Clonal chondroprogenitors maintain telomerase activity and Sox9 expression during extended monolayer culture and retain chondrogenic potential

Osteoarthritis and Cartilage

Volumn 17, Issue 4, 2009, Pages 518-528

  Khan, I M ^a   Bishop, J C ^b   Gilbert, S ^a   Archer, C W ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b SWANSEA UNIVERSITY   (United Kingdom)

Author keywords

Chondroprogenitor; Notch 1; sox9; Telomerase; Telomere

Indexed keywords

AGGRECAN; BETA GALACTOSIDASE; CYCLINE; FIBRONECTIN; MESSENGER RNA; NOTCH1 RECEPTOR; TELOMERASE; TRANSCRIPTION FACTOR SOX9;

ANIMAL CELL; ARTICLE; ARTICULAR CARTILAGE; BULLOCK; CARTILAGE CELL; CELL ADHESION; CELL CLONE; CELL COUNT; CELL DIFFERENTIATION; CELL GROWTH; CELL ISOLATION; CONTROLLED STUDY; CYTOLOGY; ENZYME ACTIVITY; ENZYME ANALYSIS; GENE EXPRESSION; IN VITRO STUDY; MALE; METACARPOPHALANGEAL JOINT; MONOLAYER CULTURE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SENESCENCE; STEM CELL EXPANSION; TELOMERE; ANIMAL; BOVINAE; CELL AGING; CELL CULTURE; CELL DIVISION; CHONDROGENESIS; GENETICS; METABOLISM; PHYSIOLOGY; STEM CELL;

ANIMALS; CARTILAGE, ARTICULAR; CATTLE; CELL AGING; CELL DIFFERENTIATION; CELL DIVISION; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; MALE; RECEPTOR, NOTCH1; RNA, MESSENGER; SOX9 TRANSCRIPTION FACTOR; STEM CELLS; TELOMERASE;

EID: 61549122060     PISSN: 10634584     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.joca.2008.08.002     Document Type: Article

References (40)

1. Jakob M., Demarteau O., Schafer D., Hintermann B., Dick W., Heberer M., et al. Specific growth factors during the expansion and redifferentiation of adult human articular chondrocytes enhance chondrogenesis and cartilaginous tissue formation in vitro. J Cell Biochem 81 (2001) 368-377
2. Martin I., Vunjak-Novakovic G., Yang J., Langer R., and Freed L.E. Mammalian chondrocytes expanded in the presence of fibroblast growth factor 2 maintain the ability to differentiate and regenerate three-dimensional cartilaginous tissue. Exp Cell Res 253 (1999) 681-688
3. Yaeger P.C., Masi T.L., de Ortiz J.L., Binette F., Tubo R., and McPherson J.M. Synergistic action of transforming growth factor-beta and insulin-like growth factor-I induces expression of type II collagen and aggrecan genes in adult human articular chondrocytes. Exp Cell Res 237 (1997) 318-325
4. Brittberg M., Lindahl A., Nilsson A., Ohlsson C., Isaksson O., and Peterson L. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 331 (1994) 889-895
5. Benya P.D., and Shaffer J.D. Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 30 (1982) 215-224
6. Bonaventure J., Kadhom N., Cohen-Solal L., Ng K.H., Bourguignon J., Lasselin C., et al. Reexpression of cartilage-specific genes by dedifferentiated human articular chondrocytes cultured in alginate beads. Exp Cell Res 212 (1994) 97-104
7. Aydelotte M.B., Greenhill R.R., and Kuettner K.E. Differences between sub-populations of cultured bovine articular chondrocytes. II. Proteoglycan metabolism. Connect Tissue Res 18 (1988) 223-234
8. Archer C.W., McDowell J., Bayliss M.T., Stephens M.D., and Bentley G. Phenotypic modulation in sub-populations of human articular chondrocytes in vitro. J Cell Sci 97 Pt 2 (1990) 361-371
9. Dowthwaite G.P., Bishop J.C., Redman S.N., Khan I.M., Rooney P., Evans D.J., et al. The surface of articular cartilage contains a progenitor cell population. J Cell Sci 117 (2004) 889-897
10. Hou M., Xu D., Bjorkholm M., and Gruber A. Real-time quantitative telomeric repeat amplification protocol assay for the detection of telomerase activity. Clin Chem 47 (2001) 519-524
11. Dimri G.P., Lee X., Basile G., Acosta M., Scott G., Roskelley C., et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 92 (1995) 9363-9367
12. Blain E.J., Gilbert S.J., Hayes A.J., and Duance V.C. Disassembly of the vimentin cytoskeleton disrupts articular cartilage chondrocyte homeostasis. Matrix Biol 25 (2006) 398-408
13. Wright W.E., Tesmer V.M., Huffman K.E., Levene S.D., and Shay J.W. Normal human chromosomes have long G-rich telomeric overhangs at one end. Genes Dev 11 (1997) 2801-2809
14. Allsopp R.C., and Harley C.B. Evidence for a critical telomere length in senescent human fibroblasts. Exp Cell Res 219 (1995) 130-136
15. Baird D.M. Telomere dynamics in human cells. Biochimie 90 (2008) 116-121
16. Greider C.W., and Blackburn E.H. The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell 51 (1987) 887-898
17. Piera-Velazquez S., Jimenez S.A., and Stokes D. Increased life span of human osteoarthritic chondrocytes by exogenous expression of telomerase. Arthritis Rheum 46 (2002) 683-693
18. Parsch D., Brummendorf T.H., Richter W., and Fellenberg J. Replicative aging of human articular chondrocytes during ex vivo expansion. Arthritis Rheum 46 (2002) 2911-2916
19. Martin J.A., and Buckwalter J.A. The role of chondrocyte senescence in the pathogenesis of osteoarthritis and in limiting cartilage repair. J Bone Joint Surg 85-A Suppl 2 (2003) 106-110
20. Linskens M.H., Feng J., Andrews W.H., Enlow B.E., Saati S.M., Tonkin L.A., et al. Cataloging altered gene expression in young and senescent cells using enhanced differential display. Nucleic Acids Res 23 (1995) 3244-3251
21. Bagheri S., Nosrati M., Li S., Fong S., Torabian S., Rangel J., et al. Genes and pathways downstream of telomerase in melanoma metastasis. Proc Natl Acad Sci U S A 103 (2006) 11306-11311
22. Stokes D.G., Liu G., Dharmavaram R., Hawkins D., Piera-Velazquez S., and Jimenez S.A. Regulation of type-II collagen gene expression during human chondrocyte de-differentiation and recovery of chondrocyte-specific phenotype in culture involves Sry-type high-mobility-group box (SOX) transcription factors. Biochem J 360 (2001) 461-470
23. Tew S.R., Li Y., Pothacharoen P., Tweats L.M., Hawkins R.E., and Hardingham T.E. Retroviral transduction with SOX9 enhances re-expression of the chondrocyte phenotype in passaged osteoarthritic human articular chondrocytes. Osteoarthritis Cartilage 13 (2005) 80-89
24. Akiyama H., Kim J.E., Nakashima K., Balmes G., Iwai N., Deng J.M., et al. Osteo-chondroprogenitor cells are derived from Sox9 expressing precursors. Proc Natl Acad Sci U S A 102 (2005) 14665-14670
25. Seymour P.A., Freude K.K., Tran M.N., Mayes E.E., Jensen J., Kist R., et al. SOX9 is required for maintenance of the pancreatic progenitor cell pool. Proc Natl Acad Sci U S A 104 (2007) 1865-1870
26. Lynn F.C., Smith S.B., Wilson M.E., Yang K.Y., Nekrep N., and German M.S. Sox9 coordinates a transcriptional network in pancreatic progenitor cells. Proc Natl Acad Sci U S A 104 (2007) 10500-10505
27. Lewis J. Notch signalling and the control of cell fate choices in vertebrates. Semin Cell Dev Biol 9 (1998) 583-589
28. Karlsson C., Stenhamre H., Sandstedt J., and Lindahl A. Neither Notch1 expression nor cellular size correlate with mesenchymal stem cell properties of adult articular chondrocytes. Cells Tissues Organs 187 (2008) 275-285
29. Karlsson C., Brantsing C., Egell S., and Lindahl A. Notch1, Jagged1, and HES5 are abundantly expressed in osteoarthritis. Cells Tissues Organs (2008)
30. Hiraoka K., Grogan S., Olee T., and Lotz M. Mesenchymal progenitor cells in adult human articular cartilage. Biorheology 43 (2006) 447-454
31. Hayes A.J., MacPherson S., Morrison H., Dowthwaite G., and Archer C.W. The development of articular cartilage: evidence for an appositional growth mechanism. Anat Embryol 203 (2001) 469-479
32. Watanabe N., Tezuka Y., Matsuno K., Miyatani S., Morimura N., Yasuda M., et al. Suppression of differentiation and proliferation of early chondrogenic cells by Notch. J Bone Miner Metab 21 (2003) 344-352
33. Gasca S., Canizares J., De Santa Barbara P., Mejean C., Poulat F., Berta P., et al. A nuclear export signal within the high mobility group domain regulates the nucleocytoplasmic translocation of SOX9 during sexual determination. Proc Natl Acad Sci U S A 99 (2002) 11199-11204
34. de Santa Barbara P., Moniot B., Poulat F., and Berta P. Expression and subcellular localization of SF-1, SOX9, WT1, and AMH proteins during early human testicular development. Dev Dyn 217 (2000) 293-298
35. Barbero A., Ploegert S., Heberer M., and Martin I. Plasticity of clonal populations of dedifferentiated adult human articular chondrocytes. Arthritis Rheum 48 (2003) 1315-1325
36. Dell'Accio F., De Bari C., and Luyten F.P. Microenvironment and phenotypic stability specify tissue formation by human articular cartilage-derived cells in vivo. Exp Cell Res 287 (2003) 16-27
37. de la Fuente R., Abad J.L., Garcia-Castro J., Fernandez-Miguel G., Petriz J., Rubio D., et al. Dedifferentiated adult articular chondrocytes: a population of human multipotent primitive cells. Exp Cell Res 297 (2004) 313-328
38. Diaz-Romero J., Nesic D., Grogan S.P., Heini P., and Mainil-Varlet P. Immunophenotypic changes of human articular chondrocytes during monolayer culture reflect bona fide dedifferentiation rather than amplification of progenitor cells. J Cell Physiol 214 (2008) 75-83
39. Jadin K.D., Wong B.L., Bae W.C., Li K.W., Williamson A.K., Schumacher B.L., et al. Depth-varying density and organization of chondrocytes in immature and mature bovine articular cartilage assessed by 3D imaging and analysis. J Histochem Cytochem 53 (2005) 1109-1119
40. Thornemo M., Tallheden T., Sjogren Jansson E., Larsson A., Lovstedt K., Nannmark U., et al. Clonal populations of chondrocytes with progenitor properties identified within human articular cartilage. Cells Tissues Organs 180 (2005) 141-150