Human Atherosclerosis: New Participants?

  • Yu. A. Romanov
  • E. L. Soboleva
  • V. N. Smirnov
  • A. Bobik
Part of the Progress in Experimental Cardiology book series (PREC, volume 9)

Summary

Human atherosclerosis is multi-factorial disease involving several physiological and pathological mechanisms related to remodeling of vascular wall in response to various inflammatory, immune-autoimmune, hormonal, and other disturbances. In spite of such causal complexity, the list of cellular participants is limited to a few vascular and blood-borne cells. Here we demonstrate that human atherosclerosis, although chronic disease, causes same central response as does acute tissue injury, i.e. mobilization of bone marrow stem/progenitor cells into peripheral blood, gradual stem cell accumulation in the injury site followed by tissue remodeling. Driven by chemical signaling from inflammatory foci on vasculature lining, colony-forming units (CFUs) for hemopoietic lineages and pluripotent mesenchymal cells leave bone marrow and start to circulate in blood. A percentage of hemopoietic CFUs as well as of stromal CFUs become resident in aortic intima forming loci of ectopic hemopoiesis. On the other hand, stromal differentiation in vascular intima initiated by putative risk factors (including high LDL) results in fibrosis, formation of osteoid and chondroid matrices, calcification and appearance of osteoclasts and adipocytes. It is this sequence of events rather than migration and proliferation of smooth muscle cells form cellular basis of human atherosclerosis. From this point of view, human atherosclerosis is just natural cell therapy of vascular wall exerted via basic mechanism for tissue regeneration, i.e. mobilization of bone marrow stem/progenitor cells and their transport to injury location. Vascular stenosis is viewed as undesirable and unpredictable consequence of physiological cell therapy of vascular inflammation. The type of a particular plaque (fibrotic, ossified, adipocyte-rich, etc.) is determined by microenvironment where clonogenic bone marrow stem cell comes to.

Key words

atherosclerosis bone marrow endothelium colony-forming units mesenchymal stem cells extracellular matrix hypercholesterolemia 

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References

  1. 1.
    Wick J, Perschinka H, Millonig G. 2001. Atherosclerosis as an autoimmune disease: an update. Trends Immunol, 22:665–669.PubMedCrossRefGoogle Scholar
  2. 2.
    Najemnick C, Sinzinger H, Kritz H. 1999. Endothelial dysfunction, atherosclerosis and diabetes. Acta Med Austriaca, 26:148–153.Google Scholar
  3. 3.
    Landmesser U, Hornig B, Drexler H. 2000. Endothelial dysfunction in hypercholesterolemia: mechanisms, pathophysiological importance, and therapeutic interventions. Semin Thromb Hemost, 26:529–537.PubMedCrossRefGoogle Scholar
  4. 4.
    Benitez RM. 1999. Atherosclerosis: an infectious disease? Hosp Pract, 34:79–82, 85–86.CrossRefGoogle Scholar
  5. 5.
    LaRosa JC. 1998. Atherogenesis and its relationship to coronary risk factors. Clin Cornerstone, 1:3–14.PubMedCrossRefGoogle Scholar
  6. 6.
    Gimbrone MA Jr. 1999. Endothelial dysfunction, hemodynamic forces, and atherosclerosis. Thromb Haemostas, 82:722–726.Google Scholar
  7. 7.
    Libbi P, Hansson GK. 1991. Involvement of immune system in human atherogenesis: current knowledge and unanswered questions. Lab Invest, 64:5–15.Google Scholar
  8. 8.
    Rokitansky K. 1855. The organs of circulation. In: A manual of pathological anatomy, Blanchard & Lea, Philadelphia, pp. 201–208.Google Scholar
  9. 9.
    Virchow R. 1858. Cellular pathology, John Churchill, London.Google Scholar
  10. 10.
    Anitschkov N. 1913. Uber die veranderungen der kaninchenaorta bei experimenteller cholesterinsteatose. Beitr Pathol Anat Allgem Pathol, 56:379–405.Google Scholar
  11. 11.
    Ross R, Glomset JA. 1976. The pathogenesis of atherosclerosis. N Engl J Med, 295:469–377.Google Scholar
  12. 12.
    Ross R. 1986. The pathogenesis of atherosclerosis: an update. N Engl J Med, 314:488–500.PubMedCrossRefGoogle Scholar
  13. 13.
    Schwenke DC, Carew TE. 1989. Initiation of atherosclerotic lesions in cholesterol-fed rabbits: I. Focal increases in arterial LDL precede development of fatty streak lesion. Arteriosclerosis, 9:895–907.PubMedCrossRefGoogle Scholar
  14. 14.
    Witztum JL. 1990. The role of monocytes and oxidized LDL in atherosclerosis. Atherosclerosis Reviews, 21:59–69.Google Scholar
  15. 15.
    Simionescu N, Simionescu M. 1993. Proatherosclerotic events: pathobiochemical changes occurring in the arterial wall before monocyte migration. FASEB J, 7:1359–1366.PubMedGoogle Scholar
  16. 16.
    Ross R. 1992. Endothelial dysfunction and atherosclerosis. In: Endothelial cell dysfunction (Simionescu N, Simionescu M, Eds.), Plenum Press, NY, pp. 295–307.Google Scholar
  17. 17.
    Gimbrone MA Jr, Topper JN, Nagel T, Anderson KR, Garcia-Cardena G. 2000. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann NY Acad Sci, 902:230–240.PubMedCrossRefGoogle Scholar
  18. 18.
    Toborek M, Kaiser S. 1999. Endothelial cell functions. Relation to atherogenesis. Basic Res Cardiol, 94:295–314.PubMedCrossRefGoogle Scholar
  19. 19.
    Shimokawa H. 1999. Primary endothelial dysfunction: Atherosclerosis. J Mol Cell Cardiol, 31:23–37.PubMedCrossRefGoogle Scholar
  20. 20.
    Lum H, Malik AB. 1994. Regulation of vascular endothelial barrier function. Amer J Physiol, 267:L223–L241.PubMedGoogle Scholar
  21. 21.
    Vanhoutte PM, Mombouli JV. 1996. Vascular endothelium: vasoactive mediators. Progr Cardiovasc Dis, 39:229–238.CrossRefGoogle Scholar
  22. 22.
    Mann KG. 1997. Thrombosis: theoretical considerations. Amer J Clin Nutr, 65 (suppl. 5): 1657S–1664S.PubMedGoogle Scholar
  23. 23.
    Hill GE, Whitten CW. 1997. The role of the vascular endothelium in inflammatory syndromes, atherogenesis, and the propagation of disease. J Cardiothorac Vase Anesth, 11:316–321.CrossRefGoogle Scholar
  24. 24.
    Gown AM, Tsukada T, Ross R. 1986. Human atherosclerosis. II. Immunocytochemical analysis of the cellular composition of human atherosclerotic lesions. Amer J Pathol, 125:191–207.Google Scholar
  25. 25.
    Plutzky J. 2001. Inflammatory pathways in atherosclerosis and acute coronary syndromes. Amer J Cardiol, 88:10K–15K.PubMedCrossRefGoogle Scholar
  26. 26.
    Koenig W. 2001. Inflammation and coronary heart disease: an overview. Cardiol Rev, 9:31–35.PubMedCrossRefGoogle Scholar
  27. 27.
    Ross R. 1999. Atherosclerosis: an inflammatory disease. N Engl J Med, 340:115–126.PubMedCrossRefGoogle Scholar
  28. 28.
    Robbie L, Libb YP. 2001. Inflammation and atherothrombosis. Ann NY Acad Sci, 947:167–180.PubMedCrossRefGoogle Scholar
  29. 29.
    Faggiotto A, Ross R, Harker L. 1984. Studies of hypercholesterolemia in the nonhuman primate. I. Changes that lead to fatty streak formation. Arteriosclerosis, 4:323–340.PubMedCrossRefGoogle Scholar
  30. 30.
    Munro JM, Cotran RS. 1988. The pathogenesis of atherosclerosis: Atherogenesis and inflammation. Lab Invest, 58:249–261.PubMedGoogle Scholar
  31. 31.
    Cassatella MA. 1995. The production of cytokines by polymorphonuclear neutrophyls. Immunol Today, 16:21–33.PubMedCrossRefGoogle Scholar
  32. 32.
    Zimmerman GA, Prescott SM, McIntyre TM. 1992. Endothelial cell interaction with granulocytes: tethering and signaling molecules. Immunol Today, 13:93–100.PubMedCrossRefGoogle Scholar
  33. 33.
    Lorant DE, Patel KD, McIntyre TM, McEver RP, Prescott SM, Zimmerman GA. 1991. Coexpression of GMP-140 and PAF by endothelium stimulated by histamine or thrombin: a juxtacrine system for adhesion and activation of neutrophyls. J Cell Biol, 115:223–234.PubMedCrossRefGoogle Scholar
  34. 34.
    Cybulsky MI, Gimbrone MA Jr. 1991. Endothelial expression of mononuclear leukocyte adhesion molecule during atherogenesis. Science, 251:788–791.PubMedCrossRefGoogle Scholar
  35. 35.
    Poston RN, Haskard DO, Coucher JR, Gall NP, Johnson-Tidey RR. 1992. Expression of intercellular adhesion molecule-1 in atherosclerotic plaque. Amer J Pathol, 140:665–673.Google Scholar
  36. 36.
    O’Brien KD, Allen MD, McDonald TO, Chait A, Harlan JM, Fishbein D, McCarty J, Ferguson M, Hudkins K, Benjamin CD, Lobb R, Alpers CE. 1993. Vascular cell adhesion molecule-1 is expressed in human coronary atherosclerotic plaques. Implication for the mode of progression of advanced coronary atherosclerosis. J Clin Invest, 92:945–951.PubMedCrossRefGoogle Scholar
  37. 37.
    Wood KM, Cadogan MD, Ramshaw AL, Parums DV. 1993. The distribution of adhesion molecules in human atherosclerosis. Histopathology, 22:437–444.PubMedCrossRefGoogle Scholar
  38. 38.
    Hajjar DP. 1991. Viral pathogenesis of atherosclerosis. Impact of molecular mimicry and viral genes. Amer J Pathol, 139:1195–1211.Google Scholar
  39. 39.
    Persoons MCJ, Daemen MJAP, Bruning JH, Bruggeman CA. 1994. Active cytomegalovirus infection of arterial smooth muscle cells in immunocompromised rats. A clue to herpesvirus-associated atherogenesis. Circ Res, 75:214–220.PubMedCrossRefGoogle Scholar
  40. 40.
    Melnick JL, Adam E, Debakey ME. 1993. Cytomegalovirus and atherosclerosis. Eur Heart J, 14:30–38.PubMedGoogle Scholar
  41. 41.
    Childs B, Emanuel D. 1993. Cytomegalovirus infection and compromise. Exp Hematol, 21: 198–200.PubMedGoogle Scholar
  42. 42.
    Scheglovitova ON, Romanov YuA, Maksianina EV, Kabaeva NV. 2001. Herpes simplex type I virus infection of cultured human vascular endothelial cells: expression of cell adhesion molecules and induction of interferon and cytokine production by blood mononuclear cells. Russian J Immunol, 6:367–376.Google Scholar
  43. 43.
    Bevilacqua MP. 1993. Endothelial-leukocyte adhesion molecules. Annu Rev Immunol, 11:767–804.PubMedCrossRefGoogle Scholar
  44. 44.
    Scheglovitova ON, Romanov YuA, Maksianina EV, Svintsitskaya VA, Pronin AG. 2002. Herpes simplex type I virus infected human vascular endothelial cells induce the production of anti-viral and proinflammatory factors by peripheral blood leukocytes in vitro. Russian J Immunol, in press.Google Scholar
  45. 45.
    Pampou SYu, Gnedoy SN, Bystrevskaya VB, Smirnov VN, Chazov EI, Melnick JL, DeBakey ME. 2000. Cytomegalovirus genome and the immediate-early antigen in cells of different layers of human aorta. Virchows Arch, 436:539–552.PubMedCrossRefGoogle Scholar
  46. 46.
    Antonov AS, Nikolaeva MA, Klueva TS, Romanov YuA, Babaev VR, Bystrevskaya VB, Perov NA, Repin VS, Smirnov VN. 1986. Primary culture of endothelial cells from atherosclerotic human aorta. I. Identification, morphological and ultrastructural characteristics of two endothelial subpopulations. Atherosclerosis, 59:1–19.PubMedCrossRefGoogle Scholar
  47. 47.
    Tokunaga O, Fan J, Watanabe T. 1989. Atherosclerosis- and age-related multinucleated variant endothelial cells in primary culture from human aorta. Amer J Pathol, 135:967–976.Google Scholar
  48. 48.
    Smirnov VN, Repin VS, Tkachuk VA, Chazov EI. 1988. Vascular endothelium in atherosclerosis a multidisciplinary approach. In: Endothelial cells (Ryan US, Ed.) 3:139–215.Google Scholar
  49. 49.
    Watanabe T, Tokunaga O. 1990. Multinucleated variant endothelial cell. Its characteristics and relation to atherosclerosis. Ann NY Acad Sci, 598:217–222.PubMedCrossRefGoogle Scholar
  50. 50.
    Wu L, Satoh T, Tokunaga O. 1999. Formation of multinucleated variant endothelial cells in vitro and investigation of MVECs’ features. Fukuoka Igaku Zasshi, 90:377–391.PubMedGoogle Scholar
  51. 51.
    Satoh T, Sasatomi E, Yamasaki F, Ishida H, Wu L, Tokunaga O. 1998. Multinucleated variant endothelial cells (MVECs) of human aorta: expression of tumor suppressor gene p53 and relation to atherosclerosis and aging. Endothelium, 6:123–132.PubMedCrossRefGoogle Scholar
  52. 52.
    Tokunaga O, Satoh T, Yamasaki F, Wu L. 1998. Multinucleated variant endothelial cells (MVECs) in human aorta: chromosomal aneuploidy and elevated uptake of LDL. Semin Thromb Hemost, 24:279–284.PubMedCrossRefGoogle Scholar
  53. 53.
    Romanov YuA, Antonov AS. 1991. Morphological and functional features of human aortic endothelium. I. Two variants of endothelial organization in atherosclerosis. Cytologiya, 33:7–15 (in Russian).Google Scholar
  54. 54.
    Romanov YuA, Balyasnikova IV, Bystrevskaya VB, Byzova TV, Ilyinskaya OP, Krushinsky AV, Latsis RV, Soboleva EL, Tararak EM, Smirnov VN. 1995. Endothelial heterogeneity and intimal blood-borne cells. Relation to human atherosclerosis. Ann NY Acad Sci, 748:12–37.PubMedCrossRefGoogle Scholar
  55. 55.
    Romanov YuA, Khodakova TG, Kabaeva NV, Dormeneva EV, Pronin AG. 1999. Clustering of human aortic endothelium: possible involvement in atherogenesis. Angiol Vase Surg, 5 (suppl): 166–180.Google Scholar
  56. 56.
    Romanov YuA, Kabaeva NV, Dormeneva EV. 1998. Morphological and functional features of human aortic endothelium. III. Growth in culture and formation of colonies at low seeding density. Cytologiya, 40:127–132 (in Russian).Google Scholar
  57. 57.
    Huss R. 2000. Isolation of primary and immortalized CD34-hematopoietic and mesenchymal stem cells from various sources. Stem Cells, 18:1–9.PubMedCrossRefGoogle Scholar
  58. 58.
    Bender JG, Unverzagt K, Walker DE, Lee W, Smith S, Williams S, Van Epps DE. 1994. Phenotypic analysis and characterization of CD34+ cells from normal human bone marrow, cord blood, peripheral blood, and mobilized peripheral blood from patients undergoing autologous stem cell transplantation. Clin Immunol Immunopathol, 70:10–18.PubMedCrossRefGoogle Scholar
  59. 59.
    Levesque JP, Leavesley DI, Niutta S, Vadas M, Simmons PJ. 1995. Cytokines increase human hemopoietic cells adhesiveness by activation of very late antigen (VLA)-4 and VLA-5 integrins. J Exp Med, 181:1805–1815.PubMedCrossRefGoogle Scholar
  60. 60.
    Voermans C, Rood PML, Hordijk PL, Gerritsen WR, van der Schoot CE. 2000. Adhesion molecules involved in transendothelial migration of human hematopoietic progenitor cells. Stem Cells, 18:435–443.PubMedCrossRefGoogle Scholar
  61. 61.
    Whetton AD, Graham GJ. 1999. Homing and mobilization in the stem cell niche. Trends Cell Biol, 9:233–238.PubMedCrossRefGoogle Scholar
  62. 62.
    Chazov EI, Repin VS, Orekhov AN, Antonov AS, Preobrazhensky SN, Soboleva EL, Smirnov VN. 1986. What has been learned studying human arteries. Atherosclerosis Reviews, Raven Press, 14:7–60.Google Scholar
  63. 63.
    Soboleva EL, Popkova VM. 1989. Hemopoietic progenitor cells (CFU-GM) in the intima of human atheromatous aorta. Bull Exp Biol Med, 5:600–604 (in Russian).Google Scholar
  64. 64.
    Soboleva EL, Smirnov VN. 1995. Local hemo- and stromopoiesis in human vascular wall. Lectures of XIII-th Meeting of the International Society of Haematology, pp. 134–139.Google Scholar
  65. 65.
    Soboleva EL, Popkova VM, Saburova OS, Tararak EM, Tvorogova MG, Smirnov VN 1995. Colony forming units and atherosclerosis. In: Atherosclerosis X, Elsevier Science, pp. 919–925.Google Scholar
  66. 66.
    Soboleva EL, Saburova OS, Rozhkova TA, Tvorogova MG. 1999. Stem cells of hemopoietic and stromal differentiation lineages and human atherosclerosis. Angiol Vasc Surg, 5 (suppl): 190–203.Google Scholar
  67. 67.
    Smirnov VN, Antonov AS, Bystrevskaya VB, Voyno-Yasenetskaya TA, Kabaeva NV, Romanov YuA, Sukhova GA, Soboleva EL, Tkachuk VA, Tararak EM. 1992. Cellular polymorphism in human aortic intima. Atherosclerosis IX, Proc. IX-th Int. Symp. on Atherosclerosis, pp. 295–298.Google Scholar
  68. 68.
    Soboleva EL, Shindler EM, Saburova OS, Tvorogova MG, Smirnov VN. 1994. Colony-forming units for fibroblasts (CFU-f) in the peripheral blood of patients with primary hypercholesterolemia. In: New pathogenic aspects of atherosclerosis. Nordrhein-Westfalische Academie der Wissenschaffen, Westdeutscher Verlag, pp. 79–93.Google Scholar
  69. 69.
    Ross R. 1993. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature, 362: 801–808.PubMedCrossRefGoogle Scholar
  70. 70.
    Gordon D, Reidy MA, Benditt EP, Schwartz SM. 1990. Cell proliferation in coronary arteries. Proc Natl Acad Sci USA, 87:4600–4604.PubMedCrossRefGoogle Scholar
  71. 71.
    Schwartz SM, O’Brien ERM. 1995. Absence of replication of vascular smooth muscle. Atherosclerosis X, Elsevier Science, pp. 704–720.Google Scholar
  72. 72.
    Stary HC. 1993. The evolution of human atherosclerotic lesions. Merck & Co., Inc West Point.Google Scholar
  73. 73.
    Deans RJ, Moseley AB. 2000. Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol, 28:875–884.PubMedCrossRefGoogle Scholar
  74. 74.
    Minguell JJ. 2000. Biology and clinical utilization of mesenchymal progenitor cells. Braz J Med Biol Res, 33:881–887.PubMedCrossRefGoogle Scholar
  75. 75.
    Huss R, Lange C, Weissinger EM, Kolb H-J, Thalmeier K. 2000. Evidence of peripheral blood-derived, plastic-adherent CD34-/low hematopoietic stem cell clones with mesenchymal stem cell characteristics. Stem Cells, 18:252–260.PubMedCrossRefGoogle Scholar
  76. 76.
    Kuznetsov SA, Mankani MH, Gronthos SG, Satomura K, Bianco P, Robey PG. 2001. Circulating skeletal stem cells. J Cell Biol, 153:1133–1139.PubMedCrossRefGoogle Scholar
  77. 77.
    Rafii S. 2000. Circulating endothelial precursors: mystery, reality, and promise. J Clin Invest, 105:17–19.PubMedCrossRefGoogle Scholar
  78. 78.
    Zvaifler NJ, Marinova-Mutafchieva L, Adams G, Edwards CJ, Moss J, Burger JA, Maini RN. 2000. Mesenchymal precursor cells in the blood of normal individuals. Arthr Res, 2:477–488.CrossRefGoogle Scholar
  79. 79.
    Friedenstein AJ, Chailakhjan RK, Lalykina KS. 1970. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet, 3:393–403.PubMedGoogle Scholar
  80. 80.
    Friedenstein AJ, Deriglasova UF, Kulagina NN, Panasuk AF, Rudakova SF, Luria EA, Rudakov IA. 1974. Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol, 2:83–92.PubMedGoogle Scholar
  81. 81.
    Friedenstein AJ. 1990. Osteogenic stem cells in the bone marrow. Bone and Mineral Research, 7:243–272.Google Scholar
  82. 82.
    Pittenger MF, Maccay AM. 2000. Multipotential human mesenchymal stem cells. Graft, 3:288–294.Google Scholar
  83. 83.
    Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD. 2002. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation, 105:93–98.PubMedCrossRefGoogle Scholar
  84. 84.
    Sanchez-Ramos J, Song S, Cardozo-Pelaez F, Hazzi C, Stedeford T, Willing A, Freeman TB, Saporta S, Janssen W, Patel N, Cooper DR, Sanberg PR. 2000. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol, 164:247–256.PubMedCrossRefGoogle Scholar
  85. 85.
    Clarke D, Frisen J. 2001. Differentiation potential of adult stem cells. Curr Opin Gen Devel, 11:575–580.CrossRefGoogle Scholar
  86. 86.
    Makino S, Fukuda K, Miyoshi S, Konishi F, Kodama H, Pan J, Sano M, Takahashi T, Hori S, Abe H, Hata J, Umezawa A, Ogawa S. 1999. Cardiomyocytes can be generated from marrow stromal cells in vitro. J Clin Invest, 103:697–705.PubMedCrossRefGoogle Scholar
  87. 87.
    Springer ML, Brazelton TR, Blau HM. 2001. Not the usual suspects: the unexpected sources of tissue regeneration. J Clin Invest, 107:1355–1356.PubMedCrossRefGoogle Scholar
  88. 88.
    Mackenzie TC, Flake AW. 2001. Human mesenchymal stem cell persist, demonstrate site-specific multipotential differentiation, and are present in sites of wound healing and tissue regeneration after transplantation into fetal sheep. Blood Cell Mol Dis, 27:601–604.CrossRefGoogle Scholar
  89. 89.
    Gill M, Dias S, Hattori K, Rivera ML, Hioklin D, Witte L, Girardi L, Yurt R, Himel H, Rafii S. 2001. Vascular trauma induces rapid but transient mobilization of VEGFR2(+)AC133(+) endothelial precursor cells. Circ Res, 88:167–174.PubMedCrossRefGoogle Scholar
  90. 90.
    Krushinsky AV, Nestaiko GV. 1987. Morphology of smooth muscle cells from normal and atherosclerotic human aorta. Soc Med Rev A Cardiol, 1:35–73.Google Scholar
  91. 91.
    Benditt EP, Benditt JM. 1973. Evidence for a monoclonal origin of human atherosclerotic plaques. Proc Natl Acad Sci USA, 70:1753–1756.PubMedCrossRefGoogle Scholar
  92. 92.
    Pearson TA, Dillman JM, Heptinstall RH. 1987. Clonal mapping of the human aorta. Relationship of monoclonal characteristics, lesion thickness, and age in normal intima and atherosclerotic lesions. Am J Pathol, 126:33–39.PubMedGoogle Scholar
  93. 93.
    Hillebrands JL, Klatter FA, van den Hurk BM, Popa ER, Nieuwenhuis P, Rosing J. 2001. Origin of neointimal endothelium and alpha-actin-positive smooth muscle cells in transplant arteriosclerosis. J Clin Invest, 107:1411–1422.PubMedCrossRefGoogle Scholar
  94. 94.
    Brazelton TR, Adams B, Shorthouse R, Morris RE. 1999. Chronic rejection: the result of uncontrolled remodeling of graft tissue by recipient mesenchymal cells? Data from two rodent models and the effects of immunosuppressive therapies. Inflamm Res, 48 (suppl. 2):S134–S135.PubMedCrossRefGoogle Scholar
  95. 95.
    Grimm PC, Nickerson P, Jeffery J, Savani RC, Gough J, McKenna RM, Stern E, Rush DN. 2001. Neointimal and tubulointersticial infiltration by recipient mesenchymal cells in chronic renal-allograft rejection. N Engl J Med, 345:93–97.PubMedCrossRefGoogle Scholar
  96. 96.
    Quaini F, Urbanek K, Beltrami AP, Finato N, Beltrami CA, Nadal-Ginard B, Kajstura J, Leri A, Anversa P. 2002. Chimerism of the transplanted heart. N Engl J Med, 346:5–15.PubMedCrossRefGoogle Scholar
  97. 97.
    Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, Pickel J, McKay R, Nadal-Ginard B, Bodine DM, Leri A, Anversa P. 2001. Bone marrow cells regenerate infarcted myocardium. Nature, 410:701–705.PubMedCrossRefGoogle Scholar
  98. 98.
    Orlic D, Kajstura J, Chimenti S, Limana F, Jakoniuk I, Quaini F, Nadal-Ginard B, Bodine DM, Leri A, Anversa P. 2001a. Mobilized bone marrow cells repair the infarcted heart, improving function and survival. PNAS, 98:10344–10349.CrossRefGoogle Scholar
  99. 99.
    Kamihata H, Matsubara H, Nishiue T, Fujiyama S, Tsutsumi Y, Ozono R, Masaki H, Mori Y, Iba O, Tateishi E, Kosaki A, Shintani S, Murohara T. 2001. 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, 104:1046–1052.PubMedCrossRefGoogle Scholar
  100. 100.
    Jackson KA, Majka SM, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK, Goodell MA. 2001. Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest, 107:1395–1402.PubMedCrossRefGoogle Scholar
  101. 101.
    Asakura A, Komaki M, Rudnichki M. 2001. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation, 68:245–253.PubMedCrossRefGoogle Scholar
  102. 102.
    Bhattacharya V, McSweeney PA, Shi Q, Bruno B, Ishida A, Nash R, Storb RF, Sauvage LR, Hammond WP, Wu MH. 2000. Enhanced endothelialization and microvessel formation in polyester grafts seeded with CD34+ bone marrow cells. Blood, 95:581–585.PubMedGoogle Scholar
  103. 103.
    Campbell JH, Efendy Jl, Han C, Girjes AA, Campbell GR. 2000. Haemopoietic origin of myofibroblasts formed in the peritoneal cavity in response to a foreign body. J Vase Res, 37:364–371.CrossRefGoogle Scholar
  104. 104.
    Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. 2001. Multilineage cells from human adipose tissue: implication for cell-based therapies. Tissue Eng, 7:211–228.PubMedCrossRefGoogle Scholar
  105. 105.
    Soboleva EL, Kukharchuk VV, Akchurin RS, Smirnov VN. 1997. Bone marrow colony-forming units for fibroblasts in the blood of patients with primary hyperlipidemia. Atherosclerosis, 134:302.CrossRefGoogle Scholar
  106. 106.
    Smirnov VN, Soboleva EL, Rogova EM, Akchurin RS, Chazov EI. 1998. Bone marrow response to hypercholesterolemia (HCL) in coronary patients. Atherosclerosis, 136 (suppl):63.CrossRefGoogle Scholar
  107. 107.
    Bassenge E. 1996. Endothelial function in different organs. Prog Cardiovasc Dis, 39:209–228.PubMedCrossRefGoogle Scholar
  108. 108.
    Pels K, Labinaz M, O’Brien ER. 1997. Arterial wall neovascularization—potential role in atherosclerosis and restenosis. Jpn Cire J, 61:893–904.CrossRefGoogle Scholar
  109. 109.
    Moulton KS. 2001. Plaque angiogenesis and atherosclerosis. Curr Atheroscler Rep, 3:225–233.PubMedCrossRefGoogle Scholar
  110. 110.
    Freedman SB, Isner JM. 2001. Therapeutic angiogenesis for ischemic cardiovascular disease. J Mol Cell Cardiol, 33:379–393.PubMedCrossRefGoogle Scholar
  111. 111.
    Tomita S, Li R-K, Weisel RD, Mickle DAD, Kim E-J, Sakai T, Jia Z-Q. 1999. Autologous transplantation of bone marrow cells improves damaged heart function. Circulation, 100 (suppl. II): 247–256.Google Scholar
  112. 112.
    Strauer BE, Brehm M, Zeus T, Gattermann N, Hernandez A, Sorg RV, Kogler G, Wernet P. 2001. Intrakoronare, humane autologe stannzelltransplantation zur myokardregeneration nach herzinfarkt. Dtsch Med Wschr, 126:932–938.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2003

Authors and Affiliations

  • Yu. A. Romanov
    • 1
  • E. L. Soboleva
    • 1
  • V. N. Smirnov
    • 1
  • A. Bobik
    • 2
  1. 1.Cardiology Research CenterMoscowRussia
  2. 2.Alfred Baker Medical UnitBaker Medical Research Institute & Alfred HospitalMelbourneAustralia

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