Strain-dependent oxidant release in articular cartilage originates from mitochondria

Biomechanics and Modeling in Mechanobiology

Volumn 13, Issue 3, 2014, Pages 565-572

  Brouillette, M J ^a,b   Ramakrishnan, P S ^a,b   Wagner, V M ^a,b   Sauter, E E ^a,b   Journot, B J ^a,b   McKinley, T O ^a   Martin, J A ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b University of Iowa   (United States)

Author keywords

Cartilage; Chondrocyte; Cytoskeleton; Hydrostatic stress; Mechanical loading; Reactive oxygen species (ROS); Static stress; Superoxide

Indexed keywords

BODY FLUIDS; CELL DEATH; DEFORMATION; ELASTICITY; MANGANESE COMPOUNDS; MITOCHONDRIA; OXIDATIVE STRESS; OXYGEN; STRAIN; STRESS ANALYSIS; SUPEROXIDE DISMUTASE;

ARTICULAR CARTILAGES; CHONDROCYTES; CYTOSKELETONS; HYDROSTATIC STRESS; MECHANICAL LOADING; MITOCHONDRIAS; REACTIVE OXYGEN SPECIES; STATIC STRESS; SUPEROXIDES;

CARTILAGE;

CYTOCHALASIN B; FLUORESCENT DYE; HYDROETHIDINE; OXIDIZING AGENT; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; SUPEROXIDE DISMUTASE;

ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CELL DEATH; CELL PERMEABILIZATION; CONFOCAL MICROSCOPY; CYTOSKELETON; EXPLANT; HYDROSTATIC PRESSURE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY CHAIN; ANIMAL; BOVINAE; DRUG EFFECTS; IN VITRO STUDY; MECHANICAL STRESS; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; CARTILAGE, ARTICULAR; CATTLE; CYTOCHALASIN B; FLUORESCENT DYES; IN VITRO TECHNIQUES; MICROSCOPY, CONFOCAL; MITOCHONDRIA; OXIDANTS; REACTIVE OXYGEN SPECIES; ROTENONE; STRESS, MECHANICAL;

EID: 84905588583     PISSN: 16177959     EISSN: 16177940     Source Type: Journal    
DOI: 10.1007/s10237-013-0518-8     Document Type: Article

References (39)

1. Ahmad R, Sylvester J, Ahmad M, Zafarullah M (2011) Involvement of H-Ras and reactive oxygen species in proinflammatory cytokineinduced matrix metalloproteinase-13 expression in human articular chondrocytes. Arch Biochem Biophys 507(2):350-355. doi:10. 1016/j.abb.2010.12.032
2. Araujo-Chaves JC, Yokomizo CH, Kawai C, Mugnol KC, Prieto T, Nascimento OR, Nantes IL (2011) Towards the mechanisms involved in the antioxidant action of MnIII [meso-tetrakis (4-N-methyl pyridinium) porphyrin] in mitochondria. J Bioenerg Biomembr 43(6):663-671. doi:10.1007/s10863-011-9382-3
3. Bachrach NM, Mow VC, Guilak F (1998) Incompressibility of the solid matrix of articular cartilage under high hydrostatic pressures. J Biomech 31(5):445-451. doi:10.1016/S0021-9290 (98) 00035-9
4. Bell EL, Klimova TA, Eisenbart J, Schumacker PT, Chandel NS (2007) Mitochondrial reactive oxygen species trigger hypoxiainducible factor-dependent extension of the replicative life span during hypoxia. Mol Cell Biol 27(16):5737-5745. doi:10.1128/MCB. 02265-06
5. Bingham JT, Papannagari R, Van de Velde SK, Gross C, Gill TJ, Felson DT, Rubash HE, Li G (2008) In vivo cartilage contact deformation in the healthy human tibiofemoral joint. Rheumatology 47(11):1622-1627. doi:10.1093/ rheumatology/ken345
6. Blanco FJ, Rego I, Ruiz-Romero C (2011) The role of mitochondria in osteoarthritis. Nat Rev Rheumatol 7(3):161-169. doi:10.1038/nrrheum.2010.213
7. Buckley MR, Gleghorn JP, Bonassar LJ, Cohen I (2008) Mapping the depth dependence of shear properties in articular cartilage. J Biomech 41(11):2430-2437. doi:10.1016/j.jbiomech.2008.05.021
8. Chahine NO, Ateshian GA, Hung CT (2007) The effect of finite compressive strain on chondrocyte viability in statically loaded bovine articular cartilage. Biomech Model Mechanobiol 6(1-2):103-111. doi:10.1007/s10237-006-0041-2
9. Chance B, Williams GR (1955) Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J Biol Chem 217(1):383-393
10. Cillero-Pastor B, Carames B, Lires-Dean M, Vaamonde-Garcia C, Blanco FJ, Lopez-Armada MJ (2008) Mitochondrial dysfunction activates cyclooxygenase 2 expression in cultured normal human chondrocytes. Arthritis Rheum 58(8):2409-2419. doi:10.1002/art. 23644
11. Durrant LA, Archer CW, Benjamin M, Ralphs JR (1999) Organisation of the chondrocyte cytoskeleton and its response to changing mechanical conditions in organ culture. J Anat 194(Pt 3):343-353
12. Gardner PR, Nguyen DD, White CW (1996) Superoxide scavenging by Mn (II/III) tetrakis (1-methyl-4-pyridyl) porphyrin in mammalian cells. Arch Biochem Biophys 325(1):20-28. doi:10.1006/abbi.1996. 0003
13. Goodwin W, McCabe D, Sauter E, Reese E, Walter M, Buckwalter JA, Martin JA (2010) Rotenone prevents impact-induced chondrocyte death. J Orthop Res 28(8):1057-1063. doi:10.1002/jor.21091
14. Hamanaka RB, Chandel NS (2010) Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends Biochem Sci 35(9):505-513. doi:10.1016/j.tibs.2010.04.002
15. Hosseini A, Van de Velde SK, Kozanek M, Gill TJ, Grodzinsky AJ, Rubash HE, Li G (2010) In-vivo time-dependent articular cartilage contact behavior of the tibiofemoral joint. Osteoarthr Cartil 18(7):909-916. doi:10.1016/j.joca. 2010.04.011
16. Knight MM, Bomzon Z, Kimmel E, Sharma AM, Lee DA, Bader DL (2006) Chondrocyte deformation induces mitochondrial distortion and heterogeneous intracellular strain fields. Biomech Model Mechanobiol 5(2-3):180-191
17. Lee RB, Urban JP (1997) Evidence for a negative Pasteur effect in articular cartilage. Biochem J 321(Pt 1):95-102
18. Lee RB, Urban JP (2002) Functional replacement of oxygen by other oxidants in articular cartilage. Arthritis Rheum 46(12):3190-3200. doi:10.1002/art.10686
19. Martin JA, Martini A, Molinari A, Morgan W, Ramalingam W, Buckwalter JA, McKinley TO (2012) Mitochondrial electron transport and glycolysis are coupled in articular cartilage. Osteoarthr Cartil 20(4):323-329. doi:10.1016/j.joca. 2012.01.003
20. Martin JA, McCabe D, Walter M, Buckwalter JA, McKinley TO (2009) N-acetylcysteine inhibits post-impact chondrocyte death in osteochondral explants. J Bone Joint Surg Am 91(8):1890-1897. doi:10. 2106/JBJS. H.00545
21. Orr AW, Helmke BP, Blackman BR, Schwartz MA (2006) Mechanisms of mechanotransduction. Dev Cell 10(1):11-20. doi:10.1016/j.devcel.2005.12.006
22. Otte P (1991) Basic cell metabolism of articular cartilage. Manometric studies. Z Rheumatol 50(5):304-312
23. Peshavariya HM, Dusting GJ, Selemidis S (2007) Analysis of dihydroethidium fluorescence for the detection of intracellular and extracellular superoxide produced by NADPH oxidase. Free Radic Res 41(6):699-712. doi:10.1080/10715760701297354
24. Quinn TM, Grodzinsky AJ, Buschmann MD, Kim YJ, Hunziker EB (1998) Mechanical compression alters proteoglycan deposition and matrix deformation around individual cells in cartilage explants. J Cell Sci 111(Pt 5):573-583
25. Quinn TM, Morel V, Meister JJ (2001) Static compression of articular cartilage can reduce solute diffusivity and partitioning: implications for the chondrocyte biological response. J Biomech 34(11):1463-1469
26. Ramakrishnan P, Hecht BA, Pedersen DR, Lavery MR, Maynard J, Buckwalter JA, Martin JA (2010) Oxidant conditioning protects cartilage from mechanically induced damage. J Orthop Res 28(7):914-920. doi:10.1002/jor.21072
27. Ramakrishnan PS, Pedersen DR, Stroud NJ, McCabe DJ, Martin JA (2011) Repeated measurement of mechanical properties in viable osteochondral explants following a single blunt impact injury. Proc Inst Mech Eng H 225(10):993-1002
28. Sauter E, Buckwalter JA, McKinley TO, Martin JA (2012) Cytoskeletal dissolution blocks oxidant release and cell death in injured cartilage. J Orthop Res 30(4):593-598. doi:10.1002/jor.21552
29. Schinagl RM, Ting MK, Price JH, Sah RL (1996) Video microscopy to quantitate the inhomogeneous equilibrium strain within articular cartilage during confined compression. Ann Biomed Eng 24(4):500-512
30. Stevens AL, Wishnok JS, White FM, Grodzinsky AJ, Tannenbaum SR (2009) Mechanical injury and cytokines cause loss of cartilage integrity and upregulate proteins associated with catabolism, immunity, inflammation, and repair. Mol Cell Proteomics 8(7):1475-1489. doi:10.1074/mcp. M800181-MCP200
31. Stockwell RA (1991) Morphometry of cytoplasmic components of mammalian articular chondrocytes and corneal keratocytes: species and zonal variations of mitochondria in relation to nutrition. J Anat 175:251-261
32. Strathmann J, Klimo K, Sauer SW, Okun JG, Prehn JH, Gerhauser C (2010) Xanthohumol-induced transient superoxide anion radical formation triggers cancer cells into apoptosis via a mitochondriamediated mechanism. FASEB J 24(8):2938-2950. doi:10.1096/fj. 10-155846
33. Tomiyama T, Fukuda K, Yamazaki K, Hashimoto K, Ueda H, Mori S, Hamanishi C (2007) Cyclic compression loadedoncartilage explants enhances the production of reactive oxygen species. J Rheumatol 34(3):556-562
34. Torzilli PA, Deng XH, Ramcharan M (2006) Effect of compressive strain on cell viability in statically loaded articular cartilage. Biomech Model Mechanobiol 5(2-3):123-132. doi:10.1007/s10237-006-0030-5
35. Trickey WR, Vail TP, Guilak F (2004) The role of the cytoskeleton in the viscoelastic properties of human articular chondrocytes. J Orthop Res 22(1):131-139. doi:10.1016/S0736-0266 (03) 00150-5
36. Weidemann A, Johnson RS (2008) Biology of HIF-1alpha. Cell Death Differ 15(4):621-627. doi:10.1038/cdd.2008.12
37. Wolff KJ, Ramakrishnan PS, Brouillette MJ, Journot BJ, McKinley TO, Buckwalter JA, Martin JA (2013) Mechanical stress and ATP synthesis are coupled by mitochondrial oxidants in articular cartilage. J Orthop Res 31(2):191-196. doi:10.1002/jor.22223
38. Wong M, Carter DR (2003) Articular cartilage functional histomorphology and mechanobiology: a research perspective. Bone 33(1):1-13
39. 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(12):3915-3924. doi:10.1002/art.20675