Donor variation and loss of multipotency during in vitro expansion of human mesenchymal stem cells for bone tissue engineering

Journal of Orthopaedic Research

Volumn 25, Issue 8, 2007, Pages 1029-1041

  Siddappa, Ramakrishnaiah ^a   Licht, Ruud ^a   van Blitterswijk, Clemens ^a   de Boer, Jan ^a  

^a UNIVERSITY OF TWENTE   (Netherlands)

Author keywords

Bone tissue engineering; Human mesenchymal stem cells

Indexed keywords

ALKALINE PHOSPHATASE; CALCIUM; CALVASCULIN; COLLAGEN TYPE 1; DEXAMETHASONE; OSTEOCALCIN;

ADULT; AGED; ANIMAL EXPERIMENT; ARTICLE; BONE TISSUE; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL ISOLATION; CELL MEMBRANE POTENTIAL; CONTROLLED STUDY; CORRELATION ANALYSIS; DONOR; GENE EXPRESSION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCHYMAL STEM CELL; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE ENGINEERING;

ACETABULUM; ADULT; AGED; AGED, 80 AND OVER; ALKALINE PHOSPHATASE; ANIMALS; BONE SUBSTITUTES; CELL DIFFERENTIATION; DEXAMETHASONE; FEMALE; GENE EXPRESSION PROFILING; HUMANS; ILIUM; MALE; MESENCHYMAL STEM CELLS; MICE; MIDDLE AGED; MULTIPOTENT STEM CELLS; OSTEOGENESIS; TISSUE DONORS; TISSUE ENGINEERING; VARIATION (GENETICS);

EID: 34447283203     PISSN: 07360266     EISSN: None     Source Type: Journal    
DOI: 10.1002/jor.20402     Document Type: Article

References (61)

1. Bauer TW, Muschler GF. 2000. Bone graft materials. An overview of the basic science. Clin Orthop Related Res 10-27.
2. Hill NM, Horne JG, Devane, PA. 1999. Donor site morbidity in the iliac crest bone graft. Aust N Z J Surg 69:726-728.
3. Seiler JG 3rd, Johnson J. 2000. Iliac crest autogenous bone grafting: donor site complications. J South Orthop Assoc 9:91-97.
4. Bruder SP, Fox BS. 1999. Tissue engineering of bone. Cell based strategies. Clin Orthop Related Res S68-S83.
5. Le Blanc K, Pittenger M. 2005. Mesenchymal stem cells: progress toward promise. Cytotherapy 7:36-45.
6. Bruder SP, Jaiswal N, Ricalton NS, et al. 1998. Mesenchymal stem cells in osteobiology and applied bone regeneration. Clin Orthop Relat Res S247-S256.
7. Barry FP, Murphy JM. 2004. Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 36:568-584.
8. Hench LL, Polak JM. 1965. Third-generation biomedical materials. Science 295:1014-1017.
9. Urist MR. 1965. Bone: formation by autoinduction. Science 150:893-899.
10. Liu P, Oyajobi BO, Russell RG, et al. 1999. Regulation of osteogenic differentiation of human bone marrow stromal cells: interaction between transforming growth factor-beta and 1,25(OH)(2) vitamin D(3) In vitro. Calcif Tissue Int 65:173-180.
11. Koch H, Jadlowiec JA, Campbell PG. 2005. Insulin-like growth factor-I induces early osteoblast gene expression in human mesenchymal stem cells. Stem Cells Dev 14:621-631.
12. Kratchmarova I, Blagoev B, Haack-Sorensen M, et al. 2005. Mechanism of divergent growth factor effects in mesenchymal stem cell differentiation. Science 308:1472-1477.
13. Balooch G, Balooch M, Nalla RK, et al. 2005. TGF-beta regulates the mechanical properties and composition of bone matrix. Proc Natl Acad Sci USA 102:18813-18818.
14. Pettway GJ, Schneider A, Koh AJ, et al. 2005. Anabolic actions of PTH (1-34): use of a novel tissue engineering model to investigate temporal effects on bone. Bone 36: 959-970.
15. Jorgensen NR, Henriksen Z, Sorensen OH, et al. 2004. Dexamethasone, BMP-2, and 1,25-dihydroxyvitamin D enhance a more differentiated osteoblast phenotype: validation of an in vitro model for human bone marrow-derived primary osteoblasts. Steroids 69:219-226.
16. Pittenger MF, et al. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
17. Dezawa M, et al. 2005. Bone marrow stromal. cells generate muscle cells and repair muscle degeneration. Science 309:314-317.
18. Cowan CM, et al. 2004. Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nat Biotechnol 22:560-567.
19. Oreffo RO, Bord S, Triffitt JT. 1998. Skeletal progenitor cells and ageing human populations. Clin Sci (Lond) 94:549-555.
20. 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.
21. Fehrer C, Lepperdinger G. 2005. Mesenchymal stem cell aging. Exp Gerontol 12:926-930.
22. Kassem M, Ankersen L, Eriksen EF, et al. 1997. Demonstration of cellular aging and senescence in serially passaged long-term cultures of human trabecular osteoblasts. Osteoporos Int 7:514-524.
23. Kveiborg M, Kassem M, Langdahl B, et al. 1999. Telomere shortening during aging of human osteoblasts in vitro and leukocytes in vivo: lack of excessive telomere loss in osteoporotic patients. Mech Ageing Dev 106:261-271.
24. Harley CB, Futcher AB, Greider CW. 1990. Telomeres shorten during ageing of human fibroblasts. Nature 345:458-460.
25. Liu L, DiGirolamo CM, Navarro PA, et al. 2004, Telomerase deficiency impairs differentiation of mesenchymal stem cells. Exp Cell Res 294:1-8.
26. Xiaoxue Y, Zhongqiang C, Zhaoqing G, et al. 2004. Immortalization of human osteoblasts by transferring human telomerase reverse transcriptase gene. Biochem Biophys Res Commun 315:643-651.
27. 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.
28. Shi S, Gronthos, S, Chen S, et al. 2002. Bone formation by human postnatal bone marrow stromal stem cells is enhanced by telomerase expression. Nat Biotechnol 20: 587-591.
29. Sugiyama O, An DS, Kung SP, et al. 2005. Lentivirus-mediated gene transfer induces long-term transgene expression of BMP-2 in vitro and new bone formation in vivo. Mol.Ther 11:390-398.
30. Tsuda H, Wads T, Ito Y, et al. 2003. Efficient BMP2 gene transfer and bone formation of mesenchymal stem cells by a fiber-mutant adenoviral vector. Mol Ther 7:354-365.
31. Bertone AL, Pittman DD, Bouxsein ML, et al. 2004. Adenoviral-mediated transfer of human BMP-6 gene accelerates healing in a rabbit ulnar osteotomy model. J Orthop Res 22:1261-1270.
32. Abdelaal MM, Tholpady SS, Kessler JD, et al. 2004. BMP-9-transduced prefabricated muscular flaps for the treatment of bony defects. J Craniofac Surg 15:736-741; discussion 742-744.
33. Jochum W, David JP, Elliott C, et al. 2000. Increased bone formation and osteosclerosis in mice overexpressing the transcription factor Fra-1. Nat Med 6:980-984.
34. Pola E, Gao W, Zhou Y, et al. 2004. Efficient bone formation by gene transfer of human LIM mineralization protein-3. Gene Ther 11:683-693.
35. Mundy G, Garrett R, Harris S, et al. 1999. Stimulation of bone formation in vitro and in rodents by statins. Science 286:1946-1949.
36. Bancroft GN, Sikavitsas VI, van den Dolder J, et al. 2002, Fluid flow increases mineralized matrix deposition in 3D perfusion culture of marrow stromal osteoblasts in a dose-dependent manner. Proc Natl Acad Sci USA 99:12600-12605.
37. Yu X, Botchwey EA, Levine EM, et al. 2004. Bioreactor-based bone tissue engineering: the influence of dynamic flow on osteoblast phenotypic expression and matrix mineralization. Proc Natl Acad Sci USA 101:11203-11208.
38. De Boer J, Wang HJ, Van Blitterswijk C. 2004. Effects of Wnt signaling on proliferation and differentiation of human mesenchymal stem cells. Tissue Eng 10:393-401.
39. de Boer J, Siddappa R, Gaspar C, et al. 2004. Wnt signaling inhibits osteogenic differentiation of human mesenchymal stem cells. Bone 34:818-826.
40. Boer JD, Licht R, Bongers M, et al. 2006. Inhibition of histone acetylation as a tool in bone tissue engineering. Tissue Eng 12:2927-2937.
41. Phinney DG, Kopen G, Righter W, et al. 1999. Donor variation in the growth properties and osteogenic potential of human marrow stromal cells. J Cell Biochem 75:424-436.
42. Both SK, van der Muijenberg AM, van Blitterswijk CA, et al. 2007. A rapid and labour efficient method for expansion of human mesenchymal stem cells for clinical applications. Tissue Eng 13:3-9.
43. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408.
44. Yuan H, Van Den Doel M, Li S, et al. 2002. A comparison of the osteoinductive potential of two calcium phosphate ceramics implanted intramuscularly in goats. J Mater Sci Mater Med 13:1271-1275.
45. Petite H, Viateau V, Bensaid W, et al. 2000. Tissue-engineered bone regeneration. Nat Biotechnol 18:959-963.
46. Zernik J, Twarog K, Upholt WB. 1990. Regulation of alkaline phosphatase and alpha 2(I) procollagen synthesis during early intramembranous bone formation in the rat mandible. Differentiation 44:207-215.
47. Jaiswal N, 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.
48. Frank O, Heim M, Jakob M, et al. 2002. Real-time quantitative RT-PCR analysis of human bone marrow stromal cells during osteogenic differentiation in vitro. J Cell Biochem 85: 737-746.
49. Haynesworth SE, Baber MA, Caplan AI. 1992. Cell surface antigens on human marrow-derived mesenchymal cells are detected by monoclonal antibodies. Bone 13:69-80.
50. Bruder SP, Horowitz MC, Mosca JD, et al. 1997. Monoclonal antibodies reactive with human osteogenic cell surface antigens. Bone 21:225-235.
51. Haynesworth SE, Baber MA, Caplan AI. 1995. Characterization of the unique mesenchymal stem cell phenotype in vitro. Trans 41st Ann Meet Orthop Res Soc 20:7.
52. Gronthos S, Zannettino AC, Hay SJ, et al. 2003. Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 116:1827-1835.
53. Mendes SC, Tibbe JM, Veenhof M, et al. 2004. Relation between in vitro and in vivo osteogenic potential of cultured human bone marrow stromal cells. J Mater Sci Mater Med 15:1123-1128.
54. 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.
55. Kruyt MC, de Bruijn JD, Yuan H, et al. 2004. Optimization of bone tissue engineering in goats: a peroperative seeding method using cryopreserved cells and localized bone formation in calcium phosphate scaffolds. Transplantation 77:359-365.
56. Derubeis AR, Cancedda R. 2004. Bone marrow stromal cells (BMSCs) in bone engineering: limitations and recent advances. Ann Biomed Eng 32:160-165.
57. Martin I, Muraglia A, Campanile G, et al. 1997. Fibroblast growth factor-2 supports ex vivo expansion and maintenance of osteogenic precursors from human bone marrow. Endocrinology 138:4456-4462.
58. Hong JH, Hwang ES, McManus MT, et al. 2005. TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 309:1074-1078.
59. Jaiswal RK, Jaiswal N, Bruder SP, et al. 2000. Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase. J Biol Chem 275:9645-9652.
60. McBeath R, Pirone DM, Nelson CM, et al. 2004. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6:483-495.
61. Tezuka K, Yasuda M, Watanabe N, et al. 2002. Stimulation of osteoblastic cell differentiation by Notch. J Bone Miner Res 17:231-239.