Hypoxic preconditioning enhances angiogenic potential of bone marrow cells with aging-related functional impairment

Circulation Journal

Volumn 76, Issue 4, 2012, Pages 986-994

  Kubo, Masayuki ^a   Li, Tao Sheng ^a,c   Kurazumi, Hiroshi ^a   Takemoto, Yoshihiro ^a   Ohshima, Mako ^a   Murata, Tomoaki ^b   Katsura, Shunsaku ^a   Morikage, Noriyasu ^a   Furutani, Akira ^a   Hamano, Kimikazu ^a  

^a YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b YAMAGUCHI UNIVERSITY   (Japan)

^c NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

Author keywords

Aging; Angiogenesis; Cell therapy; Hypoxia; Preconditioning

Indexed keywords

CD34 ANTIGEN; PROTEIN P53; STEM CELL FACTOR RECEPTOR; TELOMERASE; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN;

AGING; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOLOGOUS BONE MARROW TRANSPLANTATION; BLOOD FLOW; BONE MARROW CELL; CAPILLARY DENSITY; CELL ADHESION; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HISTOLOGY; HYPOXIC PRECONDITIONING; LEG ISCHEMIA; MALE; MICROVASCULATURE; MOUSE; NONHUMAN; TELOMERIC REPEAT AMPLIFICATION PROTOCOL; WESTERN BLOTTING;

AGE FACTORS; AGING; ANIMALS; ANTIGENS, CD34; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CELL ADHESION; CELL HYPOXIA; CELL SURVIVAL; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HINDLIMB; ISCHEMIA; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-KIT; TELOMERASE; TUMOR SUPPRESSOR PROTEIN P53; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84858975753     PISSN: 13469843     EISSN: 13474820     Source Type: Journal    
DOI: 10.1253/circj.CJ-11-0605     Document Type: Article

References (37)

1. Hamano K, Nishida M, Hirata K, Mikamo A, Li TS, Harada M, et al. Local implantation of autologous bone marrow cells for therapeutic angiogenesis in patients with ischemic heart disease: Clinical trial and preliminary results. Jpn Circ J 2001; 65: 845-847.
2. Li TS, Murakami M, Kobayashi T, Shirasawa B, Mikamo A, Hamano K. Long-term efficacy and safety of the intramyocardial implantation of autologous bone marrow cells for the treatment of ischemic heart disease. J Thorac Cardiovasc Surg 2007; 134: 1347-1349.
3. Lunde K, Solheim S, Aakhus S, Arnesen H, Abdelnoor M, Egeland T, et al. Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. N Engl J Med 2006; 355: 1199-1209.
4. Schachinger V, Erbs S, Elsasser A, Haberbosch W, Hambrecht R, Holschermann H, et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med 2006; 355: 1210-1221.
5. Iwaguro H, Yamaguchi J, Kalka C, Murasawa S, Masuda H, Hayashi S, et al. Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation 2002; 105: 732-738.
6. Mangi AA, Noiseux N, Kong D, He H, Rezvani M, Ingwall JS, et al. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat Med 2003; 9: 1195-1201.
7. Zhang D, Fan GC, Zhou X, Zhao T, Pasha Z, Xu M, et al. Overexpression of CXCR4 on mesenchymal stem cells augments myoangiogenesis in the infarcted myocardium. J Mol Cell Cardiol 2008; 44: 281-292.
8. Das H, Abdulhameed N, Joseph M, Sakthivel R, Mao HQ, Pompili VJ. Ex vivo nanofiber expansion and genetic modification of human cord blood-derived progenitor/stem cells enhances vasculogenesis. Cell Transplant 2009; 18: 305-318.
9. Schlechta B, Wiedemann D, Kittinger C, Jandrositz A, Bonaros NE, Huber JC, et al. Ex-vivo expanded umbilical cord blood stem cells retain capacity for myocardial regeneration. Circ J 2010; 74: 188-194.
10. Shumiya T, Shibata R, Shimizu Y, Ishii M, Kubota R, Shintani S, et al. Evidence for the therapeutic potential of ex vivo expanded human endothelial progenitor cells using autologous serum. Circ J 2010; 74: 1006-1013.
11. Li TS, Hamano K, Suzuki K, Ito H, Zempo N, Matsuzaki M. Improved angiogenic potency by implantation of ex vivo hypoxia prestimulated bone marrow cells in rats. Am J Physiol Heart Circ Physiol 2002; 283: H468-H473.
12. Kubo M, Li TS, Suzuki R, Shirasawa B, Morikage N, Ohshima M, et al. Hypoxic preconditioning increases survival and angiogenic potency of peripheral blood mononuclear cells via oxidative stress resistance. Am J Physiol Heart Circ Physiol 2008; 294: H590-H595.
13. Kubo M, Li TS, Kamota T, Ohshima M, Qin SL, Hamano K. Increased expression of CXCR4 and integrin αM in hypoxia-preconditioned cells contributes to improved cell retention and angiogenic potency. J Cell Physiol 2009; 220: 508-514.
14. Akita T, Murohara T, Ikeda H, Sasaki K, Shimada T, Egami K, et al. Hypoxic preconditioning augments efficacy of human endothelial progenitor cells for therapeutic neovascularization. Lab Invest 2003; 83: 65-73.
15. Uemura R, Xu M, Ahmad N, Ashraf M. Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling. Circ Res 2006; 98: 1414-1421.
16. Hu X, Yu SP, Fraser JL, Lu Z, Ogle ME, Wang JA, et al. Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. J Thorac Cardiovasc Surg 2008; 135: 799-808.
17. Rosova I, Dao M, Capoccia B, Link D, Nolta JA. Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells 2008; 26: 2173-2182.
18. Tang YL, Zhu W, Cheng M, Chen L, Zhang J, Sun T, et al. Hypoxic preconditioning enhances the benefit of cardiac progenitor cell therapy for treatment of myocardial infarction by inducing CXCR4 expression. Circ Res 2009; 104: 1209-1216.
19. Li TS, Kubo M, Ueda K, Murakami M, Ohshima M, Kobayashi T, et al. Identification of risk factors related to poor angiogenic potency of bone marrow cells from different patients. Circulation 2009; 120: S255-S261.
20. Li TS, Kubo M, Ueda K, Murakami M, Mikamo A, Hamano K. Impaired angiogenic potency of bone marrow cells from patients with advanced age, anemia, and renal failure. J Thorac Cardiovasc Surg 2010; 139: 459-465.
21. Ballard VL, Edelberg JM. Stem cells and the regeneration of the aging cardiovascular system. Circ Res 2007; 100: 1116-1127.
22. Dimmeler S, Leri A. Aging and disease as modifiers of efficacy of cell therapy. Circ Res 2008; 102: 1319-1330.
23. Edelberg JM, Tang L, Hattori K, Lyden D, Rafii S. Young adult bone marrow-derived endothelial precursor cells restore aging-impaired cardiac angiogenic function. Circ Res 2002; 90: E89-E93.
24. Zhang H, Fazel S, Tian H, Mickle DA, Weisel RD, Fujii T, et al. Increasing donor age adversely impacts beneficial effects of bone marrow but not smooth muscle myocardial cell therapy. Am J Physiol Heart Circ Physiol 2005; 289: H2089-H2096.
25. Sugihara S, Yamamoto Y, Matsuura T, Narazaki G, Yamasaki A, Igawa G, et al. Age-related BM-MNC dysfunction hampers neovascularization. Mech Ageing Dev 2007; 128: 511-516.
26. Ebrahimian TG, Heymes C, You D, Blanc-Brude O, Mees B, Waeckel L, et al. NADPH oxidase-derived overproduction of reactive oxygen species impairs postischemic neovascularization in mice with type 1 diabetes. Am J Pathol 2006; 169: 719-728.
27. Ohshima M, Li TS, Kubo M, Qin SL, Hamano K. Antioxidant therapy attenuates diabetes-related impairment of bone marrow stem cells. Circ J 2009; 73: 162-166.
28. Walter DH, Haendeler J, Reinhold J, Rochwalsky U, Seeger F, Honold J, et al. Impaired CXCR4 signaling contributes to the reduced neovascularization capacity of endothelial progenitor cells from patients with coronary artery disease. Circ Res 2005; 97: 1142-1151.
29. Bosch-Marce M, Okuyama H, Wesley JB, Sarkar K, Kimura H, Liu YV, et al. Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia. Circ Res 2007; 101: 1310-1318.
30. Kubo M, Li TS, Suzuki R, Ohshima M, Qin SL, Hamano K. Shortterm pretreatment with low-dose hydrogen peroxide enhances the efficacy of bone marrow cells for therapeutic angiogenesis. Am J Physiol Heart Circ Physiol 2007; 292: H2582-H2588.
31. Li TS, Marban E. Physiological levels of reactive oxygen species are required to maintain genomic stability in stem cells. Stem Cells 2010; 28: 1178-1185.
32. Li TS, Cheng K, Malliaras K, Matsushita N, Sun B, Marban L, et al. Expansion of human cardiac stem cells in physiological oxygen improves cell production efficiency and potency for myocardial repair. Cardiovasc Res 2011; 89: 157-165.
33. Ivanovic Z. Hypoxia or in situ normoxia: The stem cell paradigm. J Cell Physiol 2009; 219: 271-275.
34. Pasha Z, Wang Y, Sheikh R, Zhang D, Zhao T, Ashraf M. Preconditioning enhances cell survival and differentiation of stem cells during transplantation in infarcted myocardium. Cardiovasc Res 2008; 77: 134-142.
35. Lu G, Haider HK, Jiang S, Ashraf M. Sca-1+ stem cell survival and engraftment in the infarcted heart: Dual role for preconditioninginduced connexin-43. Circulation 2009; 119: 2587-2596.
36. Hahn JY, Cho HJ, Kang HJ, Kim TS, Kim MH, Chung JH, et al. Pretreatment of mesenchymal stem cells with a combination of growth factors enhances gap junction formation, cytoprotective effect on cardiomyocytes, and therapeutic efficacy for myocardial infarction. J Am Coll Cardiol 2008; 51: 933-943.
37. Takahashi M, Li TS, Suzuki R, Kobayashi T, Ito H, Ikeda Y, et al. Cytokines produced by bone marrow cells can contribute to functional improvement of the infarcted heart by protecting cardiomyocytes from ischemic injury. Am J Physiol Heart Circ Physiol 2006; 291: H886-H893.