Telomere length, telomerase activity and osteogenic differentiation are maintained in adipose-derived stromal cells from senile osteoporotic SAMP6 mice

Journal of Tissue Engineering and Regenerative Medicine

Volumn 6, Issue 5, 2012, Pages 378-390

  Mirsaidi, Ali ^a   Kleinhans, Karin N ^b   Rimann, Markus ^a   Tiaden, André N ^a   Stauber, Martin ^c   Rudolph, K Lenhard ^b   Richards, Peter J ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF ULM   (Germany)

^c B cube AG   (Switzerland)

Author keywords

Adipose; Ageing; Differentiation; Mesenchymal stem cell; Osteoporosis

Indexed keywords

BONE; CHROMOSOMES; DISEASE CONTROL; DISEASES; MAMMALS; QUALITY CONTROL; STEM CELLS; STRAIN;

% REDUCTIONS; ADIPOSE; ADIPOSE TISSUE; ADIPOSE-DERIVED STROMAL CELLS; BONE QUALITY; DIFFERENTIATION; MESENCHYMAL STEM CELL; OSTEOPOROTIC; TELOMERASE ACTIVITY; TELOMERE LENGTH;

CELL CULTURE;

TELOMERASE;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; ENZYME ACTIVITY; LIVER; MOUSE; MOUSE STRAIN; NONHUMAN; OSTEOBLAST; OSTEOPOROSIS; PRIORITY JOURNAL; STROMA CELL; TELOMERE HOMEOSTASIS; TIBIA;

EID: 84859941981     PISSN: 19326254     EISSN: 19327005     Source Type: Journal    
DOI: 10.1002/term.440     Document Type: Article

References (56)

1. Baxter MA, Wynn RF, Jowitt SN, et al. 2004; Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 22: 675-682.
2. Beck GR Jr, Sullivan EC, Moran E, et al. 1998; Relationship between alkaline phosphatase levels, osteopontin expression, and mineralization in differentiating MC3T3-E1 osteoblasts. J Cell Biochem 68: 269-280.
3. Bonyadi M, Waldman SD, Liu D, et al. 2003; Mesenchymal progenitor self-renewal deficiency leads to age-dependent osteoporosis in Sca-1/Ly-6A null mice. Proc Natl Acad Sci USA 100: 5840-5845.
4. Bruder SP, Fink DJ, Caplan AI. 1994; Mesenchymal stem cells in bone development, bone repair, and skeletal regeneration therapy. J Cell Biochem 56: 283-294.
5. Chan SW, Blackburn EH. 2002; New ways not to make ends meet: telomerase, DNA damage proteins and heterochromatin. Oncogene 21: 553-63.
6. Chang S, Multani AS, Cabrera NG, et al. 2004; Essential role of limiting telomeres in the pathogenesis of Werner syndrome. Nat Genet 36: 877-882.
7. Choi Y, Wright AC, Johnson FB. 2008; Defects in telomere maintenance molecules impair osteoblast differentiation and promote osteoporosis. Aging Cell 7: 23-31
8. D'Ippolito G, Schiller PC, Ricordi C, et al. 1999; Age-related osteogenic potential of mesenchymal stem cells from human vertebral bone marrow. J Bone Miner Res 14: 1115-1122.
9. Dudas JR, Marra KG, Cooper GM, et al. 2006; The osteogenic potential of adipose-derived stem cells for the repair of rabbit calvarial defects. Ann Plast Surg 56: 543-548.
10. Egermann M, Heil P, Tami A, et al. 2010; Influence of defective bone marrow osteogenesis on fracture repair in an experimental model of senile osteoporosis. J Orthop Res 28: 798-804.
11. Gimble JM. 2003; Adipose tissue-derived therapeutics. Expert Opin Biol Ther 3: 705-713.
12. Halvorsen YC, Wilkison WO, Gimble JM. 2000; Adipose-derived stromal cells-their utility and potential in bone formation. Int J Obes Relat Metab Disord 24(suppl 4): S41-44.
13. Halvorsen YD, Franklin D, Bond AL, et al. 2001; Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng 7: 729-741.
14. Helder MN, Knippenberg M, Klein-Nulend J, et al. 2007; Stem cells from adipose tissue allow challenging new concepts for regenerative medicine. Tissue Eng 13: 1799-1808.
15. Hicok KC, Du Laney TV, Zhou YS, et al. 2004; Human adipose-derived adult stem cells produce osteoid in vivo. Tissue Eng 10: 371-380.
16. Hildebrand T, Laib A, Müller R, et al. 1999; Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res 14: 1167-1174.
17. Izadpanah R, Trygg C, Patel B, et al. 2006; Biologic properties of mesenchymal stem cells derived from bone marrow and adipose tissue. J Cell Biochem 99: 1285-1297.
18. Jilka RL, Weinstein RS, Takahashi K, et al. 1996; Linkage of decreased bone mass with impaired osteoblastogenesis in a murine model of accelerated senescence. J Clin Invest 97: 1732-1740.
19. Justesen J, Pedersen SB, Stenderup K, Kassem M. 2004; Subcutaneous adipocytes can differentiate into bone-forming cells in vitro and in vivo. Tissue Eng 10: 381-391.
20. Kang SK, Putnam L, Dufour J, et al. 2004; Expression of telomerase extends the lifespan and enhances osteogenic differentiation of adipose tissue-derived stromal cells. Stem Cells 22: 1356-1372.
21. Kawaguchi H, Manabe N, Miyaura C, et al. 1999; Independent impairment of osteoblast and osteoclast differentiation in klotho mouse exhibiting low-turnover osteopenia. J Clin Invest 104: 229-237.
22. Khan WS, Adesida AB, Tew SR, et al. 2009; The epitope characterization and the osteogenic differentiation potential of human fat pad-derived stem cells is maintained with ageing in later life. Injury 40: 150-157.
23. Kojima H, Uede T, Uemura T. 2004; In vitro and in vivo effects of the overexpression of osteopontin on osteoblast differentiation using a recombinant adenoviral vector. J Biochem 136: 377-386.
24. Kuro-o M, Matsumura Y, Aizawa H, et al. 1997; Mutation of the mouse klotho gene leads to a syndrome resembling aging. Nature 390: 45-51.
25. Lane NE. 2006; Epidemiology, etiology, and diagnosis of osteoporosis. Am J Obstet Gynecol 194(2, suppl): S3-11.
26. Li H, Dai K, Tang T, Zhang X, et al. 2007; Bone regeneration by implantation of adipose-derived stromal cells expressing BMP-2. Biochem Biophys Res Commun 356: 836-842.
27. Lu L, DiGirolamo CM, Navarro PAA, et al. 2004; Telomerase deficiency impairs differentiation of mesenchymal stem cells. Exp Cell Res 294: 1-8.
28. Matsushita M, Tsuboyama T, Kasai R, et al. 1986; Age-related changes in bone mass in the senescence-accelerated mouse (SAM), SAM-R/3 and SAM-P/6 as new murine models for senile osteoporosis. Am J Pathol 125: 276-283.
29. Mesimäki K, Lindroos B, Törnwall J, et al. 2009; Novel maxillary reconstruction with ectopic bone formation by GMP adipose stem cells. Int J Oral Maxillofac Surg 38: 201-209.
30. Meunier P, Aaron J, Edouard C, et al. 1971; Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop Relat Res 80: 147-154.
31. Odgaard A. 1997; Three-dimensional methods for quantification of cancellous bone architecture. Bone 20: 315-328.
32. Pittenger MF, Mackay AM, Beck SC, et al. 1999; Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147.
33. Recker RR and Barger-Lux MJ. 2004; The elusive concept of bone quality. Curr Osteoporosis Rep 2: 97-100.
34. Rodríguez JP, Garat S, Gajardo H, et al. 1999; Abnormal osteogenesis in osteoporotic patients is reflected by altered mesenchymal stem cells dynamics. J Cell Biochem 75: 414-423.
35. Rodríguez JP, Montecinos L, Ríos S, et al. 2000; Mesenchymal stem cells from osteoporotic patients produce a type I collagen-deficient extracellular matrix favoring adipogenic differentiation. J Cell Biochem 79: 557-565.
36. + mesenchymal stem cells. Eur J Heart Fail 8: 555-563.
37. Sahin E and Depinho RA. 2010; Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature 464: 520-528.
38. Satyanarayana A, Wiemann SU, Buer J, et al. 2003; Telomere shortening impairs organ regeneration by inhibiting cell cycle re-entry of a subpopulation of cells. EMBO J 22: 4003-4013.
39. Schäffler A and Büchler C. 2007; Concise review: adipose tissue-derived stromal cells-basic and clinical implications for novel cell-based therapies. Stem Cells 25: 818-827.
40. 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
41. Seeman E and Delmas PD. 2006; Bone quality-the material and structural basis of bone strength and fragility. N Engl J Med 354: 2250-2261.
42. 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.
43. Silva MJ, Brodt MD, Ettner SL. 2002; Long bones from the senescence accelerated mouse SAMP6 have increased size but reduced whole-bone strength and resistance to fracture. J Bone Miner Res 17: 1597-1603.
44. Silva MJ, Brodt MD, Ko M, et al. 2005; Impaired marrow osteogenesis is associated with reduced endocortical bone formation but does not impair periosteal bone formation in long bones of SAMP6 mice. J Bone Miner Res 20: 419-427.
45. Simonsen JL, Rosada C, Serakinci N, et al. 2002; Telomerase expression extends the proliferative life-span and maintains the osteogenic potential of human bone marrow stromal cells. Nat Biotechnol 20: 592-596.
46. Stenderup K, Justesen J, Clausen C, et al. 2003; Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33: 919-926.
47. Stolzing A, Jones E, McGonagle D, et al. 2008; Age-related changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mech Ageing Dev 129: 163-173.
48. Suzuki H, Amizuka N, Oda K, et al. 2005; Histological evidences on altered distribution of osteocytes and bone matrix synthesis in klotho-deficient mice. Arch Histol Cytol 68: 371-381.
49. Takeda T. 1999; Senescence-accelerated mouse (SAM): a biogerontological resource in aging research. Neurobiol Aging 20: 105-110.
50. Tapp H, Hanley JR EN, Patt JC, et al. 2009; Adipose-derived stem cells: characterization and current application in orthopaedic tissue repair. Exp Biol Med 234: 1-9.
51. Weinzierl K, Hemprich A, Frerich B. 2006; Bone engineering with adipose tissue derived stromal cells. J Craniomaxillofac Surg 34: 466-471.
52. Wiemann SU, Satyanarayana A, Tsahuridu M, et al. 2002; Hepatocyte telomere shortening and senescence are general markers of human liver cirrhosis. FASEB J 16: 935-942.
53. Yoon E, Dhar S, Chun DE, et al. 2007; In vivo osteogenic potential of human adipose-derived stem cells/polylactide-co-glycolic acid constructs for bone regeneration in a rat critical-sized calvarial defect model. Tissue Eng 13: 619-627.
54. Yu JM, Wu X, Gimble JM, et al., 2011; Age-related changes in mesenchymal stem cells derived from rhesus macaque bone marrow. Aging Cell 10: 66-79.
55. Zhu M, Kohan E, Bradley J, et al. 2009; The effect of age on osteogenic, adipogenic and proliferative potential of female adipose-derived stem cells. J Tissue Eng Regen Med 3: 290-301.
56. Zuk PA, Zhu M, Mizuno H, et al. 2001; Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7: 211-228.