The effect of age on osteogenic, adipogenic and proliferative potential of female adipose-derived stem cells

Journal of Tissue Engineering and Regenerative Medicine

Volumn 3, Issue 4, 2009, Pages 290-301

  Zhu, Min ^a   Kohan, Emil ^b   Bradley, James ^b   Hedrick, Marc ^a   Benhaim, Prosper ^b   Zuk, Patricia ^b  

^a Cytori Therapeutics Inc   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adipogenic potential; Adipose tissue; Adipose derived stem cells; Osteogenic potential; Proliferative potential; Stem cells

Indexed keywords

BONE; CELL CULTURE; CELL ENGINEERING; CELL GROWTH; CELL PROLIFERATION; GROWTH KINETICS; TISSUE REGENERATION;

ADIPOGENIC; ADIPOGENIC POTENTIAL; ADIPOSE DERIVED STEM CELLS; ADIPOSE TISSUE; HUMAN ADIPOSE TISSUE; OSTEOGENIC; OSTEOGENIC POTENTIAL; PROLIFERATIVE POTENTIAL; STEM-CELL; TISSUES ENGINEERINGS;

STEM CELLS;

ADIPOGENESIS; ADIPOSE DERIVED STEM CELL; ADIPOSE TISSUE CELL; AGE; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL FUNCTION; CELL GROWTH; CELL ISOLATION; CELL KINETICS; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; LIPOSUCTION; PRIORITY JOURNAL; STEM CELL; ADIPOSE TISSUE; ADULT; BONE; CYTOLOGY; MIDDLE AGED;

ADIPOSE TISSUE; ADULT; AGE FACTORS; BONE AND BONES; CELL DIFFERENTIATION; CELL PROLIFERATION; FEMALE; HUMANS; MIDDLE AGED; OSTEOGENESIS; STEM CELLS;

EID: 67349107689     PISSN: 19326254     EISSN: 19327005     Source Type: Journal    
DOI: 10.1002/term.165     Document Type: Article

References (59)

1. Ankrom MA, Robey PG, Shapiro JR, et al. 1998; Age-related changes in human oestrogen receptor α function and levels in osteoblasts. Biochem J 333: 787-794.
2. Bailey AJ, Sims TJ, Ebbesen EN, et al. 1999; Age-related changes in the biochemical properties of human cancellous bone collagen: relationship to bone strength. Calcif Tiss Int 65: 203-210.
3. Beauśejour C. 2007; Bone marrow-derived cells: the influence of aging and cellular senescence. Handb Exp Pharmacol 180: 67-88.
4. Becerra J, Andrades JA, Ertl DC, et al. 1996; Demineralized bone matrix mediates differentiation of bone marrow stromal cells in vitro: effect of age of cell donor. J Bone Miner Res 11: 1073-1714.
5. Benayahu D, Kletter Y, Zipori D, et al. 1989; Bone-marrow derived stromal cell line expressing osteoblast phenotype in vitro and osteogenic capacity in vivo. J Cell Physiol 140: 1-7.
6. Beresford JN, Bennett JH, Devlin C, et al. 1992; Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. J Cell Sci 102: 341-351.
7. Bergman RJ, Gazit D, Kahn AJ, et al. 1996; Age-related changes in osteogenic stem cells in mice. J BoneMiner Res 11: 568-577.
8. Berry L, Grant ME, McClure J, et al. 1992; Bone-marrow-derived chondrogenesis in vitro. J Cell Sci 101: 333-342.
9. Bruder SP, Jaiswal N, Haynesworth SE. 1997; Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J Cell Biochem 64: 278-294.
10. Bruder SP, Jaiswal N, Ricalton NS, et al. 1998; Mesenchymal stem cells in osteobiology and applied bone regeneration. Clin Orthop S247-256.
11. Cartwright MJ, Tchkonia T, Kirkland JL. 2007; Aging in adipocytes: potential impact of inherent, depot-specific mechanisms. Exp Gerontol 42: 463-471.
12. Chen X, Hausman DB, Dean RG, et al. 1997; Differentiationdependent expression of obese (ob) gene by preadipocytes and adipocytes in primary cultures of porcine stromal-vascular cells. Biochim Biophys Acta 1359: 136-142.
13. Conejero JA, Lee JA, Parrett BM, et al. 2006; Repair of palatal bone defects using osteogenically differentiated fat-derived stem cells. Plast Reconstr Surg 117: 857-863.
14. Djian P, Roncari AK, Hollenberg CH. 1983; Influence of anatomic site and age on the replication and differentiation of rat adipocyte precursors in culture. J Clin Invest 72: 1200-1208.
15. D'Ippolito G, Schiller PC, Ricordi C, et al. 1999; Age-related osteogenic potential of mesenchymal stromal stem cells from human vertebral bone marrow. J Bone Miner Res 14: 1115-1122.
16. Fehrer C, Lepperdinger G. 2005; Mesenchymal stem cell aging. Exp Gerontol 40: 926-930.
17. Ferrari G, Cusella-De Angelis G, Coletta M, et al. 1998; Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279: 1528-1530.
18. Gazit D, Zilberman Y, Ebner R, et al. 1998; Bone loss (osteopenia) in old male mice results from diminished activity and availability of TGF-β. J Cell Biochem 70: 478-488.
19. Glowacki J. 1995; Influence of age on human marrow. Calcif Tiss Int 56S1: S50-51.
20. Grigoradis A, Heersche JNM, Aubin J. 1988; Differentiation of muscle fat, cartilage and bone from progenitor cells present in a bone-derived clonal cell population: effect of dexamethasone. J Cell Biol 106: 2139-2151.
21. Hahn TJ. 1993; Metabolic bone disease. In Textbook of Rheumatology, Kelly WN, Harris ED, Ruddy S, et al. (eds). W. B. Saunders: New York; 1593-1627.
22. Hauner H, Schmid P, Pfeiffer EF. 1987; Glucocorticoids and insulin promote the differentiation of human adipocyte precursor cells into fat cells. J Clin Endocrinol Metabol 64: 832-835.
23. Hauner H, Entenmann G, Wabitsh CM, et al. 1989; Promoting effect of glucocorticoids on the differentiation of fhuman adipocyte precursor cells cultured in a chemically defined medium. J Clin Invest 84: 1663-1670.
24. He XZ, Baker DW. 2004; Changes in weight among a nationally representative cohort of adults aged 51 to 61, 1992 to 2000. Am J Prev Med 27: 8-15.
25. Hicok KC, Du Laney TV, Zhou YS, et al. 2004; Human adiposederived adult stem cells produce osteoid in vivo. Tissue Eng 10: 371-380.
26. Huibregtse BA, Johnstone B, Goldberg VM, et al. 2000; Effect of age and sampling site on the chondro-osteogenic potential of rabbit marrow-derived mesenchymal progenitor cells. J Orthop Res 18: 18-24.
27. JaiswalN, Haynesworth SE, Caplan AI, et al. 1997; Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 64: 295-312.
28. Johnstone B, Hering TM, Caplan AI, et al. 1998; In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 238: 265-272.
29. Johnstone B, Yoo JU. 1999; Autologous mesenchymal progenitor cells in articular cartilage repair. Clin Orthop Relat Res S156-162.
30. Justesen J, Pedersen SB, Stenderup K, et al. 2004; Subcutaneous adipocytes can differentiate into bone-forming cells in vitro and in vivo. Tissue Eng 10: 381-391.
31. Karagiannides I, Tchkonia T, Dobson DE, et al. 2001; Altered expression of C/EBP family members results in decreased adipogenesis with aging. Am J Physiol Regul Integr Comp Physiol 280: R1772-1780.
32. Khan WS, Adesida AB, Tew SR, et al. 2008; The epitope characterisation and the osteogenic differentiation potential of human fat pad-derived stem cells is maintained with ageing in later life, Injury (in press).
33. Kirkland JL, Dax EM. 1984; Adipose hormone responsiveness and aging in the rat. J Am Geriatr Soc 32: 219-228.
34. Kirkland JL, Hollenberg CH, Gillon WS. 1990; Age, anatomic site, and the replication and differentiation of adipocyte precursors. Am J Physiol. 258(2, pt 1): C206-210.
35. Kirkland JL, Hollenberg CH, Kindler S, et al. 1994; Effects of age and anatomic site on preadipocyte number in rat fat depots. J Gerontol 49: B31-35.
36. Kirkland JL, Dobson DE. 1997; Preadipocyte function and aging: links between age-related changes in cell dynamics and altered fat cell function. J Am Geriatr Soc 45: 959-967.
37. Kirkland JL, Tchkonia T, Pirtskhalava T, et al. 2002; Adipogenesis and aging: does aging make fat go MAD? Exp Gerontol 37: 757-767.
38. Krebsbach PH, Kuznetsor SA, Satomura K, et al. 1997; Bone formation in vivo: comparision of osteogenesis by transplanted mouse and human marrow stromal fibroblasts. Transplantation 63: 1059-1069.
39. Lansdorp PM, Gragowska W, Thomas TE, et al. 1994; Age-related decline in proliferative potential of purified stem cell candidates. Blood Cells 20: 376-380.
40. Lei L, Liao W, Sheng P, et al. 2007; Biological character of human adipose-derived adult stem cells and influence of donor age on cell replication in culture. Sci China C Life Sci 50: 320-328.
41. Long MW, Ashcraft EK, Normalle D, et al. 1999; Age-related phenotypic alterations in populations of purified human bone precursor cells. J Gerontol A Biol Sci Med Sci 54: B54-62.
42. Majors AK, BoehmCA, NittoH, et al. 1997; Characterization of human bone marrow stromal cells with respect to osteoblastic differentiation. J Orthop Res 15: 546-557.
43. Oreffo RO, Bord S, Triffit JT. 1998; Skeletal progenitor cells and aging human populations. Clin Sci (Lond) 94: 549-555.
44. Owen ME, Cave J, Joyner CJ. 1987; Clonal analysis in vitro of osteogenic differentiation of marrow CFU-F. J Cell Sci 87: 731-738.
45. Parfitt AM. 1990; Bone forming cells in clinical conditions. In Bone, vol 1, Hall BK (ed.). Telford Press: Caldwell, NJ; 351-431.
46. Pittenger MF, Mackay AM, Beck SC, et al. 1999; Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147.
47. Proenza AM, Poissonnet CM, Ozata M, et al. 2000; Association of sets of alleles of genes encoding β3-adrenoreceptor, uncoupling protein 1 and lipoprotein lipase with increased risk of metabolic complication in obesity. Int J Obes Rel Metab Disord 24: 93-100.
48. Rao MS, Mattson MP. 2001; Stem cells and aging: expanding the possibilities. Mech Ageing Dev 122: 713-734.
49. Rickard DJ, Kassem M, Hefferan TE, et al. 1996; Isolation and characterization of osteoblast precursor cells from human bone marrow. J Bone Miner Res 11: 312-324.
50. Robinson JA, Harris SA, Riggs BL, et al. 1997; Estrogen regulation of human osteoblastic cell proliferation and differentiation. Endocrinology 138: 2919-2917.
51. Schipper BM, Marra KG, Zhang W, et al. 2008; Regional anatomic and age effects on cell function of human adipose-derived stem cells. Ann Plast Surg 60: 538-544.
52. Shi YY, Nacamuli RP, Salim A, et al. 2005; The osteogenic potential of adipose-derived mesenchymal cells is maintained with aging, Plast Reconstr Surg 116: 1686-1696.
53. Sethe S, Scutt A, Stolzing A. 2006; Aging of mesenchymal stem cells. Ageing Res Rev 5: 91-116.
54. Van Harmelen V, Skurk T, Hauner H. 2004; Primary culture and differentiation of human adipocyte precursor cells. Methods Mol Med 107: 125-135.
55. Van Zant G. 2003; Genetic control of stem cells: implications for aging. Int J Hematol 77: 29-36.
56. Wakitani S, Saito T, Caplan AI. 1995; Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve 18: 1417-1426.
57. Weinzierl K, Hemprich A, Frerich B. 2006; Bone engineering with adipose tissue derived stromal cells. J Craniomaxillofac Surg 34: 466-471.
58. Zuk PA, Zhu M, Ashjian P, et al. 2002; Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13: 4279-4295.
59. Zuk PA, Zhu M, Mizuno H, et al. 2001; Multi-lineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7: 211-228.