An overview of underlying causes and animal models for the study of age-related degenerative disorders of the spine and synovial joints

Journal of Orthopaedic Research

Volumn 31, Issue 6, 2013, Pages 831-837

  Vo, Nam ^a,b   Niedernhofer, Laura J ^c   Nasto, Luigi Aurelio ^a,d   Jacobs, Lloydine ^a,b   Robbins, Paul D ^c   Kang, James ^a,b   Evans, Christopher H ^e  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d CATHOLIC UNIVERSITY   (Italy)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

aging; DNA repair; intervertebral disc; oxidative damage; synovial joints

Indexed keywords

ANGIOGENIC FACTOR; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; MATRIX METALLOPROTEINASE; REACTIVE OXYGEN METABOLITE; SCLEROPROTEIN; TRANSCRIPTION FACTOR;

AGING; CADAVER; DNA DAMAGE; DOG; EXTRACELLULAR MATRIX; GENE MUTATION; GUINEA PIG; HUMAN; INTERVERTEBRAL DISK DEGENERATION; LIFESPAN; MOUSE; NONHUMAN; OSTEOARTHRITIS; OSTEOPOROSIS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROGERIA; RABBIT; REVIEW;

AGING; ANIMALS; CARTILAGE, ARTICULAR; DISEASE MODELS, ANIMAL; DNA DAMAGE; DNA-BINDING PROTEINS; ENDONUCLEASES; HUMANS; INTERVERTEBRAL DISC; JOINT DISEASES; OXIDATIVE STRESS; SPINAL DISEASES;

EID: 84876282986     PISSN: 07360266     EISSN: 1554527X     Source Type: Journal    
DOI: 10.1002/jor.22204     Document Type: Review

References (70)

1. Felson DT., 2006. Clinical practice. Osteoarthritis of the knee. N Engl J Med 354: 841-848.
2. Dillon CF, Rasch EK, Gu Q, et al. 2006. Prevalence of knee osteoarthritis in the United States: arthritis data from the Third National Health and Nutrition Examination Survey 1991-1994. J Rheumatol 33: 2271-2279.
3. Goldring MB, Goldring SR., 2007. Osteoarthritis. J Cell Physiol 213: 626-634.
4. Miller JA, Schmatz C, Schultz AB., 1988. Lumbar disc degeneration: correlation with age, sex, and spine level in 600 autopsy specimens. Spine 13: 173-178.
5. Aigner T, Rose J, Martin J, et al. 2004. Aging theories of primary osteoarthritis: from epidemiology to molecular biology. Rejuvenation Res 7: 134-145.
6. Christensen K, Doblhammer G, Rau R, et al. 2009. Ageing populations: the challenges ahead. Lancet 374: 1196-1208.
7. Kirkwood TB., 2005. Understanding the odd science of aging. Cell 120: 437-447.
8. Niedernhofer LJ, Robbins PD., 2008. Signaling mechanisms involved in the response to genotoxic stress and regulating lifespan. Int J Biochem Cell Biol 40: 176-180.
9. Hasty P, Campisi J, Hoeijmakers J, et al. 2003. Aging and genome maintenance: lessons from the mouse ? Science 299: 1355-1359.
10. Guarente L., 2008. Mitochondria-A nexus for aging, calorie restriction, and sirtuins ? Cell 132: 171-176.
11. Finkel T, Holbrook NJ., 2000. Oxidants, oxidative stress and the biology of ageing. Nature 408: 239-247.
12. Di Virgilio F., 2004. New pathways for reactive oxygen species generation in inflammation and potential novel pharmacological targets. Curr Pharm Des 10: 1647-1652.
13. Roughley PJ, Alini M, Antoniou J., 2002. The role of proteoglycans in aging, degeneration and repair of the intervertebral disc. Biochem Soc Trans 30: 869-874.
14. Urban JP, Smith S, Fairbank JC., 2004. Nutrition of the intervertebral disc. Spine (Phila Pa 1976) 29: 2700-2709.
15. Boos N, Weissbach S, Rohrbach H, et al. 2002. Classification of age-related changes in lumbar intervertebral discs: 2002 Volvo Award in basic science. Spine (Phila Pa 1976) 27: 2631-2644.
16. Edelson JG, Nathan H., 1988. Stages in the natural history of the vertebral end-plates. Spine (Phila Pa 1976) 13: 21-26.
17. Bibby SR, Jones DA, Ripley RM, et al. 2005. Metabolism of the intervertebral disc: effects of low levels of oxygen, glucose, and pH on rates of energy metabolism of bovine nucleus pulposus cells. Spine (Phila Pa 1976) 30: 487-496.
18. Adams MA, Roughley PJ., 2006. What is intervertebral disc degeneration, and what causes it ? Spine (Phila Pa 1976) 31: 2151-2161.
19. Roughley PJ., 2006. The structure and function of cartilage proteoglycans. Eur Cell Mater 12: 92-101.
20. Martin JA, Buckwalter JA., 2001. Roles of articular cartilage aging and chondrocyte senescence in the pathogenesis of osteoarthritis. Iowa Orthop J 21: 1-7.
21. Buckwalter JA, Roughley PJ, Rosenberg LC., 1994. Age-related changes in cartilage proteoglycans: quantitative electron microscopic studies. Microsc Res Tech 28: 398-408.
22. Martin JA, Buckwalter JA., 2001. Telomere erosion and senescence in human articular cartilage chondrocytes. J Gerontol A Biol Sci Med Sci 56: B172-B179.
23. Zhou HW, Lou SQ, Zhang K., 2004. Recovery of function in osteoarthritic chondrocytes induced by p16INK4a-specific siRNA in vitro. Rheumatology (Oxford) 43: 555-568.
24. Kirkwood TB., 1998. Biological theories of aging: an overview. Aging (Milano) 10: 144-146.
25. Loeser RF., 2009. Aging and osteoarthritis: the role of chondrocyte senescence and aging changes in the cartilage matrix. Osteoarthritis Cartilage 17: 971-979.
26. Jallali N, Ridha H, Thrasivoulou C, et al. 2005. Vulnerability to ROS-induced cell death in ageing articular cartilage: the role of antioxidant enzyme activity. Osteoarthritis Cartilage 13: 614-622.
27. Nerlich AG, Bachmeier BE, Schleicher E, et al. 2007. Immunomorphological analysis of RAGE receptor expression and NF-kappaB activation in tissue samples from normal and degenerated intervertebral discs of various ages. Ann N Y Acad Sci 1096: 239-248.
28. Tiku ML, Liesch JB, Robertson FM., 1990. Production of hydrogen peroxide by rabbit articular chondrocytes. Enhancement by cytokines. J Immunol 145: 690-696.
29. McMillan TJ, Leatherman E, Ridley A, et al. 2008. Cellular effects of long wavelength UV light (UVA) in mammalian cells. J Pharm Pharmacol 60: 969-976.
30. Jallali N, Ridha H, Thrasivoulou C, et al. 2007. Modulation of intracellular reactive oxygen species level in chondrocytes by IGF-1, FGF, and TGF-beta1. Connect Tissue Res 48: 149-158.
31. Del Carlo M, Schwartz D, Erickson EA, et al. 2007. Endogenous production of reactive oxygen species is required for stimulation of human articular chondrocyte matrix metalloproteinase production by fibronectin fragments. Free Radic Biol Med 42: 1350-1358.
32. Davies CM, Guilak F, Weinberg JB, et al. 2008. Reactive nitrogen and oxygen species in interleukin-1-mediated DNA damage associated with osteoarthritis. Osteoarthritis Cartilage 16: 624-630.
33. Ali R, Le Maitre CL, Richardson SM, et al. 2008. Connective tissue growth factor expression in human intervertebral disc: implications for angiogenesis in intervertebral disc degeneration. Biotech Histochem 83: 239-245.
34. Carlo MD Jr, Loeser RF., 2003. Increased oxidative stress with aging reduces chondrocyte survival: correlation with intracellular glutathione levels. Arthritis Rheum 48: 3419-3430.
35. Ruiz-Romero C, Calamia V, Mateos J, et al. 2009. Mitochondrial dysregulation of osteoarthritic human articular chondrocytes analyzed by proteomics: a decrease in mitochondrial superoxide dismutase points to a redox imbalance. Mol Cell Proteomics 8: 172-189.
36. Reiter CD, Teng RJ, Beckman JS., 2000. Superoxide reacts with nitric oxide to nitrate tyrosine at physiological pH via peroxynitrite. J Biol Chem 275: 32460-32466.
37. Loeser RF, Carlson CS, Del Carlo M, et al. 2002. Detection of nitrotyrosine in aging and osteoarthritic cartilage: correlation of oxidative damage with the presence of interleukin-1beta and with chondrocyte resistance to insulin-like growth factor 1. Arthritis Rheum 46: 2349-2357.
38. Yin W, Park JI, Loeser RF., 2009. Oxidative stress inhibits insulin-like growth factor-I induction of chondrocyte proteoglycan synthesis through differential regulation of phosphatidylinositol 3-Kinase-Akt and MEK-ERK MAPK signaling pathways. J Biol Chem 284: 31972-31981.
39. Loeser RF, Shanker G, Carlson CS, et al. 2000. 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 43: 2110-2120.
40. Baker MS, Feigan J, Lowther DA., 1988. Chondrocyte antioxidant defences: the roles of catalase and glutathione peroxidase in protection against H2O2 dependent inhibition of proteoglycan biosynthesis. J Rheumatol 15: 670-677.
41. Bank RA, Bayliss MT, Lafeber FP, et al. 1998. Ageing and zonal variation in post-translational modification of collagen in normal human articular cartilage. The age-related increase in non-enzymatic glycation affects biomechanical properties of cartilage. Biochem J 330: 345-351.
42. Sivan SS, Tsitron E, Wachtel E, et al. 2006. Age-related accumulation of pentosidine in aggrecan and collagen from normal and degenerate human intervertebral discs. Biochem J 399: 29-35.
43. Verzijl N, DeGroot J, Thorpe SR, et al. 2000. Effect of collagen turnover on the accumulation of advanced glycation end products. J Biol Chem 275: 39027-39031.
44. DeGroot J, Verzijl N, Bank RA, et al. 1999. Age-related decrease in proteoglycan synthesis of human articular chondrocytes: the role of nonenzymatic glycation. Arthritis Rheum 42: 1003-1009.
45. DeGroot J, Verzijl N, Wenting-van Wijk MJ, et al. 2004. Accumulation of advanced glycation end products as a molecular mechanism for aging as a risk factor in osteoarthritis. Arthritis Rheum 50: 1207-1215.
46. Bendele AM., 2001. Animal models of osteoarthritis. J Musculoskelet Neuronal Interact 1: 363-376.
47. Gruber HE, Ingram JA, Norton HJ, et al. 2007. Senescence in cells of the aging and degenerating intervertebral disc: immunolocalization of senescence-associated beta-galactosidase in human and sand rat discs. Spine 32: 321-327.
48. Lotz JC., 2004. Animal models of intervertebral disc degeneration: lessons learned. Spine (Phila Pa 1976) 29: 2742-2750.
49. Sobajima S, Kompel JF, Kim JS, et al. 2005. A slowly progressive and reproducible animal model of intervertebral disc degeneration characterized by MRI, X-ray, and histology. Spine 30: 15-24.
50. Ameye LG, Young MF., 2006. Animal models of osteoarthritis: lessons learned while seeking the 'Holy Grail'. Curr Opin Rheumatol 18: 537-547.
51. Raducanu A, Aszõdi A., 2008. Knock-out mice in osteoarthritis research. Curr Rheumatol Rev 4: 1-10.
52. Neuhold LA, Killar L, Zhao W, et al. 2001. Postnatal expression in hyaline cartilage of constitutively active human collagenase-3 (MMP-13) induces osteoarthritis in mice. J Clin Invest 107: 35-44.
53. Sahebjam S, Khokha R, Mort JS., 2007. Increased collagen and aggrecan degradation with age in the joints of Timp3(-/-) mice. Arthritis Rheum 56: 905-909.
54. Saamanen AM, Vuorio E., 2004. Generation and use of transgenic mice as models of osteoarthritis. Methods Mol Med 101: 1-23.
55. Young MF., 2005. Mouse models of osteoarthritis provide new research tools. Trends Pharmacol Sci 26: 333-335.
56. Bomsta BD, Bridgewater LC, Seegmiller RE., 2006. Premature osteoarthritis in the disproportionate micromelia (Dmm) mouse. Osteoarthritis Cartilage 14: 477-485.
57. Zemmyo M, Meharra EJ, Kuhn K, et al. 2003. Accelerated, aging-dependent development of osteoarthritis in alpha1 integrin-deficient mice. Arthritis Rheum 48: 2873-2880.
58. Matsui Y, Iwasaki N, Kon S, et al. 2009. Accelerated development of aging-associated and instability-induced osteoarthritis in osteopontin-deficient mice. Arthritis Rheum 60: 2362-2371.
59. 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.
60. Vo N, Seo HY, Robinson A, et al. 2010. Accelerated aging of intervertebral discs in a mouse model of progeria. J Orthop Res 28: 1600-1607.
61. Tyner SD, Venkatachalam S, Choi J, et al. 2002. p53 mutant mice that display early ageing-associated phenotypes. Nature 415: 45-53.
62. Hishiya A, Ito M, Aburatani H, et al. 2005. Ataxia telangiectasia mutated (Atm) knockout mice as a model of osteopenia due to impaired bone formation. Bone 37: 497-503.
63. Mounkes LC, Kozlov S, Hernandez L, et al. 2003. A progeroid syndrome in mice is caused by defects in A-type lamins. Nature 423: 298-301.
64. Hosokawa M., 2002. A higher oxidative status accelerates senescence and aggravates age-dependent disorders in SAMP strains of mice. Mech Ageing Dev 123: 1553-1561.
65. Kuro-o M, Matsumura Y, Aizawa H, et al. 1997. Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390: 45-51.
66. de Boer J, Andressoo JO, de Wit J, et al. 2002. Premature aging in mice deficient in DNA repair and transcription. Science 296: 1276-1279.
67. Botter SM, Zar M, van Osch GJ, et al. 2011. Analysis of osteoarthritis in a mouse model of the progeroid human DNA repair syndrome trichothiodystrophy. Age (Dordr) 33: 247-260.
68. Gruber HE, Gordon B, Williams C, et al. 2007. Vertebral endplate and disc changes in the aging sand rat lumbar spine: cross-sectional analyses of a large male and female population. Spine 32: 2529-2536.
69. Niedernhofer LJ, Garinis GA, Raams A, et al. 2006. A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis. Nature 444: 1038-1043.
70. de Waard MC, van der Pluijm I, Zuiderveen Borgesius N, et al. 2010. Age-related motor neuron degeneration in DNA repair-deficient Ercc1 mice. Acta Neuropathol 120: 461-475.