Mechanical stress and ATP synthesis are coupled by mitochondrial oxidants in articular cartilage

Journal of Orthopaedic Research

Volumn 31, Issue 2, 2013, Pages 191-196

  Wolff, Katherine J ^a   Ramakrishnan, Prem S ^a   Brouillette, Marc J ^a,b   Journot, Brice J ^a,b   McKinley, Todd O ^a   Buckwalter, Joseph A ^a,c   Martin, James A ^a  

^a UNIVERSITY OF IOWA   (United States)

^b University of Iowa   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

articular cartilage; glycolysis; mechanical stress; oxidants; reactive oxygen species

Indexed keywords

ADENOSINE TRIPHOSPHATE; HYDROETHIDINE; LUCIFERASE; REACTIVE OXYGEN METABOLITE; ROTENONE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; BLUNT TRAUMA; CARTILAGE CELL; CONTROLLED STUDY; GLYCOLYSIS; MECHANICAL STRESS; MITOCHONDRION; MOLECULAR PROBE; NONHUMAN; OSTEOARTHRITIS; PATHOGENESIS; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; ANIMALS; CARTILAGE, ARTICULAR; CATTLE; CHONDROCYTES; ELECTRON TRANSPORT; MITOCHONDRIA; ORGANOPHOSPHORUS COMPOUNDS; REACTIVE OXYGEN SPECIES; ROTENONE; STRESS, MECHANICAL; UBIQUINONE;

EID: 84871609424     PISSN: 07360266     EISSN: 1554527X     Source Type: Journal    
DOI: 10.1002/jor.22223     Document Type: Article

References (45)

1. Carter DR, Orr TE, Fyhrie DP, et al. 1987. Influences of mechanical stress on prenatal and postnatal skeletal development. Clin Orthop Relat Res 219: 237-250.
2. Kiviranta I, Tammi M, Jurvelin J, et al. 1988. Moderate running exercise augments glycosaminoglycans and thickness of articular cartilage in the knee joint of young beagle dogs. J Orthop Res 6: 188-195.
3. Saamanen AM, Tammi M, Kiviranta I, et al. 1988. Running exercise as a modulatory of proteoglycan matrix in the articular cartilage of young rabbits. Int J Sports Med 9: 127-133.
4. Jurvelin J, Kiviranta I, Tammi M, et al. 1986. Effect of physical exercise on indentation stiffness of articular cartilage in the canine knee. Int J Sports Med 7: 106-110.
5. Brama PA, Tekoppele JM, Bank RA, et al. 2000. The influence of strenuous exercise on collagen characteristics of articular cartilage in Thoroughbreds age 2 years. Equine Vet J 32: 551-554.
6. Vanwanseele B, Eckstein F, Knecht H, et al. 2002. Knee cartilage of spinal cord-injured patients displays progressive thinning in the absence of normal joint loading and movement. Arthritis Rheum 46: 2073-2078.
7. Paukkonen K, Helminen HJ, Tammi M, et al. 1984. Quantitative morphological and biochemical investigations on the effects of physical exercise and immobilization on the articular cartilage of young rabbits. Acta Biol Hung 35: 293-304.
8. Haapala J, Arokoski J, Pirttimaki J, et al. 2000. Incomplete restoration of immobilization induced softening of young beagle knee articular cartilage after 50-week remobilization. Int J Sports Med 21: 76-81.
9. Jurvelin J, Kiviranta I, Saamanen AM, et al. 1989. Partial restoration of immobilization-induced softening of canine articular cartilage after remobilization of the knee (stifle) joint. J Orthop Res 7: 352-358.
10. Urban JP,. 2000. Present perspectives on cartilage and chondrocyte mechanobiology. Biorheology 37: 185-190.
11. Wong M, Carter DR,. 2003. Articular cartilage functional histomorphology and mechanobiology: a research perspective. Bone 33: 1-13.
12. Martin JA, Martini A, Molinari A, et al. 2012. Mitochondrial electron transport and glycolysis are coupled in articular cartilage. Osteoarthritis Cartilage 20: 323-329.
13. Guilak F,. 2000. The deformation behavior and viscoelastic properties of chondrocytes in articular cartilage. Biorheology 37: 27-44.
14. Knight MM, van de Breevaart Bravenboer J, Lee DA, et al. 2002. Cell and nucleus deformation in compressed chondrocyte-alginate constructs: temporal changes and calculation of cell modulus. Biochim Biophys Acta 1570: 1-8.
15. Knight MM, Bomzon Z, Kimmel E, et al. 2006. Chondrocyte deformation induces mitochondrial distortion and heterogeneous intracellular strain fields. Biomech Model Mechanobiol 5: 180-191.
16. Martin JA, McCabe D, Walter M, et al. 2009. N-acetylcysteine inhibits post-impact chondrocyte death in osteochondral explants. J Bone Joint Surg Am 91: 1890-1897.
17. Sauter E, Buckwalter JA, McKinley TO, et al. 2012. Cytoskeletal dissolution blocks oxidant release and cell death in injured cartilage. J Orthop Res 30: 593-598.
18. Goodwin W, McCabe D, Sauter E, et al. 2010. Rotenone prevents impact-induced chondrocyte death. J Orthop Res 28: 1057-1063.
19. Ramakrishnan PS, Pedersen DR, Stroud NJ, et al. 2011. Repeated measurement of mechanical properties in viable osteochondral explants following a single blunt impact injury. Proc Inst Mech Eng(Part H); J Eng Med 225: 993-1002.
20. Long JA, Guthrie HD,. 2006. Validation of a rapid, large-scale assay to quantify ATP concentration in spermatozoa. Theriogenology 65: 1620-1630.
21. Gane EJ, Weilert F, Orr DW, et al. 2010. The mitochondria-targeted anti-oxidant mitoquinone decreases liver damage in a phase II study of hepatitis C patients. Liver Int 30: 1019-1026.
22. Boldogh IR, Nowakowski DW, Yang HC, et al. 2003. A protein complex containing Mdm10p, Mdm12p, and Mmm1p links mitochondrial membranes and DNA to the cytoskeleton-based segregation machinery. Mol Biol Cell 14: 4618-4627.
23. Yi M, Weaver D, Hajnoczky G,. 2004. Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J Cell Biol 167: 661-672.
24. Gourlay CW, Ayscough KR,. 2005. The actin cytoskeleton: a key regulator of apoptosis and ageing? Nat Rev Mol Cell Biol 6: 583-589.
25. Pillay J, Ramakers BP, Kamp VM, et al. 2010. Functional heterogeneity and differential priming of circulating neutrophils in human experimental endotoxemia. J Leukoc Biol 88: 211-220.
26. Benassi B, Fanciulli M, Fiorentino F, et al. 2006. c-Myc phosphorylation is required for cellular response to oxidative stress. Mol Cell 21: 509-519.
27. Burgering BM, Kops GJ,. 2002. Cell cycle and death control: long live Forkheads. Trends Biochem Sci 27: 352-360.
28. St-Pierre J, Drori S, Uldry M, et al. 2006. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127: 397-408.
29. Cillero-Pastor B, Carames B, Lires-Dean M, et al. 2008. Mitochondrial dysfunction activates cyclooxygenase 2 expression in cultured normal human chondrocytes. Arthritis Rheum 58: 2409-2419.
30. Ahmad R, Sylvester J, Ahmad M, et al. 2011. Involvement of H-Ras and reactive oxygen species in proinflammatory cytokine-induced matrix metalloproteinase-13 expression in human articular chondrocytes. Arch Biochem Biophys 507: 350-355.
31. Lee RB, Urban JP,. 2002. Functional replacement of oxygen by other oxidants in articular cartilage. Arthritis Rheum 46: 3190-3200.
32. Ramakrishnan P, Hecht BA, Pedersen DR, et al. 2010. Oxidant conditioning protects cartilage from mechanically induced damage. J Orthop Res 28: 914-920.
33. Chuang DM, Hough C, Senatorov VV,. 2005. Glyceraldehyde-3-phosphate dehydrogenase, apoptosis, and neurodegenerative diseases. Annu Rev Pharmacol Toxicol 45: 269-290.
34. Mobasheri A, Platt N, Thorpe C, et al. 2006. Regulation of 2-deoxy- D -glucose transport, lactate metabolism, and MMP-2 secretion by the hypoxia mimetic cobalt chloride in articular chondrocytes. Ann N Y Acad Sci 1091: 83-93.
35. Eckstein F, Lemberger B, Stammberger T, et al. 2000. Patellar cartilage deformation in vivo after static versus dynamic loading. J Biomech 33: 819-825.
36. Bingham JT, Papannagari R, Van de Velde SK, et al. 2008. In vivo cartilage contact deformation in the healthy human tibiofemoral joint. Rheumatology (Oxford) 47: 1622-1627.
37. Blanco FJ, Lopez-Armada MJ, Maneiro E,. 2004. Mitochondrial dysfunction in osteoarthritis. Mitochondrion 4: 715-728.
38. Liu JT, Guo X, Ma WJ, et al. 2010. Mitochondrial function is altered in articular chondrocytes of an endemic osteoarthritis, Kashin-Beck disease. Osteoarthritis Cartilage 18: 1218-1226.
39. Korhonen RK, Laasanen MS, Toyras J, et al. 2002. Comparison of the equilibrium response of articular cartilage in unconfined compression, confined compression and indentation. J Biomech 35: 903-909.
40. Bae WC, Lewis CW, Levenston ME, et al. 2006. Indentation testing of human articular cartilage: effects of probe tip geometry and indentation depth on intra-tissue strain. J Biomech 39: 1039-1047.
41. Guilak F, Mow VC,. 2000. The mechanical environment of the chondrocyte: a biphasic finite element model of cell-matrix interactions in articular cartilage. J Biomech 33: 1663-1673.
42. Kalyanaraman B, Darley-Usmar V, Davies KJ, et al. 2012. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med 52: 1-6.
43. Cocheme HM, Kelso GF, James AM, et al. 2007. Mitochondrial targeting of quinones: therapeutic implications. Mitochondrion 7: S94-S102.
44. Zhou S, Cui Z, Urban JP,. 2004. Factors influencing the oxygen concentration gradient from the synovial surface of articular cartilage to the cartilage-bone interface: a modeling study. Arthritis Rheum 50: 3915-3924.
45. Lee RB, Urban JP,. 1997. Evidence for a negative Pasteur effect in articular cartilage. Biochem J 321: 95-102.