laham & D. S. Baim (Eds.), Contemporary cardiology: Angiogenesis and direct myocardial revasularization. Totowa, NJ: Humana Press Inc.

    Google Scholar 

  3. Mukherjee, D., Bhatt, D. L., Roe, M. T., Patel, V., & Ellis, S. G. (1999). Direct myocardial revascularization and angiogenesis–how many patients might be eligible? American Journal of Cardiology, 84(5), 598–600. A8.

    PubMed  CAS  Google Scholar 

  4. Shah, P. B., Lotun, K., & Losordo, D. W. (2005). Gene therapy for angiogenesis in the treatment of cardiovascular and peripheral arterial disease. In R. J. Laham & D. S. Baim (Eds.), Contemporary cardiology: angiogenesis and direct myocardial revasularization. Totowa: Humana Press Inc.

    Google Scholar 

  5. Schaper, W., & Ito, W. D. (1996). Molecular mechanisms of coronary collateral vessel growth. Circulation Research, 79(5), 911–919.

    PubMed  CAS  Google Scholar 

  6. Ware, J. A., & Simons, M. (1997). Angiogenesis in ischemic heart disease. Nature Medicine, 3(2), 158–164.

    PubMed  CAS  Google Scholar 

  7. Folkman, J. (1998). Angiogenic therapy of the human heart. Circulation, 97(7), 628–629.

    PubMed  CAS  Google Scholar 

  8. Das, H., George, J. C., Joseph, M., Das, M., Abdulhameed, N., Blitz, A., et al. (2009). Stem cell therapy with overexpressed VEGF and PDGF genes improves cardiac function in a rat infarct model. Plos One, 4(10), e7325.

    PubMed  Google Scholar 

  9. Carmeliet, P. (2005). Angiogenesis in life, disease and medicine. Nature, 438(7070), 932–936.

    PubMed  CAS  Google Scholar 

  10. Byrd, N., & Gradel, L. (2004). Hedgehog signaling in murine vasculogenesis and angiogenesis. Trends in Cardiovascular Medicine, 14(8), 308–313.

    PubMed  CAS  Google Scholar 

  11. Pugh, C. W., & Ratcliffe, P. J. (2003). Regulation of angiogenesis by hypoxia: role of the HIF system. Nature Medicine, 9(6), 677–684.

    PubMed  CAS  Google Scholar 

  12. Egami, K., Murohara, T., Aoki, M., & Matsuishi, T. (2006). Ischemia-induced angiogenesis: role of inflammatory response mediated by P-selectin. Journal of Leukocyte Biology, 79(5), 971–976.

    PubMed  CAS  Google Scholar 

  13. Suchting, S., & Eichmann, A. (2009). Jagged gives endothelial tip cells an edge. Cell, 137(6), 988–990.

    PubMed  CAS  Google Scholar 

  14. Phng, L. K., & Gerhardt, H. (2009). Angiogenesis: a team effort coordinated by notch. Developmental Cell, 16(2), 196–208.

    PubMed  CAS  Google Scholar 

  15. Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., et al. (2003). VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. Journal of Cell Biology, 161(6), 1163–1177.

    PubMed  CAS  Google Scholar 

  16. Iruela-Arispe, M. L., & Davis, G. E. (2009). Cellular and molecular mechanisms of vascular lumen formation. Developmental Cell, 16(2), 222–231.

    PubMed  CAS  Google Scholar 

  17. Blum, Y., Belting, H. G., Ellertsdottir, E., Herwig, L., Luders, F., & Affolter, M. (2008). Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. Developmental Biology, 316(2), 312–322.

    PubMed  CAS  Google Scholar 

  18. Goetze, J. P., Gore, A., Moller, C. H., Steinbruchel, D. A., Rehfeld, J. F., & Nielsen, L. B., (2004). Acute myocardial hypoxia increases BNP gene expression. FASEB Journal, 18(12), 1928–1930.

    Google Scholar 

  19. Smith, L. M., Golub, A. S., & Pittman, R. N. (2002). Interstitial Po-2 determination by phosphorescence quenching microscopy. Microcirculation, 9(5), 389–395.

    PubMed  Google Scholar 

  20. Fong, G. H. (2009). Regulation of angiogenesis by oxygen sensing mechanisms. Journal of Molecular Medicine, 87(6), 549–560.

    PubMed  CAS  Google Scholar 

  21. Kaelin, W. G., & Ratcliffe, P. J. (2008). Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Molecular Cell, 30(4), 393–402.

    PubMed  CAS  Google Scholar 

  22. Ramirez-Bergeron, D. L., Runge, A., Dahl, K. D. C., Fehling, H. J., Keller, G., & Simon, M. C. (2004). Hypoxia affects mesoderm and enhances hemangioblast specification during early development. Development, 131(18), 4623–4634.

    PubMed  CAS  Google Scholar 

  23. Tillmanns, J., Rota, M., Hosoda, T., Misao, Y., Esposito, G., Gonzalez, A., et al. (2008). Formation of large coronary arteries by cardiac progenitor cells. Proceedings of the National Academy of Sciences of the United States of America, 105(5), 1668–1673.

    PubMed  CAS  Google Scholar 

  24. Du, R., Lu, K. V., Petritsch, C., Liu, P., Ganss, R., Passegue, E., et al. (2008). HIF1 alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell, 13(3), 206–220.

    PubMed  CAS  Google Scholar 

  25. Ceradini, D. J., Kulkarni, A. R., Callaghan, M. J., Tepper, O. M., Bastidas, N., Kleinman, M. E., et al. (2004). Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nature Medicine, 10(8), 858–864.

    PubMed  CAS  Google Scholar 

  26. Lee, S. P., Youn, S. W., Cho, H. J., Li, L., Kim, T. Y., Yook, H. S., et al. (2006). Integrin-linked kinase, a hypoxia-responsive molecule, controls postnatal vasculogenesis by recruitment of endothelial progenitor cells to ischemic tissue. Circulation, 114(2), 150–159.

    PubMed  CAS  Google Scholar 

  27. Fraisl, P., Mazzone, M., Schmidt, T., & Carmeliet, P. (2009). Regulation of angiogenesis by oxygen and metabolism. Dev Cell, 16(2), 167–179.

    PubMed  CAS  Google Scholar 

  28. Schumacher, B., Pecher, P., von Specht, B. U., & Stegmann, T. (1998). Induction of neoangiogenesis in ischemic myocardium by human growth factors: first clinical results of a new treatment of coronary heart disease. Circulation, 97(7), 645–650.

    PubMed  CAS  Google Scholar 

  29. Laham, R. J., Sellke, F. W., Edelman, E. R., Pearlman, J. D., Ware, J. A., Brown, D. L., et al. (1999). Local perivascular delivery of basic fibroblast growth factor in patients undergoing coronary bypass surgery: results of a phase I randomized, double-blind, placebo-controlled trial. Circulation, 100(18), 1865–1871.

    PubMed  CAS  Google Scholar 

  30. Ruel, M., Laham, R. J., Parker, J. A., Post, M. J., Ware, J. A., Simons, M., et al. (2002). Long-term effects of surgical angiogenic therapy with fibroblast growth factor 2 protein. Journal of Thoracic and Cardiovascular Surgery, 124(1), 28–34.

    PubMed  CAS  Google Scholar 

  31. Laham, R. J., Chronos, N. A., Pike, M., Leimbach, M. E., Udelson, J. E., Pearlman, J. D., et al. (2000). Intracoronary basic fibroblast growth factor (FGF-2) in patients with severe ischemic heart disease: results of a phase I open-label dose escalation study. Journal of the American College of Cardiology, 36(7), 2132–2139.

    PubMed  CAS  Google Scholar 

  32. Unger, E. F., Goncalves, L., Epstein, S. E., Chew, E. Y., Trapnell, C. B., Cannon, R. O., 3rd, et al. (2000). Effects of a single intracoronary injection of basic fibroblast growth factor in stable angina pectoris. American Journal of Cardiology, 85(12), 1414–1419.

    PubMed  CAS  Google Scholar 

  33. Udelson, J. E., Dilsizian, V., Laham, R. J., Chronos, N., Vansant, J., Blais, M., et al. (2000). Therapeutic angiogenesis with recombinant fibroblast growth factor-2 improves stress and rest myocardial perfusion abnormalities in patients with severe symptomatic chronic coronary artery disease. Circulation, 102(14), 1605–1610.

    PubMed  CAS  Google Scholar 

  34. Simons, M., Annex, B. H., Laham, R. J., Kleiman, N., Henry, T., Dauerman, H., et al. (2002). Pharmacological treatment of coronary artery disease with recombinant fibroblast growth factor-2: double-blind, randomized, controlled clinical trial. Circulation, 105(7), 788–793.

    PubMed  CAS  Google Scholar 

  35. Hendel, R. C., Henry, T. D., Rocha-Singh, K., Isner, J. M., Kereiakes, D. J., Giordano, F. J., et al. (2000). Effect of intracoronary recombinant human vascular endothelial growth factor on myocardial perfusion: evidence for a dose-dependent effect. Circulation, 101(2), 118–121.

    PubMed  CAS  Google Scholar 

  36. Henry, T. D., Rocha-Singh, K., Isner, J. M., Kereiakes, D. J., Giordano, F. J., Simons, M., et al. (2001). Intracoronary administration of recombinant human vascular endothelial growth factor to patients with coronary artery disease. American Heart Journal, 142(5), 872–880.

    PubMed  CAS  Google Scholar 

  37. Henry, T. D., Annex, B. H., McKendall, G. R., Azrin, M. A., Lopez, J. J., Giordano, F. J., et al. (2003). The VIVA trial: vascular endothelial growth factor in Ischemia for vascular angiogenesis. Circulation, 107(10), 1359–1365.

    PubMed  CAS  Google Scholar 

  38. Seiler, C., Pohl, T., Wustmann, K., Hutter, D., Nicolet, P. A., Windecker, S., et al. (2001). Promotion of collateral growth by granulocyte-macrophage colony-stimulating factor in patients with coronary artery disease: a randomized, double-blind, placebo-controlled study. Circulation, 104(17), 2012–2017.

    PubMed  CAS  Google Scholar 

  39. Pecher, P., & Schumacher, B. A. (2000). Angiogenesis in ischemic human myocardium: clinical results after 3 years. Annals of Thoracic Surgery, 69(5), 1414–1419.

    PubMed  CAS  Google Scholar 

  40. Vale, P. R., Losordo, D. W., Milliken, C. E., McDonald, M. C., Gravelin, L. M., Curry, C. M., et al. (2001). Randomized, single-blind, placebo-controlled pilot study of catheter-based myocardial gene transfer for therapeutic angiogenesis using left ventricular electromechanical mapping in patients with chronic myocardial ischemia. Circulation, 103(17), 2138–2143.

    PubMed  CAS  Google Scholar 

  41. Losordo, D. W., Vale, P. R., Hendel, R. C., Milliken, C. E., Fortuin, F. D., Cummings, N., et al. (2002). Phase 1/2 placebo-controlled, double-blind, dose-escalating trial of myocardial vascular endothelial growth factor 2 gene transfer by catheter delivery in patients with chronic myocardial ischemia. Circulation, 105(17), 2012–2018.

    PubMed  CAS  Google Scholar 

  42. Grines, C. L., Watkins, M. W., Helmer, G., Penny, W., Brinker, J., Marmur, J. D., et al. (2002). Angiogenic gene therapy (AGENT) trial in patients with stable angina pectoris. Circulation, 105(11), 1291–1297.

    PubMed  CAS  Google Scholar 

  43. Grines, C. L., Watkins, M. W., Mahmarian, J. J., Iskandrian, A. E., Rade, J. J., Marrott, P., et al. (2003). A randomized double-blind, placebo-controlled trial of Ad5FGF-4 gene therapy and its effect on myocardial perfusion in patients with stable angina. Journal of the American College of Cardiology, 42(8), 1339–1347.

    PubMed  CAS  Google Scholar 

  44. Ruel, M., Beanlands, R. S., Lortie, M., Chan, V., Camack, N., deKemp, R. A., Suuronen, E. J., Rubens, F. D., DaSilva, J. N., Sellke, F. W., Stewart, D. J., & Mesana, T. G., (2008). Concomitant treatment with oral l-arginine improves the efficacy of surgical angiogenesis in patients with severe diffuse coronary artery disease: the endothelial modulation in angiogenic therapy randomized controlled trial. Journal of Thoracic and Cardiovascular Surgery, 135(4), 762–770, 770 e1.

    Google Scholar 

  45. Bikfalvi, A., & Bicknell, R. (2002). Recent advances in angiogenesis, anti-angiogenesis and vascular targeting. Trends in Pharmacological Sciences, 23(12), 576–582.

    PubMed  CAS  Google Scholar 

  46. Shalaby, F., Rossant, J., Yamaguchi, T. P., Gertsenstein, M., Wu, X. F., Breitman, M. L., et al. (1995). Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature, 376(6535), 62–66.

    PubMed  CAS  Google Scholar 

  47. Shalaby, F., Ho, J., Stanford, W. L., Fischer, K. D., Schuh, A. C., Schwartz, L., et al. (1997). A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell, 89(6), 981–990.

    PubMed  CAS  Google Scholar 

  48. Choi, K., Kennedy, M., Kazarov, A., Papadimitriou, J. C., & Keller, G. (1998). A common precursor for hematopoietic and endothelial cells. Development, 125(4), 725–732.

    PubMed  CAS  Google Scholar 

  49. Chung, Y. S., Zhang, W. J., Arentson, E., Kingsley, P. D., Palis, J., & Choi, K. (2002). Lineage analysis of the hemangioblast as defined by FLK1 and SCL expression. Development, 129(23), 5511–5520.

    PubMed  CAS  Google Scholar 

  50. Ema, M., & Rossant, J. (2003). Cell fate decisions in early blood vessel formation. Trends in Cardiovascular Medicine, 13(6), 254–259.

    PubMed  CAS  Google Scholar 

  51. Ghabrial, A. S., & Krasnow, M. A. (2006). Social interactions among epithelial cells during tracheal branching morphogenesis. Nature, 441(7094), 746–749.

    PubMed  CAS  Google Scholar 

  52. Bentley, K., Gerhardt, H., & Bates, P. A. (2008). Agent-based simulation of Notch-mediated tip cell selection in angiogenic sprout initialisation. Journal of Theoretical Biology, 250(1), 25–36.

    PubMed  CAS  Google Scholar 

  53. Gille, H., Kowalski, J., Li, B., LeCouter, J., Moffat, B., Zioncheck, T. F., et al. (2001). Analysis of biological effects and signaling properties of Flt-1 (VEGFR-1) and KDR (VEGFR-2)—a reassessment using novel receptor-specific vascular endothelial growth factor mutants. Journal of Biological Chemistry, 276(5), 3222–3230.

    PubMed  CAS  Google Scholar 

  54. Roca, C., & Adams, R. H. (2007). Regulation of vascular morphogenesis by Notch signaling. Genes and Development, 21(20), 2511–2524.

    PubMed  CAS  Google Scholar 

  55. Hellstrom, M., Phng, L. K., Hofmann, J. J., Wallgard, E., Coultas, L., Lindblom, P., et al. (2007). Dll4 signaling through Notch1 regulates formation of tip cells during angiogenesis. Nature, 445(7129), 776–780.

    PubMed  Google Scholar 

  56. Suchting, S., Freitas, C., le Noble, F., Benedito, R., Breant, C., Duarte, A., et al. (2007). The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proceedings of the National Academy of Sciences of the United States of America, 104(9), 3225–3230.

    PubMed  CAS  Google Scholar 

  57. Tammela, T., Zarkada, G., Wallgard, E., Murtomaki, A., Suchting, S., Wirzenius, M., et al. (2008). Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature, 454(7204), 656–660.

    PubMed  CAS  Google Scholar 

  58. Leslie, J. D., Ariza-McNaughton, L., Bermange, A. L., McAdow, R., Johnson, S. L., & Lewis, J. (2007). Endothelial signaling by the Notch ligand Delta-like 4 restricts angiogenesis. Development, 134(5), 839–844.

    PubMed  CAS  Google Scholar 

  59. Siekmann, A. F., & Lawson, N. D. (2007). Notch signaling limits angiogenic cell behaviour in developing zebrafish arteries. Nature, 445(7129), 781–784.

    PubMed  CAS  Google Scholar 

  60. Siekmann, A. F., Covassin, L., & Lawson, N. D. (2008). Modulation of VEGF signaling output by the Notch pathway. Bioessays, 30(4), 303–313.

    PubMed  CAS  Google Scholar 

  61. Dou, G. R., Wang, Y. C., Hu, X. B., Hou, L. H., Wang, C. M., Xu, J. F., et al. (2008). RBPJ the transcription factor downstream of Notch receptors, is essential for the maintenance of vascular homeostasis in adult mice. FASEB Journal, 22(5), 1606–1617.

    PubMed  CAS  Google Scholar 

  62. Liu, Z. J., Xiao, M., Balint, K., Soma, A., Pinnix, C. C., Capobianco, A. J., Velazquez, O. C., & Herlyn, M. (2006). Inhibition of endothelial cell proliferation by Notch1 signaling is mediated by repressing MAPK and PI3 K/Akt pathways and requires MAML1. FASEB Journal, 20(7), 1009–1011.

    Google Scholar 

  63. Noseda, M., Chang, L., McLean, G., Grim, J. E., Clurman, B. E., Smith, L. L., et al. (2004). Notch activation induces endothelial cell cycle arrest and participates in contact inhibition: role of p21Cip1 repression. Molecular and Cellular Biology, 24(20), 8813–8822.

    PubMed  CAS  Google Scholar 

  64. Harrington, L. S., Sainson, R. C., Williams, C. K., Taylor, J. M., Shi, W., Li, J. L., et al. (2008). Regulation of multiple angiogenic pathways by Dll4 and Notch in human umbilical vein endothelial cells. Microvascular Research, 75(2), 144–154.

    PubMed  CAS  Google Scholar 

  65. Trindade, A., Kumar, S. R., Scehnet, J. S., Lopes-da-Costa, L., Becker, J., Jiang, W., et al. (2008). Overexpression of delta-like 4 induces arterialization and attenuates vessel formation in developing mouse embryos. Blood, 112(5), 1720–1729.

    PubMed  CAS  Google Scholar 

  66. Silvestre, J. S., Mallat, Z., Tedgui, A., & Levy, B. I. (2008). Post-ischaemic neovascularization and inflammation. Cardiovascular Research, 78(2), 242–249.

    PubMed  CAS  Google Scholar 

  67. Heil, M., & Schaper, W. (2007). Insights into pathways of arteriogenesis. Current Pharmaceutical Biotechnology, 8(1), 35–42.

    PubMed  CAS  Google Scholar 

  68. Heil, M., Ziegelhoeffer, T., Pipp, F., Kostin, S., Martin, S., Clauss, M., et al. (2002). Blood monocyte concentration is critical for enhancement of collateral artery growth. American Journal of Physiology-Heart and Circulatory Physiology, 283(6), H2411–H2419.

    PubMed  CAS  Google Scholar 

  69. Capoccia, B. J., Shepherd, R. M., & Link, D. C. (2006). G-CSF and AMD3100 mobilize monocytes into the blood that stimulate angiogenesis in vivo through a paracrine mechanism. Blood, 108(7), 2438–2445.

    PubMed  CAS  Google Scholar 

  70. Stabile, E., Burnett, M. S., Watkins, C., Kinnaird, T., Bachis, A., la Sala, A., et al. (2003). Impaired arteriogenic response to acute hindlimb ischemia in CD4-knockout mice. Circulation, 108(2), 205–210.

    PubMed  Google Scholar 

  71. Couffinhal, T., Silver, M., Kearney, M., Sullivan, A., Witzenbichler, B., Magner, M., et al. (1999). Impaired collateral vessel development associated with reduced expression of vascular endothelial growth factor in ApoE(-/-) mice. Circulation, 99(24), 3188–3198.

    PubMed  CAS  Google Scholar 

  72. Stabile, E., Kinnaird, T., la Sala, A., Hanson, S. K., Watkins, C., Campia, U., et al. (2006). CD8(+) T lymphocytes regulate the arteriogenic response to ischemia by infiltrating the site of collateral vessel development and recruiting CD4(+) mononuclear cells through the expression of interleukin-16. Circulation, 113(1), 118–124.

    PubMed  Google Scholar 

  73. van Weel, V., Toes, R. E. M., Seghers, L., Deckers, M. M. L., de Vries, M. R., Eilers, P. H., et al. (2007). Natural killer cells and CD4(+) T-Cells modulate collateral artery development. Arteriosclerosis, Thrombosis, and Vascular Biology, 27(11), 2310–2318.

    PubMed  Google Scholar 

  74. Iba, O., Matsubara, H., Nozawa, Y., Fujiyama, S., Amano, K., Mori, Y., et al. (2002). Angiogenesis by implantation of peripheral blood mononuclear cells and platelets into ischemic limbs. Circulation, 106(15), 2019–2025.

    PubMed  CAS  Google Scholar 

  75. Griendling, K. K., & FitzGerald, G. A. (2003). Oxidative stress and cardiovascular injury—Part I: basic mechanisms and in vivo monitoring of ROS. Circulation, 108(16), 1912–1916.

    PubMed  Google Scholar 

  76. Griendling, K. K., & FitzGerald, G. A. (2003). Oxidative stress and cardiovascular injury—Part II: animal and human studies. Circulation, 108(17), 2034–2040.

    PubMed  Google Scholar 

  77. Li, J. M., & Shah, A. M. (2004). Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. American Journal of Physiology-Regulatory Integrative and Comparative Physiology, 287(5), R1014–R1030.

    CAS  Google Scholar 

  78. Yasuda, M., Ohzeki, Y., Shimizu, S., Naito, S., Ohtsuru, A., Yamamoto, T., et al. (1998). Stimulation of in vitro angiogenesis by hydrogen peroxide and the relation with ETS-1 in endothelial cells. Life Sciences, 64(4), 249–258.

    Google Scholar 

  79. Gerald, D., Berra, E., Frapart, Y. M., Chan, D. A., Giaccia, A. J., Mansuy, D., et al. (2004). JunD reduces tumor angiogenesis by protecting cells from oxidative stress. Cell, 118(6), 781–794.

    PubMed  CAS  Google Scholar 

  80. Guzy, R. D., & Schumacker, P. T. (2006). Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Experimental Physiology, 91(5), 807–819.

    PubMed  CAS  Google Scholar 

  81. Ebrahimian, T. G., Heymes, C., You, D., Blanc-Brude, O., Mees, B., Waeckel, L., et al. (2006). NADPH oxidase-derived overproduction of reactive oxygen species impairs postischemic neovascularization in mice with type 1 diabetes. American Journal of Pathology, 169(2), 719–728.

    PubMed  CAS  Google Scholar 

  82. Bayraktutan, U., Blayney, L., & Shah, A. M. (2000). Molecular characterization and localization of the NAD(P)H oxidase components gp91-phox and p22-phox in endothelial cells. Arteriosclerosis, Thrombosis, and Vascular Biology, 20(8), 1903–1911.

    PubMed  CAS  Google Scholar 

  83. Duilio, C., Ambrosio, G., Kuppusamy, P., DiPaula, A., Becker, L. C., & Zweier, J. L. (2001). Neutrophils are primary source of O2 radicals during reperfusion after prolonged myocardial ischemia. American Journal of Physiology–Heart and Circulatory Physiolology, 280(6), H2649–H2657.

    CAS  Google Scholar 

  84. Golino, P., Ragni, M., Cirillo, P., Avvedimento, V. E., Feliciello, A., Esposito, N., et al. (1996). Effects of tissue factor induced by oxygen free radicals on coronary flow during reperfusion. Nature Medicine, 2(1), 35–40.

    PubMed  CAS  Google Scholar 

  85. Harlan, J. M., Killen, P. D., Harker, L. A., Striker, G. E., & Wright, D. G. (1981). Neutrophil-mediated endothelial injury in vitro mechanisms of cell detachment. Journal of Clinical Investigation, 68(6), 1394–1403.

    PubMed  CAS  Google Scholar 

  86. May, A. E., Seizer, P., & Gawaz, M. (2008). Platelets: inflammatory firebugs of vascular walls. Arteriosclerosis, Thrombosis, and Vascular Biology, 28(3), S5–S10.

    PubMed  CAS  Google Scholar 

  87. Nierodzik, M. L., & Karpatkin, S. (2006). Thrombin induces tumor growth, metastasis, and angiogenesis: evidence for a thrombin-regulated dormant tumor phenotype. Cancer Cell, 10(5), 355–362.

    PubMed  CAS  Google Scholar 

  88. De Paula, E. V., Nascimento, M. C. F., Ramos, C. D., Ozelo, M. C., Machado, T. F., Guillaumon, A. T., et al. (2006). Early in vivo anticoagulation inhibits the angiogenic response following hindlimb ischemia in a rodent model. Thrombosis and Haemostasis, 96(1), 68–72.

    PubMed  Google Scholar 

  89. Rafii, S., & Lyden, D. (2003). Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nature Medicine, 9(6), 702–712.

    PubMed  CAS  Google Scholar 

  90. Rajantie, I., Ilmonen, M., Alminaite, A., Ozerdem, U., Alitalo, K., & Salven, P. (2004). Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells. Blood, 104(7), 2084–2086.

    PubMed  CAS  Google Scholar 

  91. Ziegelhoeffer, T., Fernandez, B., Kostin, S., Heil, M., Voswinckel, R., Helisch, A., et al. (2004). Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circulation Research, 94(2), 230–238.

    PubMed  CAS  Google Scholar 

  92. Peters, B. A., Diaz, L. A., Polyak, K., Meszler, L., Romans, K., Guinan, E. C., et al. (2005). Contribution of bone marrow-derived endothelial cells to human tumor vasculature. Nature Medicine, 11(3), 261–262.

    PubMed  CAS  Google Scholar 

  93. Hattori, K., Dias, S., Heissig, B., Hackett, N. R., Lyden, D., Tateno, M., et al. (2001). Vascular endothelial growth factor and angiopoietin-1 stimulate postnatal hematopoiesis by recruitment of vasculogenic and hematopoietic stem cells. Journal of Experimental Medicine, 193(9), 1005–1014.

    PubMed  CAS  Google Scholar 

  94. Tepper, O. M., Galiano, R. D., Capla, J. M., Kalka, C., Gagne, P. J., Jacobowitz, G. R., et al. (2002). Human endothelial progenitor exhibit impaired proliferation, cells from type II diabetics adhesion, and incorporation into vascular structures. Circulation, 106(22), 2781–2786.

    PubMed  Google Scholar 

  95. Asahara, T., Masuda, H., Takahashi, T., Kalka, C., Pastore, C., Silver, M., et al. (1999). Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circulation Research, 85(3), 221–228.

    PubMed  CAS  Google Scholar 

  96. Crosby, J. R., Kaminski, W. E., Schatteman, G., Martin, P. J., Raines, E. W., Seifert, R. A., et al. (2000). Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circulation Research, 87(9), 728–730.

    PubMed  CAS  Google Scholar 

  97. Takahashi, T., Kalka, C., Masuda, H., Chen, D., Silver, M., Kearney, M., et al. (1999). Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nature Medicine, 5(4), 434–438.

    PubMed  CAS  Google Scholar 

  98. Lin, Y., Weisdorf, D. J., Solovey, A., & Hebbel, R. P. (2000). Origins of circulating endothelial cells and endothelial outgrowth from blood. Journal of Clinical Investigation, 105(1), 71–77.

    PubMed  CAS  Google Scholar 

  99. Aicher, A., Rentsch, M., Sasaki, K., Ellwart, J. W., Fandrich, F., Siebert, R., et al. (2007). Non bonemarrow-derived circulating progenitor cells contribute to postnatal neovascularization following tissue ischemia. Circulation Research, 100(4), 581–589.

    PubMed  CAS  Google Scholar 

  100. You, D., Waeckel, L., Ebrahimian, T. G., Blanc-Brude, O., Foubert, P., Barateau, V., et al. (2006). Increase in vascular permeability and vasodilation are critical for proangiogenic effects of stem cell therapy. Circulation, 114(4), 328–338.

    PubMed  Google Scholar 

  101. Urbich, C., Aicher, A., Heeschen, C., Dernbach, E., Hofmann, W. K., Zeiher, A. M., et al. (2005). Soluble factors released by endothelial progenitor cells promote migration of endothelial cells and cardiac resident progenitor cells. Journal of Molecular and Cellular Cardiology, 39(5), 733–742.

    PubMed  CAS  Google Scholar 

  102. Rehman, J., Li, J., Orschell, C. M., & March, K. L. (2003). Peripheral blood “endothelial progenitor cells” are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation, 107(8), 1164–1169.

    PubMed  Google Scholar 

  103. Hur, J., Yoon, C. H., Kim, H. S., Choi, J. H., Kang, H. J., Hwang, K. K., et al. (2004). Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arteriosclerosis, Thrombosis, and Vascular Biology, 24(2), 288–293.

    PubMed  CAS  Google Scholar 

  104. Tordjman, R., Delaire, S., Plouet, J., Ting, S., Gaulard, P., Fichelson, S., et al. (2001). Erythroblasts are a source of angiogenic factors. Blood, 97(7), 1968–1974.

    PubMed  CAS  Google Scholar 

  105. Huang, Y. Q., Li, J. J., & Karpatkin, S. (2000). Identification of a family of alternatively spliced mRNA species of angiopoietin-1. Blood, 95(6), 1993–1999.

    PubMed  CAS  Google Scholar 

  106. Coussens, L. M., Tinkle, C. L., Hanahan, D., & Werb, Z. (2000). MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell, 103(3), 481–490.

    PubMed  CAS  Google Scholar 

  107. Grant, M. B., May, W. S., Caballero, S., Brown, G. A., Guthrie, S. M., Mames, R. N., et al. (2002). Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nature Medicine, 8(6), 607–612.

    PubMed  CAS  Google Scholar 

  108. Bailey, A. S., Jiang, S. G., Afentoulis, M., Baumann, C. I., Schroeder, D. A., Olson, S. B., et al. (2004). Transplanted adult hematopoietic stems cells differentiate into functional endothelial cells. Blood, 103(1), 13–19.

    PubMed  CAS  Google Scholar 

  109. Takakura, N., Watanabe, T., Suenobu, S., Yamada, Y., Noda, T., Ito, Y., et al. (2000). A role for hematopoietic stem cells in promoting angiogenesis. Cell, 102(2), 199–209.

    PubMed  CAS  Google Scholar 

  110. Carmeliet, P. (2003). Angiogenesis in health and disease. Nature Medicine, 9(6), 653–660.

    PubMed  CAS  Google Scholar 

  111. Gehling, U. M., Ergun, S., Schumacher, U., Wagener, C., Pantel, K., Otte, M., et al. (2000). In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood, 95(10), 3106–3112.

    PubMed  CAS  Google Scholar 

  112. Urbich, C., & Dimmeler, S. (2004). Endothelial progenitor cells—characterization and role in vascular biology. Circulation Research, 95(4), 343–353.

    PubMed  CAS  Google Scholar 

  113. Nieda, M., Nicol, A., Denning-Kendall, P., Sweetenham, J., Bradley, B., & Hows, J. (1997). Endothelial cell precursors are normal components of human umbilical cord blood. British Journal Haematology, 98(3), 775–777.

    CAS  Google Scholar 

  114. Rookmaaker, M. B., Verhaar, M. C., Loomans, C. J., Verloop, R., Peters, E., Westerweel, P. E., et al. (2005). CD34+ cells home, proliferate, and participate in capillary formation, and in combination with CD34− cells enhance tube formation in a 3-dimensional matrix. Arteriosclerosis, Thrombosis, and Vascular Biology, 25(9), 1843–1850.

    PubMed  CAS  Google Scholar 

  115. Murohara, T., Ikeda, H., Duan, J., Shintani, S., Sasaki, K., Eguchi, H., et al. (2000). Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. Journal of Clinical Investigation, 105(11), 1527–1536.

    PubMed  CAS  Google Scholar 

  116. Ma, N., Stamm, C., Kaminski, A., Li, W., Kleine, H. D., Muller-Hilke, B., et al. (2005). Human cord blood cells induce angiogenesis following myocardial infarction in NOD/scid-mice. Cardiovascular Research, 66(1), 45–54.

    PubMed  CAS  Google Scholar 

  117. Ma, N., Ladilov, Y., Moebius, J. M., Ong, L., Piechaczek, C., David, A., et al. (2006). Intramyocardial delivery of human CD133 + cells in a SCID mouse cryoinjury model: bone marrow vs. cord blood-derived cells. Cardiovascular Research, 71(1), 158–169.

    PubMed  CAS  Google Scholar 

  118. Bababeygy, S. R., Cheshier, S. H., Hou, L. C., Higgins, D. M., Weissman, I. L., & Tse, V. C. (2008). Hematopoietic stem cell-derived pericytic cells in brain tumor angio-architecture. Stem Cells and Development, 17(1), 11–18.

    PubMed  CAS  Google Scholar 

  119. Das, H., Abdulhameed, N., Joseph, M., Sakthivel, R., Mao, H. Q., & Pompili, V. J. (2009). Ex vivo nanofiber expansion and genetic modification of human cord blood-derived progenitor/stem cells enhances vasculogenesis. Cell Transplantation, 18(3), 305–318.

    PubMed  Google Scholar 

  120. Lu, J., Aggarwal, R., Pompili, V. J., & Das, H. (2010). A novel technology for hematopoietic stem cell expansion using combination of nanofiber and growth factors. Recent Patents on Nanotechnology, 4(2), 125–135.

    PubMed  Google Scholar 

  121. Aggarwal, R., Pompili, V. J., & Das, H. (2010). Genetic modification of ex vivo expanded stem cells for clinical application. Frontiers in Bioscience, 15, 854–871.

    CAS  Google Scholar 

  122. Jackson, K. A., Majka, S. M., Wang, H., Pocius, J., Hartley, C. J., Majesky, M. W., et al. (2001). Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. Journal of Clinical Investigation, 107(11), 1395–1402.

    PubMed  CAS  Google Scholar 

  123. Rohde, D., Wickenhauser, C., Denecke, S., Stach, A., Lorenzen, J., Hansmann, M. L., et al. (1994). Cytokine release by human bone marrow cells: analysis at the single cell level. Virchows Archiv, 424(4), 389–395.

    PubMed  CAS  Google Scholar 

  124. Bikfalvi, A., & Han, Z. C. (1994). Angiogenic factors are hematopoietic growth factors and vice versa. Leukemia, 8(3), 523–529.

    PubMed  CAS  Google Scholar 

  125. Adams, R. H., & Alitalo, K. (2007). Molecular regulation of angiogenesis and lymphangiogenesis. Nature Reviews Molecular Cell Biology, 8(6), 464–478.

    PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported in part by National Institutes of Health grants, K01 AR054114 (NIAMS), SBIR R44 HL092706-01 (NHLBI), Third Frontier Projects, Ohio Technology BRCP Grant, and The Ohio State University start-up fund for stem cell research. The funders had no role in study design, data collection, and analysis, decision to publish, or preparation of the manuscript.

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  1. Cardiovascular Stem Cell Research Laboratory, The Dorothy M. Davis Heart and Lung Research Institute, The Ohio State University Medical Center, 460W, 12th Avenue, BRT 382, Columbus, OH, 43210, USA

    Jingwei Lu, Vincent J. Pompili & Hiranmoy Das

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  1. Jingwei Lu
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  2. Vincent J. Pompili
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  3. Hiranmoy Das
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Correspondence to Hiranmoy Das.

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Lu, J., Pompili, V.J. & Das, H. Neovascularization and Hematopoietic Stem Cells. Cell Biochem Biophys 67, 235–245 (2013). https://doi.org/10.1007/s12013-011-9298-x

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