CELL THERAPY OF CRITICAL LIMB ISCHEMIA (PROBLEMS AND PROSPECTS)

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Abstract

Critical limb ischemia is a syndrome that combines several peripheral artery diseases with different ethiology and pathogenesis but with similar prognosis, high morbidity and mortality. Possibility of surgical and conservative treatment of critical limb ischemia almost completely exhausted. Some hopes have arisen due to progress in cell technology. The article provides a critical analysis of pathogenic prerequisites of stem/progenitor cells for the treatment of patients with a critical limb ischemia in detail the basic results of preclinical and clinical studies on the safety and efficacy of cell technology. Unsolved problems and prospects of practical application are also discussed.

About the authors

S. V. Lebedev

Medical Center of the Bank of Russia, Moscow, Russian Federation

Author for correspondence.
Email: lebedsv@mail.ru
кандидат медицинских наук, старший научный сотрудник, врач Центра доказательной медицинской практики и инновационных технологий стационара Медицинского центра Банка России Адрес: 117593, Москва, Севастопольский проспект, д. 66; тел.: (495) 676-80-50 Россия

A. V. Karasev

Medical Center of the Bank of Russia, Moscow, Russian Federation

Email: stemcell@inbox.ru
заведующий отделением молекулярно-клеточных технологий Медицинского центра Банка России Адрес: 117593, Москва, Севастопольский проспект, д. 66; тел.: (495) 676-80-50 Россия

V. V. Kungurtsev

Medical Center of the Bank of Russia, Moscow, Russian Federation

Email: kung-vadim@yandex.ru
доктор медицинских наук, профессор, сердечно-сосудистый хирург Медицинского центра Банка России Адрес: 117593, Москва, Севастопольский проспект, д. 66; тел.: (495) 676-83-16 Россия

A. V. Lokhonina

Medical Center of the Bank of Russia, Moscow, Russian Federation

Email: anastasia.cell@gmail.com
биолог Центра доказательной медицинской практики и инновационных техно- логий стационара Медицинского центра Банка России Адрес: 117593, Москва, Севастопольский проспект, д. 66; тел.: (495) 676-83-74 Россия

E. B. Kleimenova

Medical Center of the Bank of Russia, Moscow, Russian Federation

Email: stemcell@inbox.ru
доктор медицинских наук, заведующая Центром доказательной медицинской прак- тики и инновационных технологий стационара Медицинского центра Банка России Адрес: 117593, Москва, Севастопольский проспект, д. 66; тел.: (495) 676-80-11 Россия

References

  1. Bell P.F., Charlesworth D., DePalma R.G. The difinition of critical ischemia of a limb. Brit. J. Surg. 1982; 69: 2.
  2. Samodai V.D., Parkhisenko Yu.A., Ivanov A.A. Nestandartnaya khirurgiya kriticheskoi ishemii nizhnikh konechnostei [Nonstandard Surgery of Critical Lower Limb Ischemia]. Moscow, MIA, 2009. 240 p.
  3. Bosiers M., Schneider P.A. Critical limb ischemia. N.-Y.: Informa Healthcare USA. 2009. 352 p.
  4. Autologichnye stvolovye kletki. Eksperimental'nye issledovaniya i perspektivy klinicheskogo primeneniya. Rukovodstvo dlya vrachei. Pod red. V.A. Tkachuka [Autologous stem cells. Experimental study and clinical application prospects. Guidelines for doctors. Ed. V.A. Tkachuk]. Moscow, Litterra, 2009. 448 p.
  5. Hirsch A.T., Haskal Z.J., Hertzer N.R., Bakal C.W., Creager M.A., Halperin J.L., Hiratzka L.F., Murphy W.R., Olin J.W., Puschett J.B., Rosenfield K.A., Sacks D., Stanley J.C., Taylor L.M. Jr., White C.J., White J., White R.A., Antman E.M., Smith S.C. Jr., Adams C.D., Anderson J.L., Faxon D.P., Fuster V., Gibbons R.J., Hunt S.A., Jacobs A.K., Nishimura R., Ornato J.P., Page R.L., Riegel B. Practice Guidelines for the management of patients with peripheral arterial disease (lower extremity, renal, mesenteric, and abdominal aortic): a collaborative report from the American Association for Vascular Surgery Society for Vascular Surgery, Society for Cardiovascular Angiography and Interventions, Society for Vascular Medicine and Biology, Society of Interventional Radiology, and the ACC/AHA Task Force on Practice Guidelines (Writing Committee to Develop Guidelines for the Management of Patients With Peripheral Arterial Disease): endorsed by the American Association of Cardiovascular and Pulmonary Rehabilitation; National Heart, Lung, and Blood Institute; Society for Vascular Nursing; Transatlantic Inter-Society Consensus; and Vascular Disease Foundation. Circulation. 2006; 113: 463–654.
  6. Second European Consensus Document on chronic critical leg ischemia. Circulation. 1991; 84 (4): 16–26.
  7. Lawall H., Bramlage P., Amann B. Stem cell and progenitor cell therapy in peripheral artery disease. A critical appraisal. Thromb. Haemost. 2010; 103: 696–709.
  8. Adam D.J., Beard J.D., Cleveland T., Bell J., Bradbury A.W., Forbes J.F., Fowkes F.G., Gillepsie I., Ruckley C.V., Raab G., Storkey H. Bypass versus angioplasty in severe ischaemia of the leg (BASIL): multicentre, randomised controlled trial. Lancet. 2005; 366: 1925–1934.
  9. Norgren L., Hiatt W.R., Dormandy J.A., Nehler M.R., Harris K.A., Fowkes F.G., Bell K., Caporusso J., Durand-Zaleski I., Komori K., Lammer J., Liapis C., Novo S., Razavi M., Robbs J., Schaper N., Shigematsu H., Sapoval M., White C., White J., Clement D., Creager M., Jaff M., Mohler E. 3rd, Rutherford R.B., Sheehan P., Sillesen H., Rosenfield K. Inter-society consensus for the management of peripheral arterial disease (TASC II). Eur. J. Vasc. Endovasc. Surg. 2007; 33 (1): 1–75.
  10. Guidelines for percutaneous transluminal angioplasty. Standards of practice committee of the society of cardiovascular and interventional radiology. Radiology. 1990; 177: 619–626.
  11. Valentine R.J., Myers S.I., Inman M.H., Roberts J.R., Clagett G.P. Late outcome of amputees with premature atherosclerosis. Surgery. 1996; 119: 487–493.
  12. Asahara T., Masuda H., Takahashi T. , Kalka C., Pastore C., Silver M., Kearne M., Magner M., Isner J.M. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ. Res. 1999; 85: 221–228.
  13. Makinen K., Manninen H., Hedman M., Matsi P., Mussalo H., Alhava E., Ylä-Herttuala S. Increased vascularity detected by digital subtraction angiography after VEGF gene transfer to human lower limb artery: a randomized, placebo-controlled, double-blinded phase II study. Mol. Ther. 2002; 6: 127–133.
  14. Rajagopalan S., Mohler E.R., Lederman R.J., Mendelsohn F.O., Saucedo J.F., Goldman C.K., Blebea J., Macko J., Kessler P.D., Rasmussen H.S., Annex B.H. Regional angiogenesis with vascular endothelial growth factor in peripheral arterial disease: a phase II randomized, double-blind, controlled study of adenoviral delivery of vascular endothelial growth factor 121 in patients with disabling intermittent claudication. Circulation. 2003; 108: 1933–1938.
  15. Isner J.M., Walsh K., Symes J., Pieczek A., Takeshita S., Lowry J., Rosenfield K., Weir L., Brogi E., Jurayj D. Arterial gene transfer for therapeutic angiogenesis in patients with peripheral artery disease. Hum. Gene Ther. 1996; 7 (8): 959–988.
  16. Khan T.A., Sellke F.W., Laham R.J. Gene therapy progress and prospects: therapeutic angiogenesis for limb and myocardial ischemia. Gene Ther. 2003; 10: 285–291.
  17. Maulik N. NV1FGF, a pCOR plasmid-based angiogenic gene therapy for the treatment of intermittent claudication and critical limb ischemia. Curr. Opin. Investig. Drugs. 2009; 10 (3): 259–268.
  18. Nikol S., Baumgartner I.,Van Belle E., Diehm C., Visoná A., Capogrossi M.C., Ferreira-Maldent N., Gallino A., Wyatt M.G., Wijesinghe L.D., Fusari M., Stephan D., Emmerich J., Pompilio G., Vermassen F., Pham E., Grek V., Coleman M., Meyer F. Therapeutic angiogenesis with intramuscular NV1FGF improves amputation-free survival in patients with critical limb ischemia. Mol. Ther. 2008; 16 (5): 972–978.
  19. Belch J., Hiatt W.R., Baumgartner I., Driver I.V., Nikol S., Norgren L., Van Belle E. Effect of fibroblast growth factor NV1FGF on amputation and death: a randomised placebo-controlled trial of gene therapy in critical limb ischaemia. TAMARIS Committees and Investigators. Lancet. 2011; 377 (9781): 1929–1937.
  20. Kusumanto Y.H., Van Weel V., Mulder N.H., Smit A.J., Van den Dungen J.J., Hooymans J.M., Sluiter W.J., Tio R.A., Quax P.H., Gans R.O., Dullaart R.P., Hospers G.A. Treatment with intramuscular vascular endothelial growth factor gene compared with placebo for patients with diabetes mellitus and critical limb ischemia: a double-blind randomized trial. Hum. Gene Ther. 2006; 17: 683–691.
  21. Testa U., Pannitteri G. Vascular endothelial growth factors in cardiovascular medicine. J. Cardiovasc. Med. 2008; 9 (12): 1190–1221.
  22. Lederman R.J., Mendelsohn F.O., Anderson R.D., Saucedo J.F., Tenaglia A.N., Hermiller J.B., Hillegass W.B., Rocha-Singh K., Moon T.E., Whitehouse M.J., Annex B.H. Therapeutic angiogenesis with recombinant fibroblast growth factor-2 for intermittent claudication (the TRAFFIC study): a randomised trial. Lancet. 2002; 359 (9323): 2053–2058.
  23. Comerota A.J., Throm R.C., Miller K.A., Henry T., Chronos N., Laird J., Sequeira R., Kent C.K., Bacchetta M., Goldman C., Salenius J.P., Schmieder F.A., Pilsudski R. Naked plasmid DNA encoding fibroblast growth factor type 1 for the treatment of end-stage unreconstructible lower extremity ischemia: preliminary results of a phase I trial. J. Vasc. Surg. 2002; 35: 930–936.
  24. Leppanen P., Kholova I. Short and long-term effects of hVEGF-A (165) in Creactivated transgenetic mice. PLoS One. 2006; 1: 13.
  25. Tang, D.C., DeVit, M., Johnston S.A. Genetic immunization is a simple method for eliciting an immune response. Nature. 1992; 356: 152–154.
  26. Armstrong L., Lako M., Buckley N., Lappin T.R., Murphy M.J., Nolta J.A., Pittenger M., Stojkovic M. Our top 10 developments in stem cell biology over the last 30 years. Stem Cells. 2012; 30 (1): 2–9.
  27. Lawall H, Bramlage P, Amann B. Stem cell and progenitor cell therapy in peripheral artery disease. Thromb. Haemost. 2010; 103: 696–709.
  28. Biologicheskie rezervy kletok kostnogo mozga i korrektsiya organnykh disfunktsii. Pod red. V.I. Shumakova, N.A. Onishchenko [Biological reserves of bone marrow cells and correction of organ dysfunction. Ed. V.I. Shumakov, N.A. Onishchenko]. Moscow, Lavr, 2009. 308 p.
  29. Toma C., Wagner W.R., Bowry S., Schwartz A., Villanueva F. Fate of cultured-expanded mesenchymal stem cells in the microvasculature: in vivo observations of cell kinetics. Circ. Res. 2009; 104 (3): 398–402.
  30. Furlani D., Ugurlucan M., Ong L., Bieback K., Pittermann E., Westien I., Wang W., Yerebakan C., Li W., Gaebel R., Li R.K., Vollmar B., Steinhoff G., Ma N. Is the intravascular administration of mesenchymal stem cells safe? Mesenchymal stem cells and intravital microscopy. Microvasc. Res. 2009; 77 (3): 370–376.
  31. Konoplyannikov A.G., Petriev V.M., Konoplyannikova O.A. Effects of (60)Сo whole-body gamma-irradiation in different doses on the distribution of (188)Re-labeled autologous mesenchymal stem cells in wistar rats after intravenous (systemic) transplantation during different periods after exposure. Bull. Exp. Biol. Med. 2008; 145 (4): 520–525.
  32. Li S.H., Lai T.Y. Tracking cardiac engraftment and distribution of implanted bone marrow cells: Comparing intra-aortic, intravenous and intramyocardial delivery. J. Thorac. Cardiovasc. Surg. 2009; 137 (5): 1225–1233.
  33. Hou D., Youssef E.A., Brinton T.J., Zhang P., Rogers P., Price E.T., Yeung A.C., Johnstone B.H., Yock P.G., March K.L. Radiolabeled cell distribution after intramyocardial, intracoronary, and interstitial retrograde coronary venous delivery: implications for current clinical trials. Circulation. 2005; 112 (Suppl. 9): 1150–1156.
  34. Pal'tsev M.A. Biologiya stvolovykh kletok i kletochnye tekhnologii. Pod red. M.A. Pal'tseva [Stem cell biology and cellular technologies. Ed. M.A. Pal'tsev]. Moscow, Meditsina, 2009. 728 p.
  35. Buschmann I., Schaper W. The pathophysiology of the collateral circulation (arteriogenesis). J. Pathol. 2000; 190: 338–342.
  36. Voskuil M., Van Royen N., Hoefer I. Buschmann I, Schaper W, Piek JJ. Angiogenesis and arteriogenesis; the long road from concept to clinical application. Ned. Tijdschr. Geneeskd. 2001; 145: 670–675.
  37. Zhou B., Poon M.C., Pu W.T., Han Z.C. Therapeutic neovascularization for peripheral arterial diseases: advances and perspectives. Histol. Histopathol. 2007; 22: 677–686.
  38. Kalka C., Masuda H., Takahashi T. , Kalka-Moll W.M., Silver M., Kearney M., Li T., Isner J.M., Asahara T. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc. Natl. Acad. Sci. USA. 2000; 97: 3422–3427.
  39. Hirota K., Semenza G.L. Regulation of angiogenesis by hypoxia-inducible factor 1. Crit. Rev. Oncol. Hematol. 2006; 59: 15–26.
  40. Harraz M., Jiao C., Hanlon H.D., Hartley R.S., Schatteman G.C. CD34+ blood-derived human endothelial cell progenitors. Stem Cells. 2001; 19: 304–312.
  41. Fernandez P.B., Lucibello F.C., Gehling U.M., Lindemann K., Weidner N., Zuzarte M.L., Adamkiewicz J., Elsässer H.P., Müller R., Havemann K. Endothelial-like cells derived from human CD14 positive monocytes. Differentiation. 2000; 65: 287–300.
  42. Rehman J., Li J., Orschell C.M., March K.L. Peripheral blood «endothelial progenitor cells» are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation. 2003; 107: 1164–1169.
  43. Urbich C., Heeschen C., Aicher A., Dernbach E., Zeiher A.M., Dimmeler S. Relevance of monocytic features for neovascularization capacity of circulating endothelial progenitor cells. Circulation. 2003; 108: 2511–2516.
  44. Asahara T., Murohara T., Sullivan A., Silver M., Van der Zee R., Li T., Witzenbichler B., Schatteman G., Isner J.M. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997; 275: 964–967.
  45. Rookmaaker M.B., Verhaar M.C., Loomans C.J., Verloop R., Peters E., Westerweel P.E., Murohara T., Staal F.J., Van Zonneveld A.J., Koolwijk P., Rabelink T.J., Van Hinsbergh V.W. CD34+ cells home, proliferate, and participate in capillary formation, and in combination with. Arterioscler. Thromb. Vasc. Biol. 2005; 25: 1843–1850.
  46. Ziegelhoeffer T., Fernandez B., Kostin S., Heil M., Voswinckel R., Helisch A., Schaper W. Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circ. Res. 2004; 94: 230–238.
  47. Heil M., Ziegelhoeffer T., Mees B. A different outlook on the role of bone marrow stem cells in vascular growth: bone marrow delivers software not hardware. Circ. Res. 2004; 94 (5): 573–574.
  48. Takahashi T., Kalka C., Masuda H., Chen D., Silver M., Kearney M., Magner M., Isner J.M., Asahara T. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat. Med. 1999; 5: 434–438.
  49. Crosby J.R., Kaminski W.E., Schatteman G. Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circ. Res. 2000; 87: 728–730.
  50. Capla J.M., Ceradini D.J., Tepper O.M., Callaghan M.J., Bhatt K.A., Galiano R.D., Levine J.P., Gurtner G.C. Skin graft vascularization involves precisely regulated regression and replacement of endothelial cells through both angiogenesis and vasculogenesis. Plast. Reconstr. Surg. 2006; 117: 836–844.
  51. 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., Hammond W.P. Evidence for circulating bone marrow-derived endothelial cells. Blood. 1998; 92: 362–367.
  52. Shintani S., Murohara T., Ikeda H., Ueno T., Sasaki K., Duan J., Imaizumi T. Augmentation of postnatal neovascularization with autologous bone marrow transplantation. Circulation. 2001; 103: 897–903.
  53. 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., Imaizumi T., Iwasaka T. 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.
  54. Tidball J.G, Villalta S.A. Regulatory interactions between muscle and the immune system during muscle regeneration. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010; 298 (5): 1173–1187.
  55. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003; 3: 23–35.
  56. Mantovani A., Sica A., Sozzani S., Allavena P., Vecchi A., Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004; 25: 677–686.
  57. De Haro, Acin F., Medina F.J., Lopez-Quintana A., March J.R. Relationship between the plasma concentration of C-reactive protein and severity of peripheral arterial disease. Clin. Med. Cardiol. 2009; 3: 1–7.
  58. Tolar J., Le Blanc K., Keating A., Blazar B.R. Concise review: hitting the right spot with mesenchymal stromal cells. Stem Cells. 2010; 28: 1446–1455.
  59. Williams J.T., Southerland S.S., Souza J., Calcutt A.F., Cartledge R.G. Cells isolated from adult human skeletal muscle capable of differentiating into multiple mesodermal phenotypes. Am. Surg. 1999; 65: 22–26.
  60. Zuk P.A., Zhu M., Mizuno H., Huang J., Futrell J.W., Katz A.J., Benhaim P., Lorenz H.P., Hedrick M.H. Multilineage cells from human adipose tissue: implication for cell-based therapies. Tissue Engl. 2001; 7: 211–228.
  61. Gronthos S., Arthur A., Bartold P.M., Shi S. A method to isolate and culture expand human dental pulp stem cells. J Methods Mol. Biol. 2011; 698: 107–121.
  62. Singer N., Caplan A. Mesenchymal stem cells: mechanisms of inflammation. Ann. Rev. Pathol. 2011; 6: 457–478.
  63. Puissant B., Barreau C., Bourin P., Clavel C, Corre J., Bousquet C., Taureau C., Cousin B., Abbal M., Laharrague P., Penicaud L., Casteilla L., Blancher A. Immunomodulatory effect of human adipose tissue-derived adult stem cell: comparison with bone marrow mesenchymal stem cells. Brit. J. Haematol. 2005; 129 (1): 118–129.
  64. Salem H. Mesenchymal stromal cells: current understanding and clinical status. Stem Cells. 2010; 28: 585–596.
  65. Bunnell B., Betancourt A., Sullivan D. New concepts on the immune modulation mediated by mesenchymal stem cells. Stem Cell Res. Ther. 2010; 1: 34.
  66. Prockop D. Repair of tissues by adult stem/progenitor cells [MSCs]: controversies, myths, and changing paradigms. Mol. Ther. 2009; 17: 939–946.
  67. Miranville A., Heeschen C., Sengenes C., Curat C.A., Busse R., Bouloumié A. Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation. 2004; 110: 349–355.
  68. Miyahara Y., Nagaya N. Monolayered mesenchymal stem cells repair system scarred myocardium after myocardial infarction. Nat. Med. 2006; 12 (4): 459–465.
  69. Rehman J., Traktuev D., Li J., Merfeld-Clauss S., Temm-Grove C.J., Bovenkerk J.E., Pell C.L., Johnstone B.H., Considine R.V., March K.L. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation. 2004; 109: 1292–1298.
  70. YoshidaM., Horimoto H., Mieno S. Intra-arterial bone marrow cell transplantation induces angiogenesis in rat hindlimb ischemia. Eur. Surg. Res. 2003; 35: 86–91.
  71. Rosova I. Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells. 2008; 26: 2173–2182.
  72. Zuk P.A., Zhu M., Ashjian P., De Ugarte D.A., Huang J.I., Mizuno H., Alfonso Z.C., Fraser J.K., Benhaim P., Hedrick M.H. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell. 2002; 13: 4279–4295.
  73. Lin G., Garcia M., Ning H., Banie L., Guo Y.L., Lue T.F., Lin C.S. Defining stem and progenitor cells within adipose tissue. Stem Cells Dev. 2008, 17 (6): 1053–1063.
  74. Lee R.H., Kim B., Choi I., Kim H., Choi H.S., Suh K., Bae Y.C., Jung J.S. Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol. Biochem. 2004; 14: 311–324.
  75. Gimbl J.M., Katz A.J., Bunnell B.A. Adipose-derived stem cells for regenerative medicine. Circ. Res. 2007; 100: 1249–1260.
  76. Peroni D., Scambi I., Pasini A., Lisi V., Bifari F., Krampera M., Rigotti G., Sbarbati A., Galiè M. Stem molecular signature of adipose-derived stromal cells. Exp. Cell Res. 2008; 314: 603–615.
  77. Cao Y., Sun Z., Liao L., Meng Y., Han Q., Zhao R.C. Human adipose tissue-derived stem cells differentiate into endothelial cells in vitro and improve postnatal neovascularization in vivo. Biochem. Biophys. Res. Commun. 2005; 332: 370–379.
  78. Planat-Benard V., Menard C., Andre M., Puceat M., Perez A., Garcia-Verdugo J.M., Pénicaud L., Casteilla L. Spontaneous cardiomyocyte differentiation from adipose tissue stromal cell. Circ. Res. 2004; 94: 223–229.
  79. Moon M.H., Kim S.Y., Kim Y.J., Kim S.J., Lee J.B., Bae Y.C., Sung S.M., Jung J.S. Human adipose tissue-derived mesenchymal stem cells improve postnatal neovascularization in a mouse model of hindlimb ischemia. Cell Physiol. Biochem. 2006; 17: 279–290.
  80. Nakagami H., Maeda K., Morishita R., Iguchi S., Nishikawa T., Takami Y., Kikuchi Y., Saito Y., Tamai K., Ogihara T., Kaneda Y. Novel autologous cell therapy in ischemic limb disease through growth factor secretion by cultured adipose tissue-derived stromal cells. Arterioscler. Thromb. Vasc. Biol. 2005; 25: 2542–2547.
  81. Di Rocco G., Iachininoto M.G., Tritarelli A., Straino S., Zacheo A., Germani A., Crea F., Capogrossi M.C. Myogenic potential of adipose-tissue-derived cells. J. Cell Sci. 2009; 119: 2945–2952.
  82. Chu K., Kim M., Chae S.H., Jeong S.W., Kang K.S., Jung K.H., Kim J., Kim Y.J., Kang L., Kim S.U., Yoon B.W. Distribution and in situ proliferation patterns of intravenously injected immortalized human neural stem-like cells in rats with focal cerebral ischemia. Neurosci. Res. 2004; 50 (4): 459–465.
  83. Murohara T., Ikeda H., Duan J., Shintani S., Sasaki K., Eguchi H., Onitsuka I., Matsui K., Imaizumi T. Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. J. Clin. Invest. 2000; 105: 1527–1536.
  84. Finney M.R., Greco N.J., Haynesworth S.E., Martin J.M., Hedrick D.P., Swan J.Z., Winter D.G., Kadereit S., Joseph M.E., Fu P., Pompili V.J., Laughlin M.J. Direct comparison of umbilical cord blood versus bone marrow-derived endothelial precursor cells in mediating neovascularization in response to vascular ischemia. Biol. Blood Marrow Transplant. 2006; 12: 585–593.
  85. Waterman R.S., Betancourt А.М. et al. Treating chronic pain with mesenchymal stem cells: A therapeutic approach worthy of continued investigation. J. Stem Cell Res. & Ther. 2011; S2:1-9.
  86. Ogawa R., Oki K., Hyakusoku H. Vascular tissue engineering and vascularized 3D tissue regeneration. Regenerative Medicine. 2007; 2 (5): 831–837.
  87. Dimmtlr S., Zeiher A.M. Vascular repair by circulation endothelial progenitor cells: the missing link in atheroscrerosis. J. Mol. Med. 2005; 82: 671–677.
  88. Tateishi-Yuyama E., Matsubara H., Murohara T., Ikeda U., Shintani S., Masaki H., Amano K., Kishimoto Y., Yoshimoto K., Akashi H., Shimada K., Iwasaka T., Imaizumi T. Therapeutic angiogenesis for patients with limb ischemia by autologous transplantation of bone-marrow cells: a pilot study and a randomized controlled trial. Lancet. 2002; 360 (9331): 427–35.
  89. Sugihara S., Yamamoto Y., Matsubara K., et al. Autoperipheral blood mononuclear cell transplantation improved giant ulcers due to chronic arteriosclerosis obliterans. Heart Vessels. 2006; 21:258–262.
  90. Matoba S., Matsubara H. Therapeutic angiogenesis for peripheral artery diseases by autologous bone marrow cell transplantation. Curr .Pharm. Des. 2009; 15 (24): 2769–2777.
  91. Di Stefano R., Limbruno U., Barone D. Therapeutic angiogenesis of critical lower limb ischemia. Review of the literature and prospects of research on stem cells. Italian Heart J. Suppl. 2004; 5 (1): 1–13.
  92. Fadini G.P., Agostini C., Avogaro A. Autologous stem cell therapy for peripheral arterial disease meta-analysis and systematic review of the literature. Atherosclerosis. 2010; 209 (1): 10–17.
  93. Arai M., Misao Y., Nagai H., Kawasaki M., Nagashima K., Suzuki K., Tsuchiya K., Otsuka S., Uno Y., Takemura G., Nishigaki K., Minatoguchi S., Fujiwara H. Granulocyte colony-stimulating factor: a noninvasive regeneration therapy for treating atherosclerotic peripheral artery disease. Circ. J. 2006; 70: 1093–1098.
  94. Bartsch T., Brehm M., Zeus T., Strauer B.E. Autologous mononuclear stem cell transplantation in patients with peripheral occlusive arterial disease. J. Cardiovasc. Nurs. 2006; 21: 430–432.
  95. Walter D.H., Krankenberg H., Balzer J.O., Kalka C., Baumgartner I., Schlüter M., Tonn T., Seeger F., Dimmeler S., Lindhoff-Last E., Zeiher A.M. Intraarterial administration of bone marrow mononuclear cells in patients with critical limb ischemia: a randomized-start, placebo-controlled pilot trial (PROVASA). Circ. Cardiovasc. Interv. 2011; 4 (1): 26–37.
  96. Van Tongeren R.B., Hamming J.F., Fibbe W.E., Van Weel V., Frerichs S.J., Stiggelbout A.M., Van Bockel J.H., Lindeman J.H. Intramuscular or combined intramuscular/intra-arterial administration of bone marrow mononuclear cells: a clinical trial in patients with advanced limb ischemia. J. Cardiovasc. Surg. (Torino). 2008; 49: 51–58.
  97. Fadini G.P., Agostini C., Sartore S., Avogaro A. Endothelial progenitor cells in the natural history of atherosclerosis. Atherosclerosis. 2007; 194: 46–54.
  98. Lawall H., Bramlage P., Amann B. Treatment of peripheral arterial disease using stem and progenitor cell therapy. J. Vasc. Surg. 2011; 53 (2): 445–453.
  99. Kudo F.A, Nishibe T., Nishibe M., Yasuda K. Autologous transplantation of peripheral blood endothelial progenitor cells (CD34+) for therapeutic angiogenesis in patients with critical limb ischemia. Int. Angiol. 2003; 22: 344–348.
  100. Cañizo M.C., Lozano F., González-Porras J.R., Barros M., López-Holgado N., Briz E., Sánchez-Guijo F.M. Peripheral endothelial progenitor cells (CD133+) for therapeutic vasculogenesis in a patient with critical limb ischemia (One year follow-up). Cytotherapy. 2007; 9: 99–102.
  101. Van Royen N., Schirmer S.H., Atasever B., Behrens C.Y., Ubbink D., Buschmann E.E., Voskuil M., Bot P., Hoefer I., Schlingemann R.O., Biemond B.J., Tijssen J.G., Bode C., Schaper W., Oskam J., Legemate D.A., Piek J.J., Buschmann I. START Trial: a pilot study on stimulation of arteriogenesis using subcutaneous application of granulocytemacrophage colony-stimulating factor as a new treatment for peripheral vascular disease. Circulation. 2005; 112: 1040–1046.
  102. Powell R.J., Comerota A.J., Berceli S.A., Guzman R., Henry T.D., Tzeng E., Velazquez O., Marston W.A., Bartel R.L., Longcore A., Stern T., Watling S. Interim analysis results from the RESTORE-CLI, a randomized, double-blind multicenter phase II trial comparing expanded autologous bone marrow-derived tissue repair cells and placebo in patients with critical limb ischemia. J. Vasc. Surg. 2011; 54 (4): 1032–1041.
  103. Arai M., Misao Y., Nagai H., Sogawa Y., Suwabe T., Higa Y., Nakanishi S., Sawa N., Katori H., Takemoto F., Fujimoto Y., Ohta E., Ohara K., Takaichi K.. Quality of life improvement and longterm effects of peripheral blood mononuclear cell transplantation for severe arteriosclerosis obliterans in diabetic patients on dialysis. Circ. J. 2007; 71: 1193–1198.
  104. Hirsch A.T. Critical limb ischemia and stem cell research: anchoring hope with Informed adverse event reporting. Circulation. 2006; 114: 2581–2583.
  105. Miyamoto K., Nishigami K., Nagaya N., Akutsu K., Chiku M., Kamei M., Soma T., Miyata S., Higashi M., Tanaka R., Nakatani T., Nonogi H., Takeshita S. Unblinded pilot study of autologous transplantation of bone marrow mononuclear cells in patients with thromboangiitis obliterans. Circulation. 2006; 114: 2679–2684.
  106. Fadini G.P., Sartore S., Albiero M., Baesso I., Murphy E., Menegolo M., Grego F., Vigili de Kreutzenberg S., Tiengo A., Agostini C., Avogaro A. Number and function of endothelial progenitor cells as a marker of severity for diabetic vasculopathy. Arterioscler. Thromb. Vasc. Biol. 2006; 26: 2140–2146.
  107. Vasa M., Fichtlscherer S., Aicher A., Adler K., Urbich C., Martin H., Zeiher A.M., Dimmeler S. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ. Res. 2001; 89: 1–7.
  108. Heeschen C., Lehmann R., Honold J., Assmus B., Aicher A., Walter D.H., Martin H., Zeiher A.M., Dimmeler S. Profoundly reduced neovascularization capacity of bone marrow mononuclear cells derived from patients with chronic ischemic heart disease. Circulation. 2004; 109: 1615–1622.
  109. Chen F., Tan Z., Dong C. Y., Li X., Xie Y., Wu Y., Chen X., Guo S. Combination of VEGF(165)/Angiopoietin-1 gene and endothelial progenitor cells for therapeutic neovascularization. Eur. J. Pharmacol. 2007; 568: 222–230.
  110. Bivalacqua T.J., Deng W., Kendirci M., Usta M.F., Robinson C., Taylor B.K., Murthy S.N., Champion H.C., Hellstrom W.J., Kadowitz P.J. Mesenchymal stem cells alone or ex vivo gene-modified with endothelial nitric oxide synthase reverse age-associated erectile disfunction. Am. J. Physiol. Heart. Circ. Physiol. 2007; 292: 1278–1290.
  111. Kurozumi K., Nakamura K., Tamiya T., Kawano Y., Ishii K., Kobune M., Hirai S., Uchida H., Sasaki K., Ito Y., Kato K., Honmou O., Houkin K., Date I., Hamada H. Mesenchymal stem cells that produce neurotrophic factors reduce ischemic damage in the rat middle cerebral artery occlusion model. Mol. Ther. 2005; 11: 96–104.
  112. Sasaki K., Heeschen C., Aicher A., Ziebart T., Honold J., Urbich C., Rossig L., Koehl U., Koyanagi M., Mohamed A., Brandes R.P., Martin H., Zeiher A.M., Dimmeler S. Ex vivo pretreatment of bone marrow mononuclear cells with endothelial NO synthase enhancer AVE9488 enhances their functional activity for cell therapy. Proc. Natl. Acad. Sci. USA. 2006; 103: 14537–14541.

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