Apoptosis and the loss of chondrocyte survival signals contribute to articular cartilage degradation in osteoarthritis

Veterinary Journal

Volumn 166, Issue 2, 2003, Pages 140-158

  Goggs, Robert ^a   Carter, Stuart D ^a   Schulze Tanzil, Gundula ^b   Shakibaei, Mehdi ^b   Mobasheri, Ali ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Apoptosis; Articular cartilage; Chondrocyte; Integrin; Nitric oxide; Osteoarthritis; Signal transduction; Survival signal

Indexed keywords

APOPTOSIS INHIBITOR; BETA1 INTEGRIN; GLUCOSAMINE; GLYCOSAMINOGLYCAN POLYSULFATE; HYALURONIC ACID; ISATIN SULFONAMIDE; NONSTEROID ANTIINFLAMMATORY AGENT; PROTEINASE INHIBITOR; SOMATOMEDIN C; UNCLASSIFIED DRUG; VITAMIN; INTEGRIN;

ANIMAL CELL; APOPTOSIS; ARTICULAR CARTILAGE; CARTILAGE CELL; CARTILAGE DEGENERATION; CATABOLISM; CELL INTERACTION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOLOGY; DRUG MECHANISM; DRUG TARGETING; EXTRACELLULAR MATRIX; HYPOTHESIS; NONHUMAN; OSTEOARTHRITIS; PATHOGENESIS; REVIEW; ANIMAL; ANIMAL DISEASE; CARTILAGE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CARTILAGE; CELL SURVIVAL; CHONDROCYTES; INTEGRINS; OSTEOARTHRITIS; SIGNAL TRANSDUCTION;

EID: 0041382662     PISSN: 10900233     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1090-0233(02)00331-3     Document Type: Article

References (143)

1. Adams M.E. Grant M.D. Ho A. Cartilage proteoglycan changes in experimental canine osteoarthritis Journal of Rheumatology 14 1987 107-109
2. Adams C.S. Horton W.E. Chondrocyte apoptosis increases with age in the articular cartilage of adult animals Anatomical Record 250 1998 418-425
3. Adams J.M. Cory S. The Bcl-2 protein family: arbiters of cell survival Science 281 1998 1322-1326
4. Adams J.M. Cory S. Life-or-death decisions by the Bcl-2 protein family Trends in Biochemical Sciences 26 2001 61-66
5. Aigner T. Apoptosis, necrosis, or whatever: how to find out what really happens? Journal of Pathology 198 2002 1-4
6. Aigner T. Hemmel M. Neureiter D. Gebhard P.M. Zeiler G. Kirchner T. McKenna L. Apoptotic cell death is not a widespread phenomenon in normal aging and osteoarthritis human articular knee cartilage: a study of proliferation, programmed cell death (apoptosis), and viability of chondrocytes in normal and osteoarthritic human knee cartilage Arthritis and Rheumatism 44 2001 1304-1312
7. Aizawa T. Kon T. Einhorn T.A. Gerstenfeld L.C. Induction of apoptosis in chondrocytes by tumour necrosis factor-α Journal of Orthopaedic Research 19 2001 785-796
8. Akiyama M. Hideshima T. Hayashi T. Tai Y.T. Mitsiades C.S. Mitsiades N. Anderson K.C. IGF-1 induced telomerase activity and protects against apoptosis in multiple myeloma cells Blood 98 Supplement Part 2 2001 2680
9. Amin A.R. Abramson M.D. The role of nitric oxide in articular cartilage breakdown in osteoarthritis Current Opinion in Rheumatology 10 1998 263-268
10. Amling M. Neff L. Tanaka S. Inoue D. Kuida K. Weir E. Phibrick W.M. Broadus A.E. Baron R. Bcl-2 lies downstream of parathyroid hormone-related peptide in a signalling pathway that regulates chondrocyte maturation during skeletal development Journal of Cell Biology 136 1997 205-213
11. Arner E.C. Hughes C.E. Decicco C.P. Caterson B. Tortorella M.D. Cytokine-induced cartilage proteoglycan degradation is mediated by aggrecanase Osteoarthritis and Cartilage 6 1998 214-228
12. Attur M.G. Dave M.N. Clancy R.M. Patel I.R. Abramson S.B. Amin A.R. Functional genomic analysis in arthritis-affected cartilage: Ying-Yang regulation of inflammatory mediators by α5β1- and αvβ3-integrins Journal of Immunology 164 2000 2684-2691
13. Bassleer C. Rovati L. Franchimont P. Stimulation of proteoglycan production by glucosamine sulfate in chondrocytes isolated from human osteoarthritic cartilage in vitro Osteoarthritis and Cartilage 6 1998 427-434
14. Blackburn E.H. Structure and function of telomeres Nature 350 1991 569-573
15. Blanco F.J. Catabolic events in osteoarthritic cartilage Osteoarthritis and Cartilage 7 1999 308-309
16. 2 Experimental Cell Research 218 1995 319-325
17. Blanco F.J. Ochs R.L. Schwarz H. Lotz M. Chondrocyte apoptosis induced by nitric oxide American Journal of Pathology 146 1995 75-85
18. Blanco F.J. Guitian R. Vazques-Martul E. Detoro F.J. Galdo F. Osteoarthritis chondrocytes die by apoptosis Arthritis and Rheumatism 41 1998 284-289
19. Brancolini C. Benedetti M. Schneider C. Microfilament reorganization during apoptosis: the role of Gas2, a possible substrate for ICE-like proteases EMBO Journal 14 1995 5179-5190
20. Bratton S.B. Macfarlane M. Cain K. Cohen G.M. Protein complexes activate distinct caspase cascades in death receptor and stress-induced apoptosis Experimental Cell Research 256 2000 27-33
21. Cao L. Lee V. Adams M.E. Kiani C. Zhang Y.O. Hu W. Yang B.B. β1-Integrin-collagen interaction reduces chondrocyte apoptosis Matrix Biology 18 1999 343-355
22. Cao M. Westerhausen-Larson A. Niyibizi C. Kavalkovich K. Georgescu H.I. Rizzo C.F. Hebda P.A. Stefanovic-Racic M. Evans C.H. Nitric oxide inhibits the synthesis of type-II collagen without altering Col2A1 mRNA abundance: prolyl hydroxylase as a possible target Biochemical Journal 324 1997 305-310
23. Cardone M.H. Salvesen G.S. Widmann C. Johnson G. Frisch S.M. The regulation of anoikis: MEKK-1 activation requires cleavage by caspases Cell 90 1997 315-323
24. Carson D.A. Ribeiro J.M. Apoptosis and disease The Lancet 341 1993 1251-1254
25. Casciola-Rosen L.A. Anhalt G.J. Rosen A. DNA-dependent protein kinase is one of a subset of autoantigens specifically cleaved early during apoptosis Journal of Experimental Medicine 182 1995 1625-1634
26. Caswell A.M. Ali S.Y. Russell R.G.G. Nucleoside triphosphate pyrophosphatase of rabbit matrix vesicles, a mechanism for the generation of inorganic pyrophosphate in epiphyseal cartilage Biochimica et Biophysica Acta 924 1987 276-283
27. Cheng E.H.Y. Kirsch D.G. Clem R.J. Ravi R. Kastan M.B. Bedi A. Ueno K. Hardwick J.M. Conversion of Bcl-2 to a Bax-like death effector by caspases Science 278 1997 1966-1968
28. Chung H.-T. Pae H.-O. Choi B.-M. Billiar T.R. Kim Y.-M. Nitric oxide as a bioregulator of apoptosis Biochemical and Biophysical Research Communications 282 2001 1075-1079
29. Clancy R.M. Nitric oxide alters chondrocyte function by disrupting cytoskeletal signaling complexes Osteoarthritis and Cartilage 7 1999 399-400
30. Clancy R.M. Rediske J. Tang X. Nijher N. Frenkel S. Philips M. Abramson S.B. Outside-in signaling in the chondrocyte. Nitric oxide disrupts fibronectin-induced assembly of a subplasmalemmal actin rho A focal adhesion kinase signaling complex Journal of Clinical Investigation 100 1997 1789-1796
31. Conus S. Rosse T. Borner C. Failure of Bcl-2 family members to interact with Apaf-1 in normal and apoptotic cells Cell Death and Differentiation 7 2000 947-954
32. Cox M.J. Mcdevitt C.A. Arnoczky S.P. Warren R.F. Changes in the chondroitin sulfate-rich region of articular cartilage proteoglycans in experimental osteoarthritis Biochimica et Biophysica Acta 840 1985 228-234
33. Das P. Schurman D.J. Smith R.L. Nitric oxide and G proteins mediate the response of bovine articular chondrocytes to fluid-induced shear Journal of Orthopedic Research 15 1997 87-93
34. De Maria R. Lenti L. Malisan F. D'agostino F. Tomassini B. Zeuner A. Rippo M.R. Testi R. Requirement for GD3 ganglioside in CD95- and ceramide-induced apoptosis Science 277 1997 1652-1655
35. Deigner H.P. Haberkorn U. Kinscherf R. Apoptosis modulators in the therapy of neurodegenerative diseases Expert Opinion on Investigational Drugs 9 2000 747-764
36. Denhardt D.T. Signal transducing protein phosphorylation cascades mediated by Ras/Rho proteins in the mammalian cell: the potential for multiplex signalling Biochemical Journal 318 1996 729-747
37. D'lima D. Hashimoto S. Chen P.C. Colwell C. Lotz M. Impact of mechanical trauma on matrix and cells Clinical Orthopaedics 391 Supplement S90-S99 2001
38. Doré S. Pelletier J.P. Dibattista J.A. Tardif G. Brazeau P. Martel-Pelletier J. Human osteoarthritic chondrocytes possess an increased number of insulin-like growth factor 1 binding sites but are unresponsive to its stimulation Arthritis and Rheumatism 37 1994 253-263
39. Dunham J. Shackleton D.R. Nahir A.M. Billingham M.E. Bitensky L. Chayen J. Muir I.H. Altered orientation of glycosaminoglycans and cellular changes in the tibial cartilage in the first two weeks of experimental canine osteoarthritis Journal of Orthopaedic Research 3 1985 258-268
40. Fam A.G. Moravaprotzner I. Purcell C. Young B.D. Bunting P.S. Lewis A.J. Acceleration of experimental lapine osteoarthritis by calcium pyrophosphate microcrystalline synovitis Arthritis and Rheumatism 38 1995 201-210
41. Feng L. Balakir R. Precht P. Horton W.E. Bcl-2 regulates chondrocyte morphology and aggrecan gene expression independent of caspase activation and full apoptosis Journal of Cellular Biochemistry 74 1999 576-586
42. Feng L. Precht P. Balakir R. Horton W.E. Evidence of a direct role for Bcl-2 in the regulation of articular chondrocyte apoptosis under the conditions of serum withdrawal and retinoic acid treatment Journal of Cellular Biochemistry 71 1998 302-309
43. Fernandez-Checa J.C. Garcia-Ruiz C. Colell A. Calvo M. Enrich C. Trafficking of ganglioside GD3 to mitochondria is a key event in tumor necrosis factor (TNF)- and ceramide-induced apoptosis of rat hepatocytes Hepatology 32 2000 219
44. Frisch S.M. Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis Journal of Cell Biology 124 1994 619-626
45. Gardner D.L. Pathological Basis of the Connective Tissue Diseases 1992 193-195 Edward Arnold London
46. Gardner D.L. Pathological Basis of the Connective Tissue Diseases 1992 896-901 Edward Arnold London
47. Gardner D.L. Pathological Basis of the Connective Tissue Diseases 1992 847-860 Edward Arnold London
48. Goldring M.B. The role of the chondrocyte in osteoarthritis Arthritis and Rheumatism 43 2000 1916-1926
49. Goping I.S. Gross A. Lavoie J.N. Nguyen M. Jemmerson R. Roth K. Korsmeyer S.J. Shore G.C. Regulated targeting of Bax to mitochondria Journal of Cell Biology 143 1998 207-215
50. Gouze J.-N. Bordji K. Gulberti S. Terlain B. Netter P. Magdalou J. Fournel-Gigleux S. Ouzzine M. Interleukin-1β down-regulates the expression of glucuronosyltransferase I, a key enzyme priming glycosaminoglycan biosynthesis Arthritis and Rheumatism 44 2001 351-360
51. Gruber H.E. Norton H.J. Hanley E.N.J.R. Anti-apoptotic effects of IGF-1 and PDGF on human intervertebral disc cells in vitro Spine 25 2000 2153-2157
52. Harley C.B. Vaziri H. Counter C.M. Allsopp R.C. The telomere hypothesis of cellular ageing Experimental Gerontology 27 1992 375-382
53. Hashimoto H. Tanaka M. Suda T. Tomita T. Hayashida K. Takeuchi E. Kaneko M. Takano H. Nagata S. Ochi T. Soluble Fas ligand in the joints of patients with rheumatoid arthritis and osteoarthritis Arthritis and Rheumatism 41 1998 657-662
54. Hashimoto S. Ochs R.L. Komiya S. Lotz M. Linkage of chondrocyte apoptosis and cartilage degradation in human osteoarthritis Arthritis and Rheumatism 41 1998 1632-1638
55. Hashimoto S. Ochs R.L. Rosen F. Quach J. Mccabe G. Solan J. Seegmiller J.E. Terkeltaub R. Lotz M. Chondrocyte-derived apoptotic bodies and calcification of articular cartilage Proceedings of the National Academy of Sciences of The United States of America 95 1998 3094-3099
56. Hashimoto S. Setareh M. Ochs R.L. Lotz M. Fas/Fas ligand expression and induction of apoptosis in chondrocytes Arthritis and Rheumatism 40 1997 1749-1755
57. Hashimoto S. Takahashi K. Amiel D. Coutts R.D. Lotz M. Chondrocyte apoptosis and nitric oxide production during experimentally induced osteoarthritis Arthritis & Rheumatism 41 1998 1266-1274
58. Hatton J. Pharmacological treatment of traumatic brain injury: a review of agents in development CNS Drugs 15 2001 553-581
59. Hering T.M. Regulation of chondrocyte gene expression Frontiers in Bioscience 4 1999 743-761
60. Holt S.E. Shay J.W. Role of telomerase in cellular proliferation and cancer Journal of Cell Physiology 180 1999 10-18
61. Horton W.E. Feng L. Adams C. Chondrocyte apoptosis in development, ageing and disease Matrix Biology 17 1998 107-115
62. Hsu H.H.T. Anderson H.C. The deposition of calcium pyrophosphate and phosphate by matrix vesicles isolated from fetal bovine epiphyseal cartilage Calcified Tissue International 36 1982 615-621
63. Huppertz B. Frank H.-G. Kaufmann P. The apoptosis cascade - morphological and immunohistochemical methods for its visualization Anatomy and Embryology 200 1999 1-18
64. Hynes R.O. Integrins: versatility, modulation, and signaling in cell adhesion Cell 69 1992 11-25
65. Jin J. Hauberg M. Heidorn K. Klapper W. Parwaresch R. Inhibition of telomerase by homoharringtonine induces apoptosis in a human Burkitt lymphoma cell line Blood 94 Supplement Part 1 1999 384
66. Johnson V.L. Cooper I.R. Jenkins J.R. Chow S.C. Effects of differential overexpression of Bcl-2 on apoptosis, proliferation and telomerase activity in Jurkat T cells Experimental Cell Research 251 1999 175-184
67. Kelekar A. Chang B.S. Harlan J.E. Fesik S.W. Thompson C.B. Bad is a BH3 domain-containing protein that forms an inactivating dimer with Bcl-x(L) Molecular and Cellular Biology 17 1997 7040-7046
68. Kim H.-A. Lee Y.J. Seong S.-C. Choe K.W. Song Y.K. Apoptotic chondrocyte death in human osteoarthritis Journal of Rheumatology 27 2000 455-462
69. Kim S.-J. Ju J.-W. Oh C.-D. Yoon Y.-M. Song W.K. Kim J.-H. Yoo Y.J. Bang O.-S. Kang S.-S. Chun J.-S. ERK-1/2 and p38 kinase oppositely regulate nitric oxide-induced apoptosis of chondrocytes in association with p53, caspase-3, and differentiation status Journal of Biological Chemistry 277 2002 1332-1339
70. Kühn K. Hashimoto S. Lotz M. Cell density modulates apoptosis in human articular chondrocytes Journal of Cell Physiology 180 1999 439-447
71. Kühn K. Hashimoto S. Lotz M. IL-1β protects human chondrocytes from CD95-induced apoptosis Journal of Immunology 164 2000 2233-2239
72. Kühn K. Lotz M. Regulation of CD95 (Fas/APO-1)-induced apoptosis in human chondrocytes Arthritis and Rheumatism 44 2001 1644-1653
73. Lapadula G. Iannone F. Zuccaro C. Grattagliano V. Covelli M. Patell B.G. Pipitone V. Chondrocyte phenotyping in human osteoarthritis Clinical Rheumatology 17 1998 99-104
74. Lazebnik Y.A. Kaufmann S.H. Desnoyers S. Poirier G.G. Earnshaw W.C. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE Nature 371 1994 346-347
75. Lee D. Long S.A. Adams J.L. Chan G. Vaidya K.S. Francis T.A. Kikly K. Winkler J.D. Sung C.M. Debouck C. Richardson S. Levy M.A. Dewolf W.E.J.R. Keller P.M. Tomaszek T. Head M.S. Ryan M.D. Haltiwanger R.C. Liang P.H. Janson C.A. Mcdevitt P.J. Johanson K. Concha N.O. Chan W. Abdel-Meguid S.S. Badger A.M. Lark M.W. Nadeau D.P. Suva L.J. Gowen M. Nuttall M.E. Potent and selective nonpeptide inhibitors of caspases 3 and 7 inhibit apoptosis and maintain cell functionality Journal of Biological Chemistry 275 2000 16007-16014
76. Lee M.S. Trindade M.C.D. Ikenoue T. Schurman D.J. Goodman S.B. Smith R.L. Effects of shear stress on nitric oxide and matrix protein gene expression in human osteoarthritic chondrocytes in vitro Journal of Orthopaedic Research 20 2002 556-561
77. Lenormand P. Sardet C. Pages G. L'allemain G. Brunet A. Pouyssegur J. Growth factors induce nuclear translocation of MAP kinases (p42 (MAPK) and p44 (MAPK)) but not their activator MAP kinase kinase (p45 (MAPKK)) in fibroblasts Journal of Cell Biology 122 1993 1079-1088
78. Lisignoli G. Grassi F. Zini N. Toneguzzi S. Piacentini A. Guidolin D. Bevilacqua C. Facchini A. Anti-Fas-induced apoptosis in chondrocytes reduced by hyaluronan Arthritis and Rheumatism 44 2001 1800-1807
79. Loening A.M. James I.E. Levenston M.E. Badger A.M. Frank E.H. Kurz B. Nuttall M.E. Hung H.H. Blake S.M. Grodzinsky A.J. Lark M.W. Injurious mechanical compression of bovine articular cartilage induces chondrocyte apoptosis Archives of Biochemistry and Biophysics 381 2000 205-212
80. Loeser R.F. Carlson C.S. Mcgee M.P. Expression of β1-integrins by cultured articular chondrocytes and in osteoarthritic cartilage Experimental Cell Research 217 1995 248-257
81. Loeser R.F. Shanker G. Autocrine stimulation by insulin-like growth factor 1 and insulin-like growth factor 2 mediates chondrocytes survival in vitro Arthritis and Rheumatism 43 2000 1552-1559
82. Loeser R.F. Shanker G. Carlson C.S. Gardin J.F. Shelton B.J. Sonntag W.E. Reduction in the chondrocyte response to insulin-like growth factor 1 in ageing and osteoarthritis Arthritis and Rheumatism 43 2000 2110-2120
83. Lotz M. Hasimoto S. Kühn K. Mechanisms of chondrocyte apoptosis Osteoarthritis and Cartilage 7 1999 389-391
84. Mandal M. Kumar R. Bcl-2 modulates telomerase activity Journal of Biological Chemistry 272 1997 14183-14187
85. Mandel N.S. Mandel G.S. Carroll D.J. Halverson P.B. Calcium pyrophosphate crystal deposition-an in vitro study using a gelatin matrix model Arthritis and Rheumatism 27 1984 789-796
86. von der Mark K. Kirsch T. Nerlich G. Kuss A. Weseloh G. Gluckert K. Stoss H. Type X collagen synthesis in human osteoarthritic cartilage: indication of chondrocyte hypertrophy Arthritis and Rheumatism 35 1992 806-811
87. Martel-Pelletier J. Pathophysiology of osteoarthritis Osteoarthritis and Cartilage 6 1998 374-376
88. Martel-Pelletier J. Dibattista J.A. Lajeunesse D. Pelletier J.P. IGF/IGFBP axis in cartilage and bone in osteoarthritis pathogenesis Inflammation Research 47 1998 90-100
89. Mashima T. Naito M. Fujita N. Noguchi K. Tsuruo T. Identification of actin as a substrate of ICE and an ICE-like protease and involvement of an ICE-like protease but not ICE in VP-16-induced U937 apoptosis Biochemical and Biophysical Research Communications 217 1995 1185-1192
90. Masuko-Hongo K. Sakata M. Yuan G.H. Nakamura H. Kato T. Nishioka K. Chondrocyte apoptosis does not depend on Fas-signaling pathway Arthritis and Rheumatism 43 Supplement 2000 1691
91. Mendes A.F. Caramona M.M. Carvalho A.P. Lopes M.C. Role of mitogen-activated protein kinases and tyrosine kinases on IL-1-induced NF-κB activation and iNOS expression in bovine articular chondrocytes Nitric Oxide-Biology and Chemistry 6 2002 35-44
92. Messai H. Duchossoy Y. Khatib A.M. Panasyuk A. Mitrovic D.R. Articular chondrocytes from ageing rats respond poorly to insulin-like growth factor-1: an altered signaling pathway Mechanisms of Ageing and Development 115 2000 21-37
93. Miwa M. Saura R. Hirata S. Hayashi Y. Mizuno K. Itoh H. Induction of apoptosis in bovine articular chondrocyte by prostaglandin E(2) through cAMP-dependent pathway Osteoarthritis and Cartilage 8 2000 17-24
94. Mobasheri A. The role of chondrocyte death and hypocellularity in ageing human articular cartilage and the pathogenesis of osteoarthritis Medical Hypotheses 58 2002 193-197 doi: 10.1054/mehy.2000.1180
95. Morin G.B. The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats Cell 59 1989 521-529
96. Muir H. The chondrocyte, architect of cartilage. Biomechanics, structure, function and molecular biology of cartilage matrix macromolecules Bioessays 12 1995 1039-1048
97. Murphree S. Hsu H.H.T. Anderson H.C. In vitro formation of crystalline apatite by matrix vesicles isolated from rachitic rat epiphyseal cartilage Calcified Tissue International 34 1982 S62-S68
98. Nishida Y. Shinomura T. Iwata H. Miura T. Kimata K. Abnormal occurrence of a large chondroitin-sulfate proteoglycan, PG-M/versican in osteoarthritic cartilage Osteoarthritis and Cartilage 2 1994 43-49
99. 2 via the induction of cyclooxygenase-2 Journal of Immunology 165 2000 3402-3410
100. Ohira T. Ishikawa K. Hydroxyapatite deposition in osteoarthritic articular cartilage of the proximal femoral head Arthritis and Rheumatism 30 1987 651-660
101. Olney R.C. Wilson D.M. Mohtai M. Fielder P.J. Smith R.L. Interleukin-1 and tumour necrosis factor-binding protein-3 (IGFBP-3) production and IGFBP-3 protease activity in human articular chondrocytes Journal of Endocrinology 146 1995 279-286
102. Oltvai Z.N. Milliman C.L. Korsmeyer S.J. Bcl-2 heterodimerises in vivo with a conserved homologue, Bax, that accelerates programmed cell death Cell 74 1993 609-619
103. 2 via the induction of cyclooxygenase-2 Arthritis and Rheumatism 43 Supplement 2000 1689
104. Petit P.X. Susin S.A. Zamzami N. Mignotte B. Kroemer G. Mitochondria and programmed cell death: back to the future FEBS Letters 396 1996 7-13
105. Piera-Velazquez S. Jimenez S.A. Stokes D.G. Increased life span of human osteoarthritic chondrocytes by exogenous expression of telomerase Arthritis and Rheumatism 46 2002 683-693
106. Rath P.C. Aggarwal B.B. TNF-induced signaling in apoptosis Journal of Clinical Immunology 19 1999 350-364
107. Ren J.G. Xia H.L. Tian Y.M. Just T. Cai G.P. Dai Y.R. Expression of telomerase inhibits hydroxyl radical-induced apoptosis in normal telomerase negative human lung fibroblasts FEBS Letters 488 2001 133-138
108. Richardson D.W. Dodge G.R. Effects of interleukin-1β and tumour necrosis factor-α on expression of matrix-related genes by cultured equine articular chondrocytes American Journal of Veterinary Research 61 2000 624-630
109. Richter C. Schweizer M. Cossarizza A. Franceschi C. Control of apoptosis by the cellular ATP level FEBS Letters 378 1996 107-110
110. Robbins J.R. Thomas B. Tan L. Choy B. Arbiser J.L. Berenbaum F. Goldring M.B. Immortalized human adult articular chondrocytes maintain cartilage specific phenotype and responses to interleukin-1β Arthritis and Rheumatism 43 2000 2189-2201
111. Roberts E.D. Baskin G.B. Watson E. Henk W.G. Shelton T.C. Calcium pyrophosphate deposition disease (CPPD) in nonhuman primates American Journal of Pathology 116 1984 359-361
112. Rosen A. Casciola-Rosen L. Macromolecular substrates for the ICE-like proteases during apoptosis Journal of Cellular Biochemistry 64 1997 50-54
113. Rudel T. Bokoch G.M. Membrane and morphological changes in apoptotic cells regulated by caspase-mediated activation of PAK2 Science 276 1997 1571-1574
114. Sabatini M. Rolland G. Leonce S. Thomas M. Lesur C. Perez V. De Nanteuil G. Bonnet J. Effects of ceramide on apoptosis, proteoglycan degradation, and matrix metalloproteinase expression in rabbit articular cartilage Biochemical and Biophysical Research Communications 267 2000 438-444
115. Sasaki K. Hattori T. Fujisawa T. Takahashi K. Inoue H. Takigawa M. Nitric oxide mediates interleukin-1-induced gene expression of matrix metalloproteinases and basic fibroblast growth factor in cultured rabbit articular chondrocytes Journal of Biochemistry 123 1998 431-439
116. Shakibaei M. Inhibition of chondrogenesis by integrin antibody in vitro Experimental Cell Research 240 1998 95-106
117. Shakibaei M. De Souza P. Merker H.J. Integrin expression and collagen type II implicated in maintenance of chondrocyte shape in monolayer culture (an immunomorphological study) Cell Biology International 21 1997 115-125
118. Shakibaei M. John T. De Souza P. Rahmanzadeh R. Merker H.J. Signal transduction by β1-integrin receptors in human chondrocytes in vitro : collaboration with the insulin-like growth factor-I receptor Biochemical Journal 342 1999 615-623
119. Shakibaei M. Schulze-Tanzil G. De Souza P. John T. Rahmanzadeh M. Rahmanzadeh R. Merker H.J. Inhibition of mitogen-activated protein kinase kinase induces apoptosis of human chondrocytes Journal of Biological Chemistry 276 2001 13289-13294
120. Shay J.W. Bacchetti S. A survey of telomerase activity in human cancer European Journal of Cancer 33 1997 787-791
121. Stadler J. Stefanovic-Racic M. Billiar T.R. Curran R.D. Mcintyre L.A. Georgescu H.I. Simmons R.L. Evans C.H. Articular chondrocytes synthesize nitric oxide in response to cytokines and lipopolysaccharide Journal of Immunology 147 1991 3915-3920
122. Stefanovic-Racic M. Taskiran D. Georgescu H.I. Evans C.H. Modulation of chondrocyte proteoglycan synthesis by endogenously produced nitric oxide Inflammation Research 44 Supplement 2 1995 216-217
123. Stockwell R.A. Cartilage failure in osteoarthritis: relevance of normal structure and function. A review Clinical Anatomy 4 1991 161-191
124. Studer R. Jaffurs D. Stefanovic-Racic M. Robbins P.D. Evans C.H. Nitric oxide in osteoarthritis Osteoarthritis and Cartilage 7 1999 377-379
125. Studer R.K. Levicoff E. Georgescu H. Miller L. Jaffurs D. Evans C.H. Nitric oxide inhibits chondrocyte response to IGF-1 inhibition of IGF-IRβ tyrosine phosphorylation American Journal of Physiology-Cell Physiology 279 2000 C961-C969
126. Sun D. Leung C.L. Liem R.K. Characterization of the microtubule binding domain of microtubule actin cross-linking factor (MACF): identification of a novel group of microtubule associated proteins Journal of Cell Science 114 2001 161-172
127. Susin S.A. Zamzami N. Castedo M. Daugas E. Wang H.-G. Geley S. Fassy F. Reed J.C. Kroemer G. The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Fas/Apo-1/CD95- and ceramide-induced apoptosis Journal of Experimental Medicine 186 1997 25-37
128. Tardif G. Reboul P. Pelletier J.-P. Geng C. Cloutier J.M. Martel-Pelleitier J. Normal expression of type 1 insulin-like growth factor receptor by human osteoarthritic chondrocytes with increased expression and synthesis of insulin-like growth factor binding proteins Arthritis and Rheumatism 1 1996 968-978
129. Taskiran D. Stefanovic-Racic M. Georgescu H. Evans C.H. Nitric oxide mediates suppression of cartilage proteoglycan synthesis by Interleukin-1 Biochemical and Biophysical Research Communications 200 1994 142-148
130. Tirgari M. Vaughan L.C. Arthritis of the canine stifle joint The Veterinary Record 96 1975 394-399
131. Tung J.T. Venta P.J. Caron J.P. Inducible nitric oxide expression in equine articular chondrocytes: effects of antiinflammatory compounds Osteoarthritis and Cartilage 10 2002 5-12
132. Ubeda M. Habener J.F. The large subunit of the DNA replication complex C (DSEB/RF-C140) cleaved and inactivated by caspase-3 (CPP32/YAMA) during Fas-induced apoptosis Journal of Biological Chemistry 272 1997 19562-19568
133. Vignon E. Arlot M. Patricot L.M. Vignon G. The cell density of human femoral head cartilage Clinical Orthopaedics 121 1976 303-308
134. Wang Y. Toury R. Hauchecorne M. Balmain N. Expression of Bcl-2 protein in the epiphyseal plate cartilage and trabecular bone of growing rats Histochemistry and Cell Biology 108 1997 45-55
135. Wikstrom B. Hjerpe A. Hultenby K. Reinholt F.P. Engfeldt B. Stereological analysis of the epiphyseal growth cartilage in the brachymorphic (BM BM) mouse, with special reference to the distribution of matrix vesicles Virchows Archives 47 1984 199-210
136. Westacott C.I. Barakat A.F. Wood L. Perry M.J. Neison P. Bisbinas I. Armstrong L. Millar A.B. Elson C.J. Tumour necrosis factor alpha can contribute to focal loss of cartilage in osteoarthritis Osteoarthritis and Cartilage 8 2000 213-221
137. Wuthier R.E. Chin J.E. Hale J.E. Register T.C. Hale L.V. Ishikawa Y. Isolation and characterization of calcium-accumulating matrix vesicles from chondrocytes of chicken epiphyseal growth plate cartilage in primary culture Journal of Biological Chemistry 260 1985 5972-5979
138. Wyllie A.H. Kerr J.F. Currie A.R. Cell death: the significance of apoptosis International Review of Cytology 68 1980 251-306
139. Yaeger P.C. Masi T.L. Buck De Ortiz J.L. Binette F. Tubo R. Mcpherson J.M. Synergistic action of transforming growth factor-β and insulin-like growth factor-1 induces expression of type II collagen and aggrecan genes in adult human articular chondrocytes Experimental Cell Research 237 1997 318-325
140. Yang C. Li S.W. Helminen H.J. Khillan J.S. Bao Y. Prockop D.J. Apoptosis of chondrocytes in transgenic mice lacking collagen II Experimental Cell Research 235 1997 370-373
141. Yang J. Zhang D. Lao D. Cherry A. Bangs C. Herron G. Telomerase expression affects apoptosis in dermal microvascular endothelial cells The Journal of Investigative Dermatology 112 1999 139
142. Yin X.M. Oltvai Z.N. Korsmeyer S.J. BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax Nature 369 1994 321-323
143. Zhang X. Mar V. Zhou W. Harrington L. Robinson M.O. Telomerase shortening and apoptosis in telomerase-inhibited human tumour cells Genes and Development 13 1999 2388-2399