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The Biology of Embryonic and Adult Endothelial Progenitor Cells

  • Chapter
Therapeutic Neovascularization–Quo Vadis?

Abstract

The growth of new blood vessels is a critical factor in many human diseases including cancer, ischemic injury and wound healing. De novo vessel formation or vasculogenesis was thought to take place solely in the embryo from mesodermal progenitor cells, whereas the vasculature in postnatal life was considered to undergo remodeling through expansion of pre-existing endothelial cells, or angiogenesis. Current evidence suggests that endothelial progenitor cells (EPCs) also exist in adult organisms as circulating cells originating in the bone marrow. They can be mobilized after vascular trauma, myocardial infarction, tissue injury, or during peripheral vascular disease, by a number of growth factors and chemokines like VEGF, GM-CSF, G-CSF and SDF-1. EPCs do not appear to represent a distinct or homogeneous cell population, but they are defined as cells that can give rise to endothelial progeny under certain circumstances in culture or in vivo. EPCs enhance tissue revascularization by contributing to new vessels and stimulating local angiogenesis, thus offering novel ways to regulate vascular growth. Results from the first clinical studies using mostly bone marrow stem cells as a source of EPCs have been encouraging, emphasizing the therapeutic potential of endothelial progenitor cells. This review summarizes the role of EPCs in the formation of new blood vessels and provides an outline of their biological characteristics and potential use in the clinical setting

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References

  1. Hatzopoulos, A.K. and Rosenberg, R.D. (1999) in Angiogenesis and Cardiovascular Disease (Ware, J.A. and Simons, M., Eds), Oxford University Press, Oxford, pp. 3–29

    Google Scholar 

  2. Risau, W. (1991) in The Development of the Vascular System (Feinberg, R.N.; Sherer, G.K. and Auerbach, R., Eds), Karger, Basel, pp. 56–68

    Google Scholar 

  3. Carmeliet, P. (2003) Nat. Med., 9(6), 653–660.

    Article  PubMed  CAS  Google Scholar 

  4. Caduff, J.H.; Fischer, L.C. and Burri, P.H. (1986) Anat. Rec., 216(2), 154–164.

    Article  PubMed  CAS  Google Scholar 

  5. Sabin, F.R. (1920) Contrib. Embryol. Carnegie Inst. Publ. Wash., 9, 213–262.

    Google Scholar 

  6. Drake, C.J. and Fleming, P.A. (2000) Blood, 95(5), 1671–1679.

    PubMed  CAS  Google Scholar 

  7. Murray, P.D.F. (1932) Proc. R. Soc. Lond. [Biol.], 11 497–521.

    Article  Google Scholar 

  8. Noden, D.M. (1989) Am. Rev. Respir. Dis., 140(4), 1097–1103.

    PubMed  CAS  Google Scholar 

  9. Jaffredo, T.; Gautier, R.; Eichmann, A. and Dieterlen-Lievre, F. (1998) Development, 125(22), 4575–4583.

    PubMed  CAS  Google Scholar 

  10. Park, C.; Ma, Y.D. and Choi, K. (2005) Exp. Hematol., 33(9), 965–970.

    Article  PubMed  CAS  Google Scholar 

  11. Pardanaud, L.; Luton, D.; Prigent, M.; Bourcheix, L.M.; Catala, M. and Dieterlen-Lievre, F. (1996) Development, 122(5), 1363–1371.

    PubMed  CAS  Google Scholar 

  12. Hatzopoulos, A.K.; Folkman, J.; Vasile, E.; Eiselen, G.K. and Rosenberg, R.D. (1998) Development, 125(8), 1457–1468.

    PubMed  CAS  Google Scholar 

  13. Furuta, C.; Ema, H.; Takayanagi, S.; Ogaeri, T.; Okamura, D.; Matsui, Y. and Nakauchi, H. (2006) Development, 133(14), 2771–2779.

    Article  PubMed  CAS  Google Scholar 

  14. Vogeli, K.M.; Jin, S.W.; Martin, G.R. and Stainier, D.Y. (2006) Nature, 443(7109), 337–339.

    Article  PubMed  CAS  Google Scholar 

  15. Wang, L. (2006) Trends. Cardiovasc. Med., 16(3), 89–94.

    Article  PubMed  CAS  Google Scholar 

  16. Huber, T.L.; Kouskoff, V.; Fehling, H.J.; Palis, J. and Keller, G. (2004) Nature, 432(7017), 625–630.

    Article  PubMed  CAS  Google Scholar 

  17. Houssaint, E. (1981) Cell. Differ., 10(5), 243–252.

    Article  PubMed  CAS  Google Scholar 

  18. Keller, G.; Lacaud, G. and Robertson, S. (1999) Exp. Hematol., 27(5), 777–787.

    Article  PubMed  CAS  Google Scholar 

  19. Folkman, J. (1995) Nat. Med., 1(1), 27–31.

    Article  PubMed  CAS  Google Scholar 

  20. Rafii, S. and Lyden, D. (2003) Nat. Med., 9(6), 702–712.

    Article  PubMed  CAS  Google Scholar 

  21. Urbich, C. and Dimmeler, S. (2004) Circ. Res., 95(4), 343–353.

    Article  PubMed  CAS  Google Scholar 

  22. Asahara, T.; Murohara, T.; Sullivan, A.; Silver, M.; van der Zee, R.; Li, T.; Witzenbichler, B.; Schatteman, G. and Isner, J.M. (1997) Science, 275(5302), 964–967.

    Article  PubMed  CAS  Google Scholar 

  23. Shi, Q.; Rafii, S.; Wu, M.H.; Wijelath, E.S.; Yu, C.; Ishida, A.; Fujita, Y.; Kothari, S.; Mohle, R.; Sauvage, L.R.; Moore, M.A.; Storb, R.F. and Hammond, W.P. (1998) Blood, 92(2), 362–367.

    PubMed  CAS  Google Scholar 

  24. Asahara, T.; Masuda, H.; Takahashi, T.; Kalka, C.; Pastore, C.; Silver, M.; Kearne, M.; Magner, M. and Isner, J.M. (1999) Circ. Res., 85(3), 221–228.

    PubMed  CAS  Google Scholar 

  25. Asahara, T.; Takahashi, T.; Masuda, H.; Kalka, C.; Chen, D.; Iwaguro, H.; Inai, Y.; Silver, M. and Isner, J.M. (1999) EMBO J., 18(14), 3964–3972.

    Article  PubMed  CAS  Google Scholar 

  26. Gehling, U.M.; Ergun, S.; Schumacher, U.; Wagener, C.; Pantel, K.; Otte, M.; Schuch, G.; Schafhausen, P.; Mende, T.; Kilic, N.; Kluge, K.; Schafer, B.; Hossfeld, D.K. and Fiedler, W. (2000) Blood, 95(10), 3106–3112.

    PubMed  CAS  Google Scholar 

  27. Lin, Y.; Weisdorf, D.J.; Solovey, A. and Hebbel, R.P. (2000) J. Clin. Invest., 105(1), 71–77.

    Article  PubMed  CAS  Google Scholar 

  28. Peichev, M.; Naiyer, A.J.; Pereira, D.; Zhu, Z.; Lane, W.J.; Williams, M.; Oz, M.C.; Hicklin, D.J.; Witte, L.; Moore, M.A. and Rafii, S. (2000) Blood, 95(3), 952–958.

    PubMed  CAS  Google Scholar 

  29. Quirici, N.; Soligo, D.; Caneva, L.; Servida, F.; Bossolasco, P. and Deliliers, G.L. (2001) Br. J. Haematol., 115(1), 186–194.

    Article  PubMed  CAS  Google Scholar 

  30. Orlic, D.; Kajstura, J.; Chimenti, S.; Jakoniuk, I.; Anderson, S.M.; Li, B.; Pickel, J.; McKay, R.; Nadal-Ginard, B.; Bodine, D.M.; Leri, A. and Anversa, P. (2001) Nature, 410(6829), 701–705.

    Article  PubMed  CAS  Google Scholar 

  31. Orlic, D.; Kajstura, J.; Chimenti, S.; Limana, F.; Jakoniuk, I.; Quaini, F.; Nadal-Ginard, B.; Bodine, D.M.; Leri, A. and Anversa, P. (2001) Proc. Natl. Acad. Sci. U S A, 98(18), 10344–10349.

    Article  PubMed  CAS  Google Scholar 

  32. Kocher, A.A.; Schuster, M.D.; Szabolcs, M.J.; Takuma, S.; Burkhoff, D.; Wang, J.; Homma, S.; Edwards, N.M. and Itescu, S. (2001) Nat. Med., 7(4), 430–436.

    Article  PubMed  CAS  Google Scholar 

  33. Kalka, C.; Masuda, H.; Takahashi, T.; Kalka-Moll, W.M.; Silver, M.; Kearney, M.; Li, T.; Isner, J.M. and Asahara, T. (2000) Proc. Natl. Acad. Sci. U S A, 97(7), 3422–3427.

    Article  PubMed  CAS  Google Scholar 

  34. Takahashi, T.; Kalka, C.; Masuda, H.; Chen, D.; Silver, M.; Kearney, M.; Magner, M.; Isner, J.M. and Asahara, T. (1999) Nat. Med., 5(4), 434–438.

    Article  PubMed  CAS  Google Scholar 

  35. Zhang, Z.G.; Zhang, L.; Jiang, Q. and Chopp, M. (2002) Circ. Res., 90(3), 284–288.

    Article  PubMed  CAS  Google Scholar 

  36. Davidoff, A.M.; Ng, C.Y.; Brown, P.; Leary, M.A.; Spurbeck, W.W.; Zhou, J.; Horwitz, E.; Vanin, E.F. and Nienhuis, A.W. (2001) Clin. Cancer. Res., 7(9), 2870–2879.

    PubMed  CAS  Google Scholar 

  37. Lyden, D.; Hattori, K.; Dias, S.; Costa, C.; Blaikie, P.; Butros, L.; Chadburn, A.; Heissig, B.; Marks, W.; Witte, L.; Wu, Y.; Hicklin, D.; Zhu, Z.; Hackett, N.R.; Crystal, R.G.; Moore, M.A.; Hajjar, K.A.; Manova, K.; Benezra, R. and Rafii, S. (2001) Nat. Med., 7(11), 1194–1201.

    Article  PubMed  CAS  Google Scholar 

  38. Young, P.P.; Hofling, A.A. and Sands, M.S. (2002) Proc. Natl. Acad. Sci. U S A, 99(18), 11951–11956.

    Article  PubMed  CAS  Google Scholar 

  39. Kupatt, C.; Hinkel, R.; Lamparter, M.; von Bruhl, M.L.; Pohl, T.; Horstkotte, J.; Beck, H.; Muller, S.; Delker, S.; Gildehaus, F.J.; Buning, H.; Hatzopoulos, A.K. and Boekstegers, P. (2005) Circulation, 112(9 Suppl), I117–122.

    PubMed  Google Scholar 

  40. Kupatt, C.; Horstkotte, J.; Vlastos, G.A.; Pfosser, A.; Lebherz, C.; Semisch, M.; Thalgott, M.; Buttner, K.; Browarzyk, C.; Mages, J.; Hoffmann, R.; Deten, A.; Lamparter, M.; Muller, F.; Beck, H.; Buning, H.; Boekstegers, P. and Hatzopoulos, A.K. (2005) FASEB J., 19(11), 1576–1578.

    PubMed  CAS  Google Scholar 

  41. Yin, A.H.; Miraglia, S.; Zanjani, E.D.; Almeida-Porada, G.; Ogawa, M.; Leary, A.G.; Olweus, J.; Kearney, J. and Buck, D.W. (1997) Blood, 90(12), 5002–5012.

    PubMed  CAS  Google Scholar 

  42. Miraglia, S.; Godfrey, W.; Yin, A.H.; Atkins, K.; Warnke, R.; Holden, J.T.; Bray, R.A.; Waller, E.K. and Buck, D.W. (1997) Blood, 90(12), 5013–5021.

    PubMed  CAS  Google Scholar 

  43. Voyta, J.C.; Via, D.P.; Butterfield, C.E. and Zetter, B.R. (1984) J. Cell. Biol., 99(6), 2034–2040.

    Article  PubMed  CAS  Google Scholar 

  44. Hristov, M.; Erl, W. and Weber, P.C. (2003) Trends Cardiovasc. Med., 13(5), 201–206.

    Article  PubMed  CAS  Google Scholar 

  45. Gulati, R.; Jevremovic, D.; Peterson, T.E.; Chatterjee, S.; Shah, V.; Vile, R.G. and Simari, R.D. (2003) Circ. Res., 93(11), 1023–1025.

    Article  PubMed  CAS  Google Scholar 

  46. Rehman, J.; Li, J.; Orschell, C.M. and March, K.L. (2003) Circulation, 107(8), 1164–1169.

    Article  PubMed  Google Scholar 

  47. Fujiyama, S.; Amano, K.; Uehira, K.; Yoshida, M.; Nishiwaki, Y.; Nozawa, Y.; Jin, D.; Takai, S.; Miyazaki, M.; Egashira, K.; Imada, T.; Iwasaka, T. and Matsubara, H. (2003) Circ. Res., 93(10), 980–989.

    Article  PubMed  CAS  Google Scholar 

  48. Yang, L.; DeBusk, L.M.; Fukuda, K.; Fingleton, B.; Green-Jarvis, B.; Shyr, Y.; Matrisian, L.M.; Carbone, D.P. and Lin, P.C. (2004) Cancer Cell, 6(4), 409–421.

    Article  PubMed  CAS  Google Scholar 

  49. Ingram, D.A.; Caplice, N.M. and Yoder, M.C. (2005) Blood, 106(5), 1525–1531.

    Article  PubMed  CAS  Google Scholar 

  50. Eggermann, J.; Kliche, S.; Jarmy, G.; Hoffmann, K.; Mayr-Beyrle, U.; Debatin, K.M.; Waltenberger, J. and Beltinger, C. (2003) Cardiovasc. Res., 58(2), 478–486.

    Article  PubMed  CAS  Google Scholar 

  51. Murga, M.; Yao, L. and Tosato, G. (2004) Stem Cells, 22(3), 385–395.

    Article  PubMed  CAS  Google Scholar 

  52. Yoo, E.S.; Lee, K.E.; Seo, J.W.; Yoo, E.H.; Lee, M.A.; Im, S.A.; Mun, Y.C.; Lee, S.N.; Huh, J.W.; Kim, M.J.; Jo, D.Y.; Ahn, J.Y.; Lee, S.M.; Chung, W.S.; Kim, J.H. and Seong, C.M. (2003) Stem Cells, 21(2), 228–235.

    Article  PubMed  CAS  Google Scholar 

  53. Bompais, H.; Chagraoui, J.; Canron, X.; Crisan, M.; Liu, X.H.; Anjo, A.; Tolla-Le Port, C.; Leboeuf, M.; Charbord, P.; Bikfalvi, A. and Uzan, G. (2004) Blood, 103(7), 2577–2584.

    Article  PubMed  CAS  Google Scholar 

  54. Yoon, C.H.; Hur, J.; Park, K.W.; Kim, J.H.; Lee, C.S.; Oh, I.Y.; Kim, T.Y.; Cho, H.J.; Kang, H.J.; Chae, I.H.; Yang, H.K.; Oh, B.H.; Park, Y.B. and Kim, H.S. (2005) Circulation, 112(11), 1618–1627.

    Article  PubMed  Google Scholar 

  55. Reyes, M.; Lund, T.; Lenvik, T.; Aguiar, D.; Koodie, L. and Verfaillie, C.M. (2001) Blood, 98(9), 2615–2625.

    Article  PubMed  CAS  Google Scholar 

  56. Reyes, M. and Verfaillie, C.M. (2001) Ann. N. Y. Acad. Sci., 938(231–233; discussion 233–235.

    Google Scholar 

  57. Niwa, H.; Miyazaki, J. and Smith, A.G. (2000) Nat. Genet., 24(4), 372–376.

    Article  PubMed  CAS  Google Scholar 

  58. Verfaillie, C.M. (2005) Novartis Found. Symp., 265, 55–61; discussion 61–65, 92–97.

    Google Scholar 

  59. Hladovec, J. (1978) Physiol. Bohemoslov., 27(2), 140–144.

    PubMed  CAS  Google Scholar 

  60. Dignat-George, F. and Sampol, J. (2000) Eur. J. Haematol., 65(4), 215–220.

    Article  PubMed  CAS  Google Scholar 

  61. Shaked, Y.; Bertolini, F.; Man, S.; Rogers, M.S.; Cervi, D.; Foutz, T.; Rawn, K.; Voskas, D.; Dumont, D.J.; Ben-David, Y.; Lawler, J.; Henkin, J.; Huber, J.; Hicklin, D.J.; D’Amato, R.J. and Kerbel, R.S. (2005) Cancer Cell, 7(1), 101–111.

    PubMed  CAS  Google Scholar 

  62. Vajkoczy, P.; Blum, S.; Lamparter, M.; Mailhammer, R.; Erber, R.; Engelhardt, B.; Vestweber, D. and Hatzopoulos, A.K. (2003) J. Exp. Med., 197(12), 1755–1765.

    Article  PubMed  CAS  Google Scholar 

  63. Pardanaud, L. and Eichmann, A. (2006) Development, 133(13), 2527–2537.

    Article  PubMed  CAS  Google Scholar 

  64. Crosby, J.R.; Kaminski, W.E.; Schatteman, G.; Martin, P.J.; Raines, E.W.; Seifert, R.A. and Bowen-Pope, D.F. (2000) Circ. Res., 87(9), 728–730.

    PubMed  CAS  Google Scholar 

  65. Montesinos, M.C.; Shaw, J.P.; Yee, H.; Shamamian, P. and Cronstein, B.N. (2004) Am. J. Pathol., 164(6), 1887–1892.

    PubMed  CAS  Google Scholar 

  66. Galiano, R.D.; Tepper, O.M.; Pelo, C.R.; Bhatt, K.A.; Callaghan, M.; Bastidas, N.; Bunting, S.; Steinmetz, H.G. and Gurtner, G.C. (2004) Am. J. Pathol., 164(6), 1935–1947.

    PubMed  CAS  Google Scholar 

  67. Yung, Y.C.; Cheshier, S.; Santarelli, J.G.; Huang, Z.; Wagers, A.; Weissman, I. and Tse, V. (2004) Microcirculation, 11(8), 699–708.

    Article  PubMed  CAS  Google Scholar 

  68. Li, B.; Sharpe, E.E.; Maupin, A.B.; Teleron, A.A.; Pyle, A.L.; Carmeliet, P. and Young, P.P. (2006) FASEB J., 20(9), 1495–1497.

    Article  PubMed  CAS  Google Scholar 

  69. Kalka, C.; Tehrani, H.; Laudenberg, B.; Vale, P.R.; Isner, J.M.; Asahara, T. and Symes, J.F. (2000) Ann. Thorac. Surg., 70(3), 829–834.

    Article  PubMed  CAS  Google Scholar 

  70. Yamaguchi, J.; Kusano, K.F.; Masuo, O.; Kawamoto, A.; Silver, M.; Murasawa, S.; Bosch-Marce, M.; Masuda, H.; Losordo, D.W.; Isner, J.M. and Asahara, T. (2003) Circulation, 107(9), 1322–1328.

    Article  PubMed  CAS  Google Scholar 

  71. Askari, A.T.; Unzek, S.; Popovic, Z.B.; Goldman, C.K.; Forudi, F.; Kiedrowski, M.; Rovner, A.; Ellis, S.G.; Thomas, J.D.; DiCorleto, P.E.; Topol, E.J. and Penn, M.S. (2003) Lancet, 362(9385), 697–703.

    Article  PubMed  CAS  Google Scholar 

  72. Aiuti, A.; Webb, I.J.; Bleul, C.; Springer, T. and Gutierrez-Ramos, J.C. (1997) J. Exp. Med., 185(1), 111–120.

    Article  PubMed  CAS  Google Scholar 

  73. Hill, W.D.; Hess, D.C.; Martin-Studdard, A.; Carothers, J.J.; Zheng, J.; Hale, D.; Maeda, M.; Fagan, S.C.; Carroll, J.E. and Conway, S.J. (2004) J. Neuropathol. Exp. Neurol., 63(1), 84–96.

    PubMed  CAS  Google Scholar 

  74. Llevadot, J.; Murasawa, S.; Kureishi, Y.; Uchida, S.; Masuda, H.; Kawamoto, A.; Walsh, K.; Isner, J.M. and Asahara, T. (2001) J. Clin. Invest., 108(3), 399–405.

    Article  PubMed  CAS  Google Scholar 

  75. Vasa, M.; Fichtlscherer, S.; Adler, K.; Aicher, A.; Martin, H.; Zeiher, A.M. and Dimmeler, S. (2001) Circulation, 103(24), 2885–2890.

    PubMed  CAS  Google Scholar 

  76. Dimmeler, S.; Aicher, A.; Vasa, M.; Mildner-Rihm, C.; Adler, K.; Tiemann, M.; Rutten, H.; Fichtlscherer, S.; Martin, H. and Zeiher, A.M. (2001) J. Clin. Invest., 108(3), 391–397.

    Article  PubMed  CAS  Google Scholar 

  77. Iwakura, A.; Luedemann, C.; Shastry, S.; Hanley, A.; Kearney, M.; Aikawa, R.; Isner, J.M.; Asahara, T. and Losordo, D.W. (2003) Circulation, 108(25), 3115–3121.

    Article  PubMed  CAS  Google Scholar 

  78. Yoon, C.H.; Hur, J.; Oh, I.Y.; Park, K.W.; Kim, T.Y.; Shin, J.H.; Kim, J.H.; Lee, C.S.; Chung, J.K.; Park, Y.B. and Kim, H.S. (2006) Arterioscler. Thromb. Vasc. Biol., 26(5), 1066–1072.

    Article  PubMed  CAS  Google Scholar 

  79. Wu, Y.; Ip, J.E.; Huang, J.; Zhang, L.; Matsushita, K.; Liew, C.C.; Pratt, R.E. and Dzau, V.J. (2006) Circ. Res., 99(3), 315–322.

    Article  PubMed  CAS  Google Scholar 

  80. Massberg, S.; Konrad, I.; Schurzinger, K.; Lorenz, M.; Schneider, S.; Zohlnhoefer, D.; Hoppe, K.; Schiemann, M.; Kennerknecht, E.; Sauer, S.; Schulz, C.; Kerstan, S.; Rudelius, M.; Seidl, S.; Sorge, F.; Langer, H.; Peluso, M.; Goyal, P.; Vestweber, D.; Emambokus, N.R.; Busch, D.H.; Frampton, J. and Gawaz, M. (2006) J. Exp. Med., 203(5), 1221–1233.

    Article  PubMed  CAS  Google Scholar 

  81. Daub, K.; Langer, H.; Seizer, P.; Stellos, K.; May, A.E.; Goyal, P.; Bigalke, B.; Schonberger, T.; Geisler, T.; Siegel-Axel, D.; Oostendorp, R.A.; Lindemann, S. and Gawaz, M. (2006) FASEB J., in press.

    Google Scholar 

  82. Langer, H.; May, A.E.; Daub, K.; Heinzmann, U.; Lang, P.; Schumm, M.; Vestweber, D.; Massberg, S.; Schonberger, T.; Pfisterer, I.; Hatzopoulos, A.K. and Gawaz, M. (2006) Circ. Res., 98(2), e2–10.

    Article  PubMed  CAS  Google Scholar 

  83. de Boer, H.C.; Verseyden, C.; Ulfman, L.H.; Zwaginga, J.J.; Bot, I.; Biessen, E.A.; Rabelink, T.J. and van Zonneveld, A.J. (2006) Arterioscler. Thromb. Vasc. Biol., 26(7), 1653–1659.

    Article  PubMed  CAS  Google Scholar 

  84. Dimmeler, S.; Zeiher, A.M. and Schneider, M.D. (2005) J. Clin. Invest., 115(3), 572–583.

    Article  PubMed  CAS  Google Scholar 

  85. Assmus, B.; Schachinger, V.; Teupe, C.; Britten, M.; Lehmann, R.; Dobert, N.; Grunwald, F.; Aicher, A.; Urbich, C.; Martin, H.; Hoelzer, D.; Dimmeler, S. and Zeiher, A.M. (2002) Circulation, 106(24), 3009–3017.

    Article  PubMed  Google Scholar 

  86. Strauer, B.E.; Brehm, M.; Zeus, T.; Kostering, M.; Hernandez, A.; Sorg, R.V.; Kogler, G. and Wernet, P. (2002) Circulation, 106(15), 1913–1918.

    Article  PubMed  Google Scholar 

  87. Schachinger, V.; Assmus, B.; Britten, M.B.; Honold, J.; Lehmann, R.; Teupe, C.; Abolmaali, N.D.; Vogl, T.J.; Hofmann, W.K.; Martin, H.; Dimmeler, S. and Zeiher, A.M. (2004) J. Am. Coll. Cardiol., 44(8), 1690–1699.

    Article  PubMed  Google Scholar 

  88. Britten, M.B.; Abolmaali, N.D.; Assmus, B.; Lehmann, R.; Honold, J.; Schmitt, J.; Vogl, T.J.; Martin, H.; Schachinger, V.; Dimmeler, S. and Zeiher, A.M. (2003) Circulation, 108(18), 2212–2218.

    Article  PubMed  CAS  Google Scholar 

  89. Fernandez-Aviles, F.; San Roman, J.A.; Garcia-Frade, J.; Fernandez, M.E.; Penarrubia, M.J.; de la Fuente, L.; Gomez-Bueno, M.; Cantalapiedra, A.; Fernandez, J.; Gutierrez, O.; Sanchez, P.L.; Hernandez, C.; Sanz, R.; Garcia-Sancho, J. and Sanchez, A. (2004) Circ. Res., 95(7), 742–748.

    Article  PubMed  CAS  Google Scholar 

  90. Wollert, K.C.; Meyer, G.P.; Lotz, J.; Ringes-Lichtenberg, S.; Lippolt, P.; Breidenbach, C.; Fichtner, S.; Korte, T.; Hornig, B.; Messinger, D.; Arseniev, L.; Hertenstein, B.; Ganser, A. and Drexler, H. (2004) Lancet, 364(9429), 141–148.

    Article  PubMed  Google Scholar 

  91. Assmus, B.; Honold, J.; Schachinger, V.; Britten, M.B.; Fischer-Rasokat, U.; Lehmann, R.; Teupe, C.; Pistorius, K.; Martin, H.; Abolmaali, N.D.; Tonn, T.; Dimmeler, S. and Zeiher, A.M. (2006) N. Engl. J. Med., 355(12), 1222–1232.

    Article  PubMed  CAS  Google Scholar 

  92. Janssens, S.; Dubois, C.; Bogaert, J.; Theunissen, K.; Deroose, C.; Desmet, W.; Kalantzi, M.; Herbots, L.; Sinnaeve, P.; Dens, J.; Maertens, J.; Rademakers, F.; Dymarkowski, S.; Gheysens, O.; Van Cleemput, J.; Bormans, G.; Nuyts, J.; Belmans, A.; Mortelmans, L.; Boogaerts, M. and Van de Werf, F. (2006) Lancet, 367(9505), 113–121.

    Article  PubMed  Google Scholar 

  93. Lunde, K.; Solheim, S.; Aakhus, S.; Arnesen, H.; Abdelnoor, M.; Egeland, T.; Endresen, K.; Ilebekk, A.; Mangschau, A.; Fjeld, J.G.; Smith, H.J.; Taraldsrud, E.; Grogaard, H.K.; Bjornerheim, R.; Brekke, M.; Muller, C.; Hopp, E.; Ragnarsson, A.; Brinchmann, J.E. and Forfang, K. (2006) N. Engl. J. Med., 355(12), 1199–1209.

    Article  PubMed  CAS  Google Scholar 

  94. Hamano, K.; Nishida, M.; Hirata, K.; Mikamo, A.; Li, T.S.; Harada, M.; Miura, T.; Matsuzaki, M. and Esato, K. (2001) Jpn. Circ. J., 65(9), 845–847.

    Article  PubMed  CAS  Google Scholar 

  95. Tse, H.F.; Kwong, Y.L.; Chan, J.K.; Lo, G.; Ho, C.L. and Lau, C.P. (2003) Lancet, 361(9351), 47–49.

    Article  PubMed  Google Scholar 

  96. Perin, E.C.; Dohmann, H.F.; Borojevic, R.; Silva, S.A.; Sousa, A.L.; Mesquita, C.T.; Rossi, M.I.; Carvalho, A.C.; Dutra, H.S.; Dohmann, H.J.; Silva, G.V.; Belem, L.; Vivacqua, R.; Rangel, F.O.; Esporcatte, R.; Geng, Y.J.; Vaughn, W.K.; Assad, J.A.; Mesquita, E.T. and Willerson, J.T. (2003) Circulation, 107(18), 2294–2302.

    Article  PubMed  Google Scholar 

  97. Perin, E.C.; Dohmann, H.F.; Borojevic, R.; Silva, S.A.; Sousa, A.L.; Silva, G.V.; Mesquita, C.T.; Belem, L.; Vaughn, W.K.; Rangel, F.O.; Assad, J.A.; Carvalho, A.C.; Branco, R.V.; Rossi, M.I.; Dohmann, H.J. and Willerson, J.T. (2004) Circulation, 110(11 Suppl 1), II213–218.

    PubMed  Google Scholar 

  98. Fuchs, S.; Satler, L.F.; Kornowski, R.; Okubagzi, P.; Weisz, G.; Baffour, R.; Waksman, R.; Weissman, N.J.; Cerqueira, M.; Leon, M.B. and Epstein, S.E. (2003) J. Am. Coll. Cardiol., 41(10), 1721–1724.

    Article  PubMed  Google Scholar 

  99. Galinanes, M.; Loubani, M.; Davies, J.; Chin, D.; Pasi, J. and Bell, P.R. (2004) Cell Transplant, 13(1), 7–13.

    PubMed  Google Scholar 

  100. Stamm, C.; Westphal, B.; Kleine, H.D.; Petzsch, M.; Kittner, C.; Klinge, H.; Schumichen, C.; Nienaber, C.A.; Freund, M. and Steinhoff, G. (2003) Lancet, 361(9351), 45–46.

    Article  PubMed  Google Scholar 

  101. Stamm, C.; Kleine, H.D.; Westphal, B.; Petzsch, M.; Kittner, C.; Nienaber, C.A.; Freund, M. and Steinhoff, G. (2004) Thorac. Cardiovasc. Surg., 52(3), 152–158.

    Article  PubMed  CAS  Google Scholar 

  102. Pompilio, G.; Cannata, A.; Peccatori, F.; Bertolini, F.; Nascimbene, A.; Capogrossi, M.C. and Biglioli, P. (2004) Ann. Thorac. Surg., 78(5), 1808–1812.

    Article  PubMed  Google Scholar 

  103. Nagamine, H.; Watanabe, G.; Shiobara, S.; Takemura, H.; Arai, S. and Tomita, S. (2004) Heart Surg. Forum, 7(4), E285–287.

    Article  PubMed  Google Scholar 

  104. Ozbaran, M.; Omay, S.B.; Nalbantgil, S.; Kultursay, H.; Kumanlioglu, K.; Nart, D. and Pektok, E. (2004) Eur. J. Cardiothorac. Surg., 25(3), 342–350; discussion 350–341.

    Google Scholar 

  105. Kang, H.J.; Kim, H.S.; Zhang, S.Y.; Park, K.W.; Cho, H.J.; Koo, B.K.; Kim, Y.J.; Soo Lee, D.; Sohn, D.W.; Han, K.S.; Oh, B.H.; Lee, M.M. and Park, Y.B. (2004) Lancet, 363(9411), 751–756.

    Article  PubMed  CAS  Google Scholar 

  106. Ince, H.; Petzsch, M.; Kleine, H.D.; Eckard, H.; Rehders, T.; Burska, D.; Kische, S.; Freund, M. and Nienaber, C.A. (2005) Circulation, 112(9 Suppl), I73–80.

    PubMed  Google Scholar 

  107. Engelmann, M.G.; Theiss, H.D.; Hennig-Theiss, C.; Huber, A.; Wintersperger, B.J.; Werle-Ruedinger, A.E.; Schoenberg, S.O.; Steinbeck, G. and Franz, W.M. (2006) J. Am. Coll. Cardiol., 48(8), 1712–1721.

    Article  PubMed  CAS  Google Scholar 

  108. Hill, J.M.; Zalos, G.; Halcox, J.P.; Schenke, W.H.; Waclawiw, M.A.; Quyyumi, A.A. and Finkel, T. (2003) N. Engl. J. Med., 348(7), 593–600.

    Article  PubMed  Google Scholar 

  109. Vasa, M.; Fichtlscherer, S.; Aicher, A.; Adler, K.; Urbich, C.; Martin, H.; Zeiher, A.M. and Dimmeler, S. (2001) Circ. Res., 89(1), E1–7.

    PubMed  CAS  Google Scholar 

  110. Werner, N.; Kosiol, S.; Schiegl, T.; Ahlers, P.; Walenta, K.; Link, A.; Bohm, M. and Nickenig, G. (2005) N. Engl. J. Med., 353(10), 999–1007.

    Article  PubMed  CAS  Google Scholar 

  111. Kunz, G.A.; Liang, G.; Cuculoski, F.; Gregg, D.; Vata, K.C.; Shaw, L.K.; Goldschmidt-Clermont, P.J.; Dong, C.; Taylor, D.A. and Peterson, E.D. (2006) Am. Heart. J., 152(1), 190–195.

    Article  PubMed  Google Scholar 

  112. Heeschen, C.; Lehmann R.; Honold J.; Assmus B.; Aicher A.; Walter D.H.; Martin H.; Zeiher A.M. and Dimmeler S. (2004) Circulation, 109(13), 1615–1622.

    Article  PubMed  Google Scholar 

  113. Ghani, U.; Shuaib, A.; Salam, A.; Nasir, A.; Shuaib, U.; Jeerakathil, T.; Sher, F.; O’Rourke, F.; Nasser, A.M.; Schwindt, B. and Todd, K. (2005) Stroke, 36(1), 151–153.

    Article  PubMed  Google Scholar 

  114. Takahashi, M.; Nakamura, T.; Toba, T.; Kajiwara, N.; Kato, H. and Shimizu, Y. (2004) Tissue Eng., 10(5–6), 771–779.

    Article  PubMed  Google Scholar 

  115. Loomans, C.J.; de Koning, E.J.; Staal, F.J.; Rookmaaker, M.B.; Verseyden, C.; de Boer, H.C.; Verhaar, M.C.; Braam, B.; Rabelink, T.J. and van Zonneveld, A.J. (2004) Diabetes, 53(1), 195–199.

    Article  PubMed  CAS  Google Scholar 

  116. Tepper, O.M.; Galiano, R.D.; Capla, J.M.; Kalka, C.; Gagne, P.J.; Jacobowitz, G.R.; Levine, J.P. and Gurtner, G.C. (2002) Circulation, 106(22), 2781–2786.

    Article  PubMed  Google Scholar 

  117. Choi, J.H.; Kim, K.L.; Huh, W.; Kim, B.; Byun, J.; Suh, W.; Sung, J.; Jeon, E.S.; Oh, H.Y. and Kim, D.K. (2004) Arterioscler. Thromb. Vasc. Biol., 24(7), 1246–1252.

    Article  PubMed  CAS  Google Scholar 

  118. Thijssen, D.H.; Vos, J.B.; Verseyden, C.; van Zonneveld, A.J.; Smits, P.; Sweep, F.C.; Hopman, M.T. and de Boer, H.C. (2006) Aging Cell, in press.

    Google Scholar 

  119. Shimada, T.; Takeshita, Y.; Murohara, T.; Sasaki, K.; Egami, K.; Shintani, S.; Katsuda, Y.; Ikeda, H.; Nabeshima, Y. and Imaizumi, T. (2004) Circulation, 110(9), 1148–1155.

    Article  PubMed  Google Scholar 

  120. Edelberg, J.M.; Tang, L.; Hattori, K.; Lyden, D. and Rafii, S. (2002) Circ. Res., 90(10), E89–93.

    Article  CAS  Google Scholar 

  121. Zhu, B.Q.; Heeschen, C.; Sievers, R.E.; Karliner, J.S.; Parmley, W.W.; Glantz, S.A. and Cooke, J.P. (2003) Cancer Cell, 4(3), 191–196.

    Article  PubMed  CAS  Google Scholar 

  122. Kondo, T.; Hayashi, M.; Takeshita, K.; Numaguchi, Y.; Kobayashi, K.; Iino, S.; Inden, Y. and Murohara, T. (2004) Arterioscler. Thromb. Vasc. Biol., 24(8), 1442–1447.

    Article  PubMed  CAS  Google Scholar 

  123. Wang, X.; Zhu, J.; Chen, J. and Shang, Y. (2004) J. Clin. Pharmacol., 44(8), 881–889.

    Article  PubMed  CAS  Google Scholar 

  124. Rehman, J.; Li, J.; Parvathaneni, L.; Karlsson, G.; Panchal, V.R.; Temm, C.J.; Mahenthiran, J. and March, K.L. (2004) J. Am. Coll. Cardiol., 43(12), 2314–2318.

    Article  PubMed  Google Scholar 

  125. Laufs, U.; Werner, N.; Link, A.; Endres, M.; Wassmann, S.; Jurgens, K.; Miche, E.; Bohm, M. and Nickenig, G. (2004) Circulation, 109(2), 220–226.

    Article  PubMed  CAS  Google Scholar 

  126. Conway, E.M.; Collen, D. and Carmeliet, P. (2001) Cardiovasc. Res., 49(3), 507–521.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Medicine and Department of Cell & Developmental Biology, Division of Cardiovascular Medicine, Vanderbilt University Medical Center, Nashville, TN, 37232, USA

    Mathias Lamparter & Antonis K. Hatzopoulos

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  1. Mathias Lamparter
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  1. Institute for Surgical Research, Munich, Germany

    Elisabeth Deindl

  2. Klinikum Grosshadern, Munich, Germany

    Christian Kupatt

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Lamparter, M., Hatzopoulos, A.K. (2007). The Biology of Embryonic and Adult Endothelial Progenitor Cells. In: Deindl, E., Kupatt, C. (eds) Therapeutic Neovascularization–Quo Vadis?. Springer, Dordrecht. https://doi.org/10.1007/1-4020-5955-8_11

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