Endogenous production of reactive oxygen species is required for stimulation of human articular chondrocyte matrix metalloproteinase production by fibronectin fragments

Free Radical Biology and Medicine

Volumn 42, Issue 9, 2007, Pages 1350-1358

  Del Carlo, Marcello ^a   Schwartz, Daniel ^a   Erickson, Elizabeth A ^b   Loeser, Richard F ^b  

^a RUSH MEDICAL COLLEGE   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Antioxidants; Integrins; Matrix metalloproteinase; Mitogen activated protein kinase; Nuclear factor B; Reactive oxygen species; Signal transduction

Indexed keywords

ACETYLCYSTEINE; ANTIOXIDANT; CATALASE; COLLAGENASE 3; FIBRONECTIN; GLUTATHIONE PEROXIDASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTEGRIN; LIPOXYGENASE INHIBITOR; MANGANESE; MANGANESE TETRAKIS(4 BENZOIC ACID)PORPHYRIN; MATRIX METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; NORDIHYDROGUAIARETIC ACID; REACTIVE OXYGEN METABOLITE; ROTENONE; STROMELYSIN; STROMELYSIN 2; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5;

ARTICLE; CARTILAGE CELL; CELL CULTURE; CELL STIMULATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; OSTEOARTHRITIS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REPORTER GENE; RESPIRATORY CHAIN; SECOND MESSENGER; SIGNAL TRANSDUCTION; STATISTICAL ANALYSIS;

ANTIOXIDANTS; CARTILAGE, ARTICULAR; CELLS, CULTURED; CHONDROCYTES; FIBRONECTINS; HUMANS; MATRIX METALLOPROTEINASE 13; MICROSCOPY, CONFOCAL; PEPTIDE FRAGMENTS; REACTIVE OXYGEN SPECIES;

EID: 33947511182     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2007.01.035     Document Type: Article

References (39)

1. Loeser R.F., and Shakoor N. Aging or osteoarthritis: which is the problem?. Rheum. Dis. Clin. North Am. 29 (2003) 653-673
2. Finkel T., and Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 408 (2000) 239-247
3. Henrotin Y.E., Bruckner P., and Pujol J.P. The role of reactive oxygen species in homeostasis and degradation of cartilage. Osteoarthritis Cartilage 11 (2003) 747-755
4. Del Carlo Jr. M., and Loeser R.F. Nitric oxide-mediated chondrocyte cell death requires the generation of additional reactive oxygen species. Arthritis Rheum. 46 (2002) 394-403
5. Del Carlo Jr. M., and Loeser R.F. Increased oxidative stress with aging reduces chondrocyte survival: correlation with intracellular glutathione levels. Arthritis Rheum. 48 (2003) 3419-3430
6. Kurz B., Lemke A., Kehn M., Domm C., Patwari P., Frank E.H., Grodzinsky A.J., and Schunke M. Influence of tissue maturation and antioxidants on the apoptotic response of articular cartilage after injurious compression. Arthritis Rheum. 50 (2004) 123-130
7. Jallali N., Ridha H., Thrasivoulou C., Underwood C., Butler P.E., and Cowen T. Vulnerability to ROS-induced cell death in ageing articular cartilage: the role of antioxidant enzyme activity. Osteoarthritis Cartilage 13 (2005) 614-622
8. Aigner T., Kim H.A., and Roach H.I. Apoptosis in osteoarthritis. Rheum. Dis. Clin. North Am. 30 (2004) 639-653
9. Nathan C. Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell signaling. J. Clin. Invest. 111 (2003) 769-778
10. Kamata H., and Hirata H. Redox regulation of cellular signalling. Cell Signal. 11 (1999) 1-14
11. Lo Y.Y., Wong J.M., and Cruz T.F. Reactive oxygen species mediate cytokine activation of c-Jun NH2- terminal kinases. J. Biol. Chem. 271 (1996) 15703-15707
12. Kheradmand F., Werner E., Tremble P., Symons M., and Werb Z. Role of Rac1 and oxygen radicals in collagenase-1 expression induced by cell shape change. Science 280 (1998) 898-902
13. Forsyth C.B., Pulai J., and Loeser R.F. Fibronectin fragments and blocking antibodies to alpha2beta1 and alpha5beta1 integrins stimulate mitogen-activated protein kinase signaling and increase collagenase 3 (matrix metalloproteinase 13) production by human articular chondrocytes. Arthritis Rheum. 46 (2002) 2368-2376
14. Loeser R.F., Forsyth C.B., Samarel A.M., and Im H.J. Fibronectin fragment activation of proline-rich tyrosine kinase PYK2 mediates integrin signals regulating collagenase-3 expression by human chondrocytes through a protein kinase C-dependent pathway. J. Biol. Chem. 278 (2003) 24577-24585
15. Im H.J., Pacione C., Chubinskaya S., Van Wijnen A.J., Sun Y., and Loeser R.F. Inhibitory effects of insulin-like growth factor-1 and osteogenic protein-1 on fibronectin fragment- and interleukin-1beta-stimulated matrix metalloproteinase-13 expression in human chondrocytes. J. Biol. Chem. 278 (2003) 25386-25394
16. Homandberg G.A., Wen C., and Hui F. Cartilage damaging activities of fibronectin fragments derived from cartilage and synovial fluid. Osteoarthritis Cartilage 6 (1998) 231-244
17. Homandberg G.A., Hui F., and Wen C. Fibronectin fragment mediated cartilage chondrolysis. I. Suppression by anti-oxidants. Biochim. Biophys. Acta 1317 (1996) 134-142
18. Pytela R., Pierschbacher M.D., and Ruoslahti E. Identification and isolation of a 140 kd cell surface glycoprotein with properties expected of a fibronectin receptor. Cell 40 (1985) 191-198
19. Werb Z., Tremble P.M., Behrendtsen O., Crowley E., and Damsky C.H. Signal transduction through the fibronectin receptor induces collagenase and stromelysin gene expression. J. Cell Biol. 109 (1989) 877-889
20. Muehleman C., Bareither D., Huch K., Cole A.A., and Kuettner K.E. Prevalence of degenerative morphological changes in the joints of the lower extremity. Osteoarthritis Cartilage 5 (1997) 23-37
21. Pulai J.I., Chen H., Im H.J., Kumar S., Hanning C., Hegde P.S., and Loeser R.F. NF-{kappa}B mediates the stimulation of cytokine and chemokine expression by human articular chondrocytes in response to fibronectin fragments. J. Immunol. 174 (2005) 5781-5788
22. Pulai J.I., Del Carlo Jr. M., and Loeser R.F. The alpha5beta1 integrin provides matrix survival signals for normal and osteoarthritic human articular chondrocytes in vitro. Arthritis Rheum. 46 (2002) 1528-1535
23. Moreno-Manzano V., Ishikawa Y., Lucio-Cazana J., and Kitamura M. Selective involvement of superoxide anion, but not downstream compounds hydrogen peroxide and peroxynitrite, in tumor necrosis factor-alpha-induced apoptosis of rat mesangial cells. J. Biol. Chem. 275 (2000) 12684-12691
24. Szabo C., Day B.J., and Salzman A.L. Evaluation of the relative contribution of nitric oxide and peroxynitrite to the suppression of mitochondrial respiration in immunostimulated macrophages using a manganese mesoporphyrin superoxide dismutase mimetic and peroxynitrite scavenger. FEBS Lett. 381 (1996) 82-86
25. Zafarullah M., Li W.Q., Sylvester J., and Ahmad M. Molecular mechanisms of N-acetylcysteine actions. Cell. Mol. Life Sci. 60 (2003) 6-20
26. Sakuma I., Stuehr D.J., Gross S.S., Nathan C., and Levi R. Identification of arginine as a precursor of endothelium-derived relaxing factor. Proc. Natl. Acad. Sci. USA 85 (1988) 8664-8667
27. Xie D.L., Hui F., Meyers R., and Homandberg G.A. Cartilage chondrolysis by fibronectin fragments is associated with release of several proteinases: stromelysin plays a major role in chondrolysis. Arch. Biochem. Biophys. 311 (1994) 205-212
28. Stanton H., Ung L., and Fosang A.J. The 45 kDa collagen-binding fragment of fibronectin induces matrix metalloproteinase-13 synthesis by chondrocytes and aggrecan degradation by aggrecanases. Biochem. J. 364 (2002) 181-190
29. Chiarugi P., Pani G., Giannoni E., Taddei L., Colavitti R., Raugei G., Symons M., Borrello S., Galeotti T., and Ramponi G. Reactive oxygen species as essential mediators of cell adhesion: the oxidative inhibition of a FAK tyrosine phosphatase is required for cell adhesion. J. Cell Biol. 161 (2003) 933-944
30. Henrotin Y., Deby-Dupont G., Deby C., De Bruyn M., Lamy M., and Franchimont P. Production of active oxygen species by isolated human chondrocytes. Br. J. Rheumatol. 32 (1993) 562-567
31. Studer R., Jaffurs D., Stefanovic-Racic M., Robbins P.D., and Evans C.H. Nitric oxide in osteoarthritis. Osteoarthritis Cartilage 7 (1999) 377-379
32. Hiran T.S., Moulton P.J., and Hancock J.T. Detection of superoxide and NADPH oxidase in porcine articular chondrocytes. Free Radic. Biol. Med. 23 (1997) 736-743
33. Tiku M.L., Shah R., and Allison G.T. Evidence linking chondrocyte lipid peroxidation to cartilage matrix protein degradation: possible role in cartilage aging and the pathogenesis of osteoarthritis. J. Biol. Chem. 275 (2000) 20069-20076
34. Day B.J., Fridovich I., and Crapo J.D. Manganic porphyrins possess catalase activity and protect endothelial cells against hydrogen peroxide-mediated injury. Arch. Biochem. Biophys 347 (1997) 256-262
35. Werner E., and Werb Z. Integrins engage mitochondrial function for signal transduction by a mechanism dependent on Rho GTPases. J. Cell Biol. 158 (2002) 357-368
36. Chen Y.R., Shrivastava A., and Tan T.H. Down-regulation of the c-Jun N-terminal kinase (JNK) phosphatase M3/6 and activation of JNK by hydrogen peroxide and pyrrolidine dithiocarbamate. Oncogene 20 (2001) 367-374
37. Reboul P., Pelletier J.P., Tardif G., Cloutier J.M., and Martel-Pelletier J. The new collagenase, collagenase-3, is expressed and synthesized by human chondrocytes but not by synoviocytes. A role in osteoarthritis. J. Clin. Invest. 97 (1996) 2011-2019
38. Mitchell P.G., Magna H.A., Reeves L.M., Lopresti-Morrow L.L., Yocum S.A., Rosner P.J., Geoghegan K.F., and Hambor J.E. Cloning, expression, and type II collagenolytic activity of matrix metalloproteinase-13 from human osteoarthritic cartilage. J. Clin. Invest. 97 (1996) 761-768
39. Billinghurst R.C., Wu W., Ionescu M., Reiner A., Dahlberg L., Chen J., van Wart H., and Poole A.R. Comparison of the degradation of type II collagen and proteoglycan in nasal and articular cartilages induced by interleukin-1 and the selective inhibition of type II collagen cleavage by collagenase. Arthritis Rheum. 43 (2000) 664-672