Age effects on angiogenic properties of adipose tissue mesenchymal stem cells

Cellular Transplantation and Tissue Engineering

Volumn 6, Issue 3, 2011, Pages 48-57

  Efimenko, A Yu ^a   Starostina, E E ^a   Kalinina, N I ^a   Parfyenova, E V ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Adipose tissue mesenchymal stem cells; Ageing; Angiogenesis

Indexed keywords

EID: 84862989091     PISSN: 1815445X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (58)

1. Fehrer C., Lepperdinger G. Mesenchymal stem cell aging. Exp. Gerontol. 2005; 40: 926-30. (Pubitemid 41682392)
2. Sethe S., Scutt A., Stolzing A. Aging of mesenchymal stem cells. Ageing Res. Rev. 2006; 5: 91-116. (Pubitemid 43139669)
3. Stolzing A., Sethe S., Scutt A.M. Stressed stem cells: temperature response in aged mesenchymal stem cells. Stem Cells Dev. 2006; 15: 478-87. (Pubitemid 44701167)
4. Katsara O., Mahaira L.G., Iliopoulou E.G. et al. Effects of donor age, gender and in vitro cellular aging on the phenotype, functional and molecular characteristics of mouse bone marrow-derived mesenchymal stem cells. Stem Cells Dev. 2011; in press.
5. Sun Y., Li W., Lu Z. et al. Rescuing replication and osteogenesis of aged mesenchymal stem cells by exposure to a young extracellular matrix. FASEB 2011; 25(5): 1474-85.
6. Gimble J.M., Katz A.J., Bunnell B.A. Adipose-derived stem cells for regenerative medicine. Circ. Res. 2007; 100: 1249-60. (Pubitemid 46742916)
7. Planat-Benard V., Silvestre J.S., Cousin B. et al. Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 2004; 109: 656-63. (Pubitemid 38198874)
8. Rehman J., Traktuev D., Li J. et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 2004; 109: 1292-8. (Pubitemid 38372789)
9. Cao Y., Sun Z., Liao L. et al. Human adipose tissue-derived stem cells differentiate into endothelial cells in vitro and improve postnatal neovascularization in vivo. Biochem. Biophys. Res. Commun. 2005; 332: 370-9. (Pubitemid 40724988)
10. Moon M.H., Kim S.Y., Kim Y.J. et al. Human adipose tissuederived mesenchymal stem cells improve postnatal neovascularization in a mouse model of hindlimb ischemia. Cell Physiol. Biochem. 2006; 17: 279-90.
11. Nakagami H., Morishita R., Maeda K. et al. Adipose tissuederived stromal cells as a novel option for regenerative cell therapy. J. Atheroscler. Thromb. 2006; 13: 77-81.
12. Sumi M., Sata M., Toya N. et al. Transplantation of adipose stromal cells, but not mature adipocytes, augments ischemia-induced angiogenesis. Life Sci. 2007; 80: 559-65. (Pubitemid 46038328)
13. Kondo K., Shintani S., Shibata R. et al. Implantation of adiposederived regenerative cells enhances ischemia-induced angiogenesis. Arterioscler. Thromb. Vasc. Biol. 2009; 29: 61-6.
14. Miyahara Y., Nagaya N., Kataoka M. et al. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat. Med. 2006; 12: 459-65.
15. Yamada Y., Wang X.D., Yokoyama S. et al. Cardiac progenitor cells in brown adipose tissue repaired damaged myocardium. Biochem. Biophys. Res. Commun. 2006; 342: 662-70. (Pubitemid 43289041)
16. Valina C., Pinkernell K., Song, Y.H. et al. Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction. Eur. Heart J. 2007; 28: 2667-77. (Pubitemid 350071533)
17. Li B., Zeng Q., Wang H. et al. Adipose tissue stromal cells transplantation in rats of acute myocardial infarction. Coron. Artery Dis. 2007; 18: 221-7. (Pubitemid 46608501)
18. Zhang D.Z., Gai L.Y., Liu H.W. et al. Transplantation of autologous adipose-derived stem cells ameliorates cardiac function in rabbits with myocardial infarction. Chin. Med. J. 2007; 120: 300-7.
19. Mazo M., Planat-Benard V., Abizanda G. et al. Transplantation of adipose derived stromal cells is associated with functional improvement in a rat model of chronic myocardial infarction. Eur. J. Heart Fail. 2008; 10: 454-62.
20. Schenke-Layland K., Strem B.M., Jordan M.C. et al. Adipose tissue-derived cells improve cardiac function following myocardial infarction. J. Surg. Res. 2009; 153: 217-23.
21. Cai L., Johnstone B.H., Cook T.G. et al. IFATS collection: human adipose tissue-derived stem cells induce angiogenesis and nerve sprouting following myocardial infarction, in conjunction with potent preservation of cardiac function. Stem Cells 2009; 27: 230-7.
22. Rubina K., Kalinina N., Efimenko A. et al. Adipose stromal cells stimulate angiogenesis via promoting progenitor cell differentiation, secretion of angiogenic factors, and enhancing vessel maturation. Tissue Eng. Part A. 2009; 15: 2039-50.
23. Madonna R., De Caterina R. Adipose tissue: a new source for cardiovascular repair. J. Cardiovasc. Med. 2010; 11: 71-80.
24. Rangappa S., Fen C., Lee E.H. et al. Transformation of adult mesenchymal stem cells isolated from the fatty tissue into cardiomyocytes. Ann. Thorac. Surg. 2003; 75: 775-9. (Pubitemid 36298339)
25. Miranville A., Heeschen C., Sengenes C. et al. Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation 2004; 110: 349-55. (Pubitemid 38955505)
26. Madonna R., Cellini C., Renna F. et al. Age-dependent impairment of number and angiogenic potential of adipose tissuederived progenitor cells. Eur. Heart J. 2008; 29: 4301.
27. Zhu M., Kohan E., Bradley J. et al. The effect of age on osteogenic, adipogenic and proliferative potential of female adiposederived stem cells. J. Tissue Eng. Regen. Med. 2009; 3: 290-301.
28. Bujak M., Kweon H.J., Chatila K. et al. Aging-related defects are associated with adverse cardiac remodeling in a mouse model of reperfused myocardial infarction. J. Am. Coll. Cardiol. 2008; 51: 1384-92. (Pubitemid 351443080)
29. El-Ftesi S., Chang E.I., Longaker M.T. et al. Aging and diabetes impair the neovascular potential of adipose-derived stromal cells. Plast. Reconstr. Surg. 2009; 123: 475-85.
30. Huang S.C., Wu T.C., Yu H.C. et al. Mechanical strain modulates age-related changes in the proliferation and differentiation of mouse adipose-derived stromal cells. BMC Cell Biology 2010; 11: 18.
31. Thangarajah H., Vial I.N., Chang E. et al. IFATS Series: Adipose stromal cells adopt a proangiogenic phenotype under the influence of hypoxia. Stem Cells 2008; 27: 266-74.
32. Zuk P.A., Zhu M., Ashjian P. et al. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell. 2002; 13: 4279- 95. (Pubitemid 35471185)
33. Ohnishi S., Yasuda T., Kitamura S. et al. Effect of hypoxia on gene expression of bone marrow-derived mesenchymal stem cells and mononuclear cells. Stem Cells 2007; 25: 1166-77. (Pubitemid 46684876)
34. Potier E., Ferreira E., Andriamanalijaona R. et al. Hypoxia affects mesenchymal stromal cell osteogenic differentiation and angiogenic factor expression. Bone 2007; 40: 1078-87. (Pubitemid 46386551)
35. Efimenko A.Yu., Starostina E.E., Kalinina N.I. et al. Angiogenic properties of aged adipose derived mesenchymal stem cells after hypoxic conditioning. J. Transl. Med. 2011; 9: 10.
36. Flores I., Blasco M. A. The role of telomeres and telomerase in stem cell aging. FEBS Lett. 2010; 584: 3826-30.
37. Dasgupta J., Kar S., Liu R. et al. Reactive oxygen species control senescence-associated matrix metalloproteinase-1 through c-Jun-N-terminal kinase. J. Cell Physiol. 2010; 225: 52-62.
38. Baxter M.A., Wynn R.F., Jowitt S.N. et al. Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 2004; 22: 675-82. (Pubitemid 39172200)
39. Stolzing A., Jones E., McGonagle D. et al. Age-related changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mech. Ageing Dev. 2008; 129: 163-73.
40. de Girolamo L., Lopa S., Arrigoni E. et al. Human adiposederived stem cells isolated from young and elderly women: their differentiation potential and scaffold interaction during in vitro osteoblastic differentiation. Cytotherapy 2009; 11(6): 793-803.
41. Harris L.J., Zhang P., Abdollahi H. et al. Availability of adiposederived stem cells in patients undergoing vascular surgical procedures. J. Surg. Res. 2010; 163(2): 105-12.
42. van Harmelen V., Skurk T., Hauner H. Primary culture and differentiation of human adipocyte precursor cells. Methods Mol. Med. 2005; 107: 125-35.
43. Schipper B.M., Marra K.G., Zhang W. et al. Regional anatomic and age effects on cell function of human adipose-derived stem cells. Ann. Plast. Surg. 2008; 60: 538-44. (Pubitemid 351591463)
44. Khan W.S., Adesida A.B., Tew S.R., et al. The epitope characterisation and the osteogenic differentiation potential of human fat pad-derived stem cells is maintained with ageing in later life. Injury 2009; 40: 150-7.
45. Jiang S., Kh Haider H., Ahmed R.P. et al. Transcriptional profiling of young and old mesenchymal stem cells in response to oxygen deprivation and reparability of the infarcted myocardium. J. Mol. Cell Cardiol. 2008; 44: 582-96.
46. Wilson A., Shehadeh L.A., Yu H. et al. Age-related molecular genetic changes of murine bone marrow mesenchymal stem cells. BMC Genomics 2010; 11: 229.
47. Sadoun E., Reed M.J. Impaired angiogenesis in aging is associated with alterations in vessel density, matrix composition, inflammatory response, and growth factor expression. J. Histochem. Cytochem. 2003; 51: 1119-30. (Pubitemid 37059523)
48. Olson B.A., Day J.R., Laping N.J. Age-related expression of renal thrombospondin 1 mRNA in F344 rats: resemblance to diabetesinduced expression in obese Zucker rats. Pharmacology 1999; 58: 200-8. (Pubitemid 29118884)
49. Darbro B.W., Schneider G.B., Klingelhutz A.J. et al. Coregulation of p16INK4A and migratory genes in culture conditions that lead to premature senescence in human keratinocytes. J. Invest. Dermatol. 2005; 125(3): 499-509.
50. Kortlever R.M., Higgins P.J., Bernards R. Plasminogen activator inhibitor-1 is a critical downstream target of p53 in the induction of replicative senescence. Nat. Cell Biol. 2006; 8: 877-84.
51. Ghosh A.K., Bradham W.S., Gleaves L.A. et al. Genetic deficiency of plasminogen activator inhibitor-1 promotes cardiac fibrosis in aged mice: involvement of constitutive transforming growth factor-beta signaling and endothelial-to-mesenchymal transition. Circulation 2010; 122(12): 1200-9.
52. Cesari M., Pahor M., Incalzi R.A. et al. Plasminogen activator inhibitor-1 (PAI-1): a key factor linking fibrinolysis and age-related subclinical and clinical conditions. Cardiovasc. Ther. 2010; 28(5): 72-91.
53. Serrano R., Barrenetxe J., Orbe J. et al. Tissue-specific PAI-1 gene expression and glycosylation pattern in insulin-resistant old rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009; 297: 1563-9.
54. Wang S., Moerman E.J., Jones R.A. et al. Characterization of IGFBP-3, PAI-1 and SPARC mRNA expression in senescent fibroblasts. Mech. Ageing. Dev. 1996; 92: 121-32. (Pubitemid 27129284)
55. Stefansson S., Petitclerc E., Wong M. K. et al. Inhibition of angiogenesis in vivo by plasminogen activator inhibitor-1. J. Biol. Chem. 2000; 276: 8135-41.
56. Devy L., Blacher S., Debrus C.G. et al. The pro- or antiangiogenic effect of plasminogen activator inhibitor 1 is dose dependent. FASEB 2002; 16: 147-54. (Pubitemid 34113008)
57. Rivard A., Berthou-Soulie L., Principe N. et al. Age-dependent defect in vascular endothelial growth factor expression is associated with reduced hypoxia-inducible factor 1 activity. J. Biol. Chem. 2000; 275: 29643-7. (Pubitemid 32043844)
58. Ahluwalia A., Narula J., Jones M.K. et al. Impaired angiogenesis in aging myocardial microvascular endothelial cells is associated with reduced importin alpha and decreased nuclear transport of HIF1 alpha: mechanistic implications. J. Physiol. Pharmacol. 2010; 61(2): 133-9.