Mitochondrial dysfunction in osteoarthritis is associated with down-regulation of superoxide dismutase 2

Arthritis and Rheumatism

Volumn 65, Issue 2, 2013, Pages 378-387

  Gavriilidis, Christos ^a,b   Miwa, Satomi ^a   Von Zglinicki, Thomas ^a   Taylor, Robert W ^a   Young, David A ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MALONALDEHYDE; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL DNA; PROTON; RNA; SMALL INTERFERING RNA; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ARTICLE; ARTICULAR CARTILAGE; BREATHING; CARTILAGE CELL; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; DNA STRAND BREAKAGE; FEMUR NECK FRACTURE; GENE REARRANGEMENT; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOASSAY; IMMUNOBLOTTING; LIPID PEROXIDATION; MICROSCALE OXYGRAPHY; MITOCHONDRIAL RESPIRATION; NUCLEOTIDE SEQUENCE; OSTEOARTHRITIS; OXIDATIVE STRESS; PHOTOGRAPHY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SPARE RESPIRATORY CAPACITY;

CARTILAGE, ARTICULAR; CELLS, CULTURED; CHONDROCYTES; DOWN-REGULATION; HUMANS; LIPID PEROXIDATION; MITOCHONDRIA; OSTEOARTHRITIS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 84873850757     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.37782     Document Type: Article

References (50)

1. Lister R, Hulett JM, Lithgow T, Whelan J,. Protein import into mitochondria: origins and functions today [review]. Mol Membr Biol 2005; 22: 87-100.
2. Turrens JF,. Mitochondrial formation of reactive oxygen species. J Physiol 2003; 552: 335-44.
3. Zelko IN, Mariani TJ, Folz RJ,. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med 2002; 33: 337-49.
4. Brandt KD, Radin EL, Dieppe PA, van de Putte L,. Yet more evidence that osteoarthritis is not a cartilage disease. Ann Rheum Dis 2006; 65: 1261-4.
5. Lee RB, Urban JP,. Evidence for a negative Pasteur effect in articular cartilage. Biochem J 1997; 321: 95-102.
6. Stockwell RA,. Metabolism of cartilage. In:, Hall BK, editor. Cartilage. Vol. 1. Structure function and biochemistry. London: Academic Press; 1983. p. 253-73.
7. Cillero-Pastor B, Carames B, Lires-Dean M, Vaamonde-Garcia C, Blanco FJ, Lopez-Armada MJ,. Mitochondrial dysfunction activates cyclooxygenase 2 expression in cultured normal human chondrocytes. Arthritis Rheum 2008; 58: 2409-19.
8. Maneiro E, Martin MA, de Andres MC, Lopez-Armada MJ, Fernandez-Sueiro JL, del Hoyo P, et al. Mitochondrial respiratory activity is altered in osteoarthritic human articular chondrocytes. Arthritis Rheum 2003; 48: 700-8.
9. Chang MC, Hung SC, Chen WY, Chen TL, Lee CF, Lee HC, et al. Accumulation of mitochondrial DNA with 4977-bp deletion in knee cartilage-an association with idiopathic osteoarthritis. Osteoarthritis Cartilage 2005; 13: 1004-11.
10. Henrotin Y, Kurz B, Aigner T,. Oxygen and reactive oxygen species in cartilage degradation: friends or foes? Osteoarthritis Cartilage 2005; 13: 643-54.
11. Loeser RF, Carlson CS, Del Carlo M, Cole A,. Detection of nitrotyrosine in aging and osteoarthritic cartilage: correlation of oxidative damage with the presence of interleukin-1β and with chondrocyte resistance to insulin-like growth factor 1. Arthritis Rheum 2002; 46: 2349-57.
12. Tiku ML, Shah R, Allison GT,. Evidence linking chondrocyte lipid peroxidation to cartilage matrix protein degradation: possible role in cartilage aging and the pathogenesis of osteoarthritis. J Biol Chem 2000; 275: 20069-76.
13. Gao F, Koenitzer JR, Tobolewski JM, Jiang D, Liang J, Noble PW, et al. Extracellular superoxide dismutase inhibits inflammation by preventing oxidative fragmentation of hyaluronan. J Biol Chem 2008; 283: 6058-66.
14. Petersen SV, Oury TD, Ostergaard L, Valnickova Z, Wegrzyn J, Thogersen IB, et al. Extracellular superoxide dismutase (EC-SOD) binds to type I collagen and protects against oxidative fragmentation. J Biol Chem 2004; 279: 13705-10.
15. Scott JL, Gabrielides C, Davidson RK, Swingler TE, Clark IM, Wallis GA, et al. Superoxide dismutase downregulation in osteoarthritis progression and end-stage disease. Ann Rheum Dis 2010; 69: 1502-10.
16. Aigner T, Fundel K, Saas J, Gebhard PM, Haag J, Weiss T, et al. Large-scale gene expression profiling reveals major pathogenetic pathways of cartilage degeneration in osteoarthritis. Arthritis Rheum 2006; 54: 3533-44.
17. Regan E, Flannelly J, Bowler R, Tran K, Nicks M, Carbone BD, et al. Extracellular superoxide dismutase and oxidant damage in osteoarthritis. Arthritis Rheum 2005; 52: 3479-91.
18. Ruiz-Romero C, Calamia V, Mateos J, Carreira V, Martinez-Gomariz M, Fernandez M, et al. Mitochondrial dysregulation of osteoarthritic human articular chondrocytes analyzed by proteomics: a decrease in mitochondrial superoxide dismutase points to a redox imbalance. Mol Cell Proteomics 2009; 8: 172-89.
19. Zhang Q, Hui W, Litherland GJ, Barter MJ, Davidson R, Darrah C, et al. Differential Toll-like receptor-dependent collagenase expression in chondrocytes. Ann Rheum Dis 2008; 67: 1633-41.
20. Passos JF, Saretzki G, Ahmed S, Nelson G, Richter T, Peters H, et al. Mitochondrial dysfunction accounts for the stochastic heterogeneity in telomere-dependent senescence. PLoS Biol 2007; 5: e110.
21. Brand MD, Nicholls DG,. Assessing mitochondrial dysfunction in cells. Biochem J 2011; 435: 297-312.
22. Brand MD,. The efficiency and plasticity of mitochondrial energy transduction. Biochem Soc Trans 2005; 33: 897-904.
23. Birket MJ, Orr AL, Gerencser AA, Madden DT, Vitelli C, Swistowski A, et al. A reduction in ATP demand and mitochondrial activity with neural differentiation of human embryonic stem cells. J Cell Sci 2011; 124: 348-58.
24. Blanco FJ, Rego I, Ruiz-Romero C,. The role of mitochondria in osteoarthritis. Nat Rev Rheumatol 2011; 7: 161-9.
25. Vaamonde-Garcia C, Riveiro-Naveira RR, Valcarcel-Ares MN, Hermida-Carballo L, Blanco FJ, Lopez-Armada MJ,. Mitochondrial dysfunction increases inflammatory responsiveness to cytokines in normal human chondrocytes. Arthritis Rheum 2012; 64: 2927-36.
26. Fernandez-Moreno M, Soto-Hermida A, Pertega S, Oreiro N, Fernandez-Lopez C, Rego-Perez I, et al. Mitochondrial DNA (mtDNA) haplogroups and serum levels of anti-oxidant enzymes in patients with osteoarthritis. BMC Musculoskelet Disord 2011; 12: 264.
27. Rego I, Fernandez-Moreno M, Fernandez-Lopez C, Gomez-Reino JJ, Gonzalez A, Arenas J, et al. Role of European mitochondrial DNA haplogroups in the prevalence of hip osteoarthritis in Galicia, Northern Spain. Ann Rheum Dis 2010; 69: 210-3.
28. Rego-Perez I, Fernandez-Moreno M, Deberg M, Pertega S, Fenandez-Lopez C, Oreiro N, et al. Mitochondrial DNA haplogroups modulate the serum levels of biomarkers in patients with osteoarthritis. Ann Rheum Dis 2010; 69: 910-7.
29. Rego-Perez I, Fernandez-Moreno M, Deberg M, Pertega S, Fernandez-Lopez C, Oreiro N, et al. Mitochondrial DNA haplogroups and serum levels of proteolytic enzymes in patients with osteoarthritis. Ann Rheum Dis 2011; 70: 646-52.
30. Rego-Perez I, Fernandez-Moreno M, Fernandez-Lopez C, Arenas J, Blanco FJ,. Mitochondrial DNA haplogroups: role in the prevalence and severity of knee osteoarthritis. Arthritis Rheum 2008; 58: 2387-96.
31. Brand MD,. The sites and topology of mitochondrial superoxide production. Exp Gerontol 2010; 45: 466-72.
32. Sciacco M, Bonilla E, Schon EA, DiMauro S, Moraes CT,. Distribution of wild-type and common deletion forms of mtDNA in normal and respiration-deficient muscle fibers from patients with mitochondrial myopathy. Hum Mol Genet 1994; 3: 13-9.
33. Hayakawa M, Hattori K, Sugiyama S, Ozawa T,. Age-associated oxygen damage and mutations in mitochondrial DNA in human hearts. Biochem Biophys Res Commun 1992; 189: 979-85.
34. Krishnan KJ, Reeve AK, Samuels DC, Chinnery PF, Blackwood JK, Taylor RW, et al. What causes mitochondrial DNA deletions in human cells? Nat Genet 2008; 40: 275-9.
35. Zhang C, Baumer A, Mackay IR, Linnane AW, Nagley P,. Unusual pattern of mitochondrial DNA deletions in skeletal muscle of an adult human with chronic fatigue syndrome. Hum Mol Genet 1995; 4: 751-4.
36. Guo X, Popadin KY, Markuzon N, Orlov YL, Kraytsberg Y, Krishnan KJ, et al. Repeats, longevity and the sources of mtDNA deletions: evidence from 'deletional spectra'. Trends Genet 2010; 26: 340-3.
37. Melov S, Coskun P, Patel M, Tuinstra R, Cottrell B, Jun AS, et al. Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc Natl Acad Sci U S A 1999; 96: 846-51.
38. Williams MD, Van Remmen H, Conrad CC, Huang TT, Epstein CJ, Richardson A,. Increased oxidative damage is correlated to altered mitochondrial function in heterozygous manganese superoxide dismutase knockout mice. J Biol Chem 1998; 273: 28510-5.
39. Grishko V, Xu M, Ho R, Mates A, Watson S, Kim JT, et al. Effects of hyaluronic acid on mitochondrial function and mitochondria-driven apoptosis following oxidative stress in human chondrocytes. J Biol Chem 2009; 284: 9132-9.
40. 2,3-ethenoguanine in rat tissue DNA. Carcinogenesis 1990; 11: 1287-92.
41. +/- mouse results in the age-related decline of mitochondrial function culminating in increased apoptosis. Proc Natl Acad Sci U S A 2001; 98: 2278-83.
42. Wang M, Dhingra K, Hittelman WN, Liehr JG, de Andrade M, Li D,. Lipid peroxidation-induced putative malondialdehyde-DNA adducts in human breast tissues. Cancer Epidemiol Biomarkers Prev 1996; 5: 705-10.
43. Shah R, Raska K Jr, Tiku ML,. The presence of molecular markers of in vivo lipid peroxidation in osteoarthritic cartilage: a pathogenic role in osteoarthritis. Arthritis Rheum 2005; 52: 2799-807.
44. Strassburger M, Bloch W, Sulyok S, Schuller J, Keist AF, Schmidt A, et al. Heterozygous deficiency of manganese superoxide dismutase results in severe lipid peroxidation and spontaneous apoptosis in murine myocardium in vivo. Free Radic Biol Med 2005; 38: 1458-70.
45. Flynn JM, Choi SW, Day NU, Gerencser AA, Hubbard A, Melov S,. Impaired spare respiratory capacity in cortical synaptosomes from Sod2 null mice. Free Radic Biol Med 2011; 50: 866-73.
46. Passos JF, Nelson G, Wang C, Richter T, Simillion C, Proctor CJ, et al. Feedback between p21 and reactive oxygen production is necessary for cell senescence. Mol Syst Biol 2010; 6: 347.
47. Johnson K, Svensson CI, Van Etten D, Ghosh SS, Murphy AN, Powell HC, et al. Mediation of spontaneous knee osteoarthritis by progressive chondrocyte ATP depletion in Hartley guinea pigs. Arthritis Rheum 2004; 50: 1216-25.
48. Price JS, Waters JG, Darrah C, Pennington C, Edwards DR, Donell ST, et al. The role of chondrocyte senescence in osteoarthritis. Aging Cell 2002; 1: 57-65.
49. + leak and ROS generation: an odd couple. Free Radic Biol Med 2005; 38: 12-23.
50. Talbot DA, Lambert AJ, Brand MD,. Production of endogenous matrix superoxide from mitochondrial complex I leads to activation of uncoupling protein 3. FEBS Lett 2004; 556: 111-5.