Effects of Oxidative Damage and Telomerase Activity on Human Articular Cartilage Chondrocyte Senescence

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 59, Issue 4, 2004, Pages 324-337

  Martin, James A ^a   Klingelhutz, Aloysius J ^b   Moussavi Harami, Farid ^a   Buckwalter, Joseph A ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TELOMERASE;

ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CELL AGING; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PRIORITY JOURNAL;

EID: 1842781743     PISSN: 10795006     EISSN: None     Source Type: Journal    
DOI: 10.1093/gerona/59.4.b324     Document Type: Article

References (90)

1. Buckwalter JA, Heckman JD, Petrie DP. An AOA critical issue. Aging of the North American population: new challenges for orthopaedics. J Bone Joint Surg Am. 2003;85A:748-758.
2. Praemer A, Furner S, Rice DP. Musculoskeletal Conditions in the United States. Rosemont IL: American Academy of Orthopaedic Surgeons; 1999.
3. Buckwalter JA, Mankin HJ. Articular cartilage II. Degeneration and osteoarthrosis, repair, regeneration and transplantation. J Bone Joint Surg. 1997;79A:612-632.
4. Buckwalter JA, Martin JA, Mankin HJ. Synovial joint degeneration and the syndrome of osteoarthritis. Instructional Course Lectures. 2000;49:481-489.
5. Buckwalter JA, Lappin DR. The disproportionate impact of chronic arthralgia and arthritis among women. Clin Orthop Rel Res. 2000;372:159-168.
6. Felson DT. The epidemiology of osteoarthritis: prevalence and risk factors. In: KE Kuettner, VM Goldberg, eds. Osteoarthritic Disorders. Rosemont, IL: American Academy of Orthopaedic Surgeons; 1995:13-24.
7. Buckwalter JA, Mankin HJ. Articular cartilage I. Tissue design and chondrocyte-matrix interactions. J Bone Joint Surg. 1997;79A:600-611.
8. Martin JA, Buckwalter JA. The role of chondrocyte senescence in the pathogenesis of osteoarthritis and in limiting cartilage repair. J Bone Joint Surg Am. 2003;85A(Suppl 2):106-110.
9. Buckwalter JA, Choi H, Tang L, Rosenberg L, Ungar R. The effect of link protein concentration of proteoglycan aggregation. Trans 32nd Meeting Ortho Res Soc. 1986;11:98.
10. Buckwalter JA, Rosenberg LC. Electron microscopic studies of cartilage proteoglycans. Elec Microsc Rev. 1988;1:87-112.
11. Buckwalter JA, Roughley PJ, Rosenberg LC. Age-related changes in cartilage proteoglycans: quantitative electron microscopic studies. Micros Res Tech. 1994;28:398-408.
12. Buckwalter JA, Rosenberg LC. Electron microscopic studies of cartilage proteoglycans: Direct evidence for the variable length of the chondroitin sulfate rich region of the proteoglycan subunit core protein. J Biol Chem. 1982;257:9830-9839.
13. Verbruggen G, Comelissen M, Almqvist KF, Wang L, Elewaut D, Broddelez C, de Ridder L, Veys EM. Influence of aging on the synthesis and morphology of the aggrecans synthesized by differentiated human articular chondrocytes. Osteoarthritis Cartilage. 2000;8:170-179.
14. Martin JA, Buckwalter JA. Telomere erosion and senescence in human articular cartilage chondrocytes. J Gerontol Biol Sci. 2001;56A:B172-B179.
15. Bolton MC, Dudhia J, Bayliss MT. Age-related changes in the synthesis of link protein and aggrecan in human articular cartilage: implications for aggregate stability. Biochem J. 1999;337:77-82.
16. Martin JA, Ellerbroek SM, Buckwalter JA. The age-related decline in chondrocyte response to insulin-like growth factor-I: the role of growth factor binding proteins. J Ortho Res. 1997;15:491-498.
17. Martin JA, Buckwalter JA. The role of chondrocyte-matrix interactions in maintaining and repairing articular cartilage. Biorheology. 2000;37:129-140.
18. Loeser RF, Shanker G, Carlson CS, Gardin JF, Shelton BJ, Sonntag WE. Reduction in the chondrocyte response to insulin-like growth factor 1 in aging and osteoarthritis: studies in a non-human primate model of naturally occurring disease. Arthritis Rheum. 2000;43:2110-2120.
19. Guerne PA, Blanco F, Kaelin A, Desgeorges A, Lotz M. Growth factor responsiveness of human articular chondrocytes in aging and development. Arthritis Rheum. 1995;38:960-968.
20. Scharstuhl A, van Beuningen HM, Vitters EL, van der Kraan PM, van den Berg WB. Loss of transforming growth factor counteraction on interleukin 1 mediated effects in cartilage of old mice. Ann Rheum Dis. 2002;61:1095-1098.
21. Martin JA, Buckwalter JA. Human chondrocyte senescence and osteoarthritis. Biorheology. 2002;39:145-152.
22. Felson DT, Hannan MT, Naimark A, Berkley J. Occupational physical demands, knee bending, and knee osteoarthritis: results from the Framingham study. J Rheumatol. 1991;18:1587-1592.
23. Felson DT, Zhang Y, Anthony JM, Naimark A, Anderson JJ. Weight loss reduces the risk for symptomatic knee osteoarthritis in women. Ann Intern Med. 1992;116:535-539.
24. Felson DT. Occupation and knee osteoarthritis: evidence from two population-based studies. Acta Orthop Scand. 1993;64(Suppl 253): 56-57.
25. Buckwalter JA. Osteoarthritis and articular cartilage use, disuse and abuse: experimental studies. J Rheumatol. 1995;22(Suppl 43):13-15.
26. Buckwalter JA, Lane NE. Aging, sports and osteoarthritis. Sports Med Arth Rev. 1996;4:276-287.
27. Buckwalter JA, Lane NE. Athletics and osteoarthritis. Am J Sports Med. 1997;25:873-881.
28. Axmacher B, Lindberg H. Coxarthrosis in farmers. Acta Orthop Scand. 1993;64(Suppl 253):59.
29. Lindberg H, Montgomery F. Heavy labor and the occurrence of gonarthrosis. Clin Orthop Rel Res. 1987;214:235-236.
30. Lindberg H, Roos H, Gardsell P. The relationship between soccer and coxarthrosis. Acta Orthop Scand. 1993;64(Suppl 253):60.
31. Roos H, Lindberg H, Gardsell P, Wingstrand H. The prevalence of gonarthrosis in former soccer players and its relationship to menisectomy. Acta Orthop Scand. 1993;64(Suppl 253):60.
32. Maxian TA, Brown TD, Weinstein SL. Chronic stress tolerance levels for human articular cartilage: two nonuniform contact models applied to long-term follow-up of CDH. J Biomech. 1995;28:159-166.
33. Elsaid KA, Jay GD, Chichester CO. Detection of collagen type II and proteoglycans in the synovial fluids of patients diagnosed with non-infectious knee joint synovitis indicates early damage to the articular cartilage matrix. Osteoarthritis Cartilage. 2003;11:673-680.
34. Ishiguro N, Ito T, Oguchi T, Kojima T, Iwata H, Ionescu M, Poole AR. Relationships of matrix metalloproteinases and their inhibitors to cartilage proteoglycan and collagen turnover and inflammation as revealed by analyses of synovial fluids from patients with rheumatoid arthritis. Arthritis Rheum. 2001;44:2503-2511.
35. Goldbach-Mansky R, Lee JM, Hoxworth JM, et al. Active synovial matrix metalloproteinase-2 is associated with radiographic erosions in patients with early synovitis. Arthritis Res. 2000;2:145-153.
36. Smith MD, Triantafillou S, Parker A, Youssef PP, Coleman M. Synovial membrane inflammation and cytokine production in patients with early osteoarthritis. J Rheumatol. 1997;24:365-371.
37. Harris ED Jr. The rationale for combination therapy of rheumatoid arthritis based on pathophysiology. J Rheumatol Suppl. 1996;44:2-4.
38. Edmonds SE, Blake DR, Morris CJ, Winyard PG. An imaginative approach to synovitis-the role of hypoxic reperfusion damage in arthritis. J Rheumatol Suppl. 1993;37:26-31.
39. Mapp PI, Grootveld MC, Blake DR. Hypoxia, oxidative stress and rheumatoid arthritis. Br Med Bull. 1995;51:419-436.
40. Nagai H, Kumamoto H, Fukuda M, Takahashi T. Inducible nitric oxide synthase and apoptosis-related factors in the synovial tissues of temporomandibular joints with internal derangement and osteoarthritis. J Oral Maxillofac Surg. 2003;61:801-807.
41. Buckwalter JA. Mechanical injuries of articular cartilage. In: G Finerman G, ed. Biology and Biomechanics of the Traumatized Synovial Joint. Park Ridge, IL: American Academy of Orthopaedic Surgeons; 1992:83-96.
42. Marsh JL, Buckwalter JA, Gelberman R, et al. AOA Symposium. Articular fractures: does an anatomic reduction really change the result? J Bone Joint Surg. 2002;84A:1259-1271.
43. Heiner AD, Martin JA, Brown TD. Cartilage responses to stress in a novel triaxial mechanical stress culture system. Transcript of the 4th Combined Orthopaedic Research Societies Meeting, 2001:141.
44. Heiner AD, Martin JA. Cartilage responses to a novel triaxial mechanostimulatory culture system. J Biomech. In Press.
45. Martin JA, Brown T, Heiner A, Buckwalter JA. Post-traumatic osteoarthritis: the role of accelerated chondrocyte senescence. Biorheology. In Press.
46. Martin JA, Mitchell CJ, Klingelhutz AJ, Buckwalter JA. Effects of telomerase and viral oncogene expression on the in vitro growth of human chondrocytes. J Gerontol Biol Sci. 2002;57A:B48-B53.
47. Martin JA, Forest E, Block JA, et al. Malignant transformation in human chondrosarcoma cells supported by telomerase activation and tumor suppressor inactivation. Cell Growth Diff. 2002;13:397-407.
48. Grimshaw MJ, Mason RM. Modulation of bovine articular chondrocyte gene expression in vitro by oxygen tension. Osteoarthritis Cartilage. 2001;9:357-364.
49. Murphy CL, Sambanis A. Effect of oxygen tension and alginate encapsulation on restoration of the differentiated phenotype of passaged chondrocytes. Tissue Eng. 2001;7:791-803.
50. Grimshaw MJ, Mason RM. Bovine articular chondrocyte function in vitro depends upon oxygen tension. Osteoarthritis Cartilage. 2000;8:386-392.
51. DeGroot H, Littauer A. Hypoxia, reactive oxygen, and cell injury. Free Radic Biol. Med. 1989;173:541-551.
52. Yusa T, Crapo JD, Freeman BA. Hyperoxia enhances lung and liver nuclear superoxide generation. Biochim Biophys Acta. 1984;798:167-174.
53. Turrens JF, Freeman BA, Levitt JG, Crapo JD. The effect of hyperoxia on superoxide production by lung submitochondrial particles. Arch Biochem Biophys. 1982;217:401-410.
54. Packer L, Fuehr K. Low oxygen concentration extends the lifespan of cultured human diploid cells. Nature. 1977;267:423-425.
55. von Zglinicki T, Saretzki G, Docke W, Lotze C. Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts: a model for senescence? Exp Cell Res. 1995;220:186-193.
56. Balin AK, Fisher AJ, Anzelone M, Leong I, Allen RG. Effects of establishing cell cultures and cell culture conditions on the proliferative life span of human fibroblasts isolated from different tissues and donors of different ages. Exp Cell Res. 2002;274:275-287.
57. Parrinello S, Samper E, Krtolica A, Goldstein J, Melov S, Campisi J. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat Cell Biol. 2003;5:741-747.
58. Johnston JC, Gasmi M, Lim LE, et al. Minimum requirements for efficient transduction of dividing and nondividing cells by feline immunodeficiency virus vectors. J Virol. 1999;73:4991-5000.
59. Hughes SM, Moussavi-Harami F, Sauter SL, Davidson BL. Viral-mediated gene transfer to mouse primary neural progenitor cells. Mol Ther. 2002;5:16-24.
60. Dimri G, Lee X, Basile G, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A. 1995;92:9363-9367.
61. Varanasi SS, Datta HK. Southern analysis of mitochondrial DNA in cortical bone of elderly patients undergoing knee and hip arthroplasty. J Pathol. 2001;193:557-562.
62. Tengan CH, Moraes CT. Detection and analysis of mitochondrial DNA deletions by whole genome PCR. Biochem Mol Med. 1996;58:130-134.
63. Kang CM, Kristal BS, Yu BP. Age-related mitochondrial DNA deletions: effect of dietary restriction. Free Rad Biol Med. 1998;24:148-154.
64. Kopsidas G, Kovalenko SA, Kelso JM, Linnane AW. An age-associated correlation between cellular bioenergy decline and mtDNA rearrangements in human skeletal muscle. Mutation Res. 1998;421:27-36.
65. Lee CM, Weindrich R, Aiken JM. Age-related alterations of the mitochondrial genome. Free Rad Biol Med. 1997;22:1259-1269.
66. Rajpurohit R, Mansfield K, Ohyama K, Ewert D, Shapiro IM. Chondrocyte death is linked to development of a mitochondrial membrane permeability transition in the growth plate. J Cell Physiol. 1999;179:287-296.
67. Li W, Miller F, Brown M, et al. Enhanced H2O2-induced cytotoxicity in "epithelioid" smooth muscle cells implications for neointimal regression. Arterioscler Thromb Vasc Biol. 2000;20:1473-1479.
68. Hayflick L, Moorhead PS. The serial cultivation of human diploid cell strains. Exp Cell Res. 1961;25:585-621.
69. Hayflick L. The limited in vitro lifetime of human diploid cell strains. Exp Cell Res. 1965;37:614-636.
70. Hayflick L. The longevity of cultured human cells. J Am Geriatr Soc. 1974;22:1-12.
71. Allsopp RC, Chang E, Kashefi-Aazam M, et al. Telomere shortening is associated with cell division in vitro and in vivo. Exp Cell Res. 1995;220:194-200.
72. Liu L, Trimarchi JR, Navarro P, Blasco MA, Keefe DL. Oxidative stress contributes to arsenic-induced telomere attrition, chromosome instability and apoptosis. J Biol Chem. 2003;278:31998-2004.
73. Furumoto K, Inoue E, Nagao N, Hiyama E, Miwa N. Age-dependent telomere shortening is slowed down by enrichment of intracellular vitamin C via suppression of oxidative stress. Life Sci. 1998;63:935-948.
74. Szalai VA, Singer MJ, Thorp HH. Site-specific probing of oxidative reactivity and telomerase function using 7,8-dihydro-8-oxoguanine in telomeric DNA. J Am Chem Soc. 2002;124:1625-1631.
75. Herbert BS, Wright WE, Shay JW. p16(INK4a) inactivation is not required to immortalize human mammary epithelial cells. Oncogene. 2002;21:7897-7900.
76. Mobasheri A. Role of chondrocyte death and hypocellularity in ageing human articular cartilage and the pathogenesis of osteoarthritis. Med Hypotheses. 2002;58:193-197.
77. Aigner T, Hemmel M, Neureiter D, et al. 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 Rheum. 2001;44:1304-1312.
78. Kusuzaki K, Sugimoto S, Takeshita H, et al. DNA cytofluorometric analysis of chondrocytes in human articular cartilages under normal aging or arthritic conditions. Osteoarthritis Cartilage. 2001;9:664-670.
79. Buckwalter JA, Mow VC, Hunziker EB. Concepts of cartilage repair in osteoarthritis. In: R Moskowitz, VM Goldberg, D Howell, R Altman, JA Buckwalter, eds. Osteoarthritis: Diagnosis and Medical/Surgical Management. 3rd Ed. Philadelphia, PA: Saunders; 2001:101-114.
80. Toussaint O, Medrano E, Zglinicki Tv. Cellular and molecular mechanisms of stress-induced premature senescence (sips) of human diploid fibroblasts and melanocytes. Exp Gerontol. 2000;35:927-945.
81. Dumont P, Chen QM, Burton M, et al. Induction of replicative senescence biomarkers by sublethal oxidative stress in normal human fibroblasts. Free Rad Biol Med. 2000;28:361-373.
82. Golden T, Melov S. Mitochondrial DNA mutations, oxidative stress, and aging. Mech Ageing Dev. 2001;122:1577-1589.
83. Arnheim N, Cortopassi G. Deleterious mitochondrial DNA mutations accumulate in aging human tissues. Mutation Res. 1992;275:157-167.
84. Beckman KB, Ames BN. Endogenous oxidative damage of mtDNA. Mutat Res. 1999;424:51-58.
85. Beckman KB, Ames BN. Oxidative decay of DNA. J Biol Chem. 1997;272:19633-19636.
86. Rajpurohit R, Koch CJ, Tao Z, Teixeira CM, Shapiro IM. Adaptation of chondrocytes to low oxygen tension: relationship between hypoxia and cellular metabolism. J Cell Physiol. 1996;168:424-432.
87. Henrotin Y, Deby-Dupont G, Deby C, De Bruyn M, Lamy M, Franchimont P. Production of active oxygen species by isolated human chondrocytes. Br J Rheumatol. 1993;32:562-567.
88. Mazzetti I, Grigolo B, Pulsatelli L, et al. Differential roles of nitric oxide and oxygen radicals in chondrocytes affected by osteoarthritis and rheumatoid arthritis. Clin Sci (Lond). 2001;101:593-599.
89. Roosendaal G, Vianen ME, Marx JJ, van den Berg HM, Lafeber FP, Bijlsma JW. Blood-induced joint damage: a human in vitro study. Arthritis Rheum. 1999;42:1025-032.
90. Schett G, Tohidast-Akrad M, Steiner G, Smolen J. The stressed synovium. Arthritis Res. 2001;3:80-86.