Reactive oxygen species (ROS), but not nitric oxide (NO), contribute to strain differences in the susceptibility to experimental arthritis in rats

Immunobiology

Volumn 212, Issue 2, 2007, Pages 95-105

  Miletić, Tatjana ^a   Kovačević Jovanović, Vesna ^a   Vujić, Vesna ^b   Stanojević, Stanislava ^a   Mitić, Katarina ^a   Lazarević Macanović, Mirjana ^c   Dimitrijević, Mirjana ^a  

^a Inst of Immunol and Virol Torlak   (Serbia)

^b UNIVERSITY OF BELGRADE   (Serbia)

^c UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

BCG; Experimental arthritis; HSP47; MHSP71; NO; Rat strains; ROS

Indexed keywords

BCG VACCINE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 47; HEAT SHOCK PROTEIN 71; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ADJUVANT ARTHRITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRITIS; ARTICLE; BACTERIAL CELL; CELL STIMULATION; CONTROLLED STUDY; DARK AGOUTI RAT; DISEASE COURSE; DISEASE PREDISPOSITION; DISEASE SEVERITY; IN VITRO STUDY; MALE; MYCOBACTERIUM BOVIS; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; RAT; RAT STRAIN; STRAIN DIFFERENCE; SYNTHESIS;

EID: 33847313733     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2006.11.012     Document Type: Article

References (44)

1. Ackerman N.R., Rooks II W.H., Shott L., Genant H., Maloney P., and West E. Effects of naproxen on connective tissue changes in the adjuvant arthritic rat. Arthritis Rheum 22 (1979) 1365-1374
2. Babior B.M. Oxidants from phagocytes: agents of defence and distruction. Blood 64 (1984) 959-966
3. Biemond P., Swaak A.J., Penders J.M., Beindorff C.M., and Koster J.F. Superoxide production by polymorphonuclear leucocytes in rheumatoid arthritis and osteoarthritis: in vivo inhibition by the antirheumatic drug piroxicam due to interference with the activation of the NADPH-oxidase. Ann. Rheum. Dis. 45 (1986) 249-255
4. Bogdan C. Nitric oxide and the immune response. Nat. Immunol. 2 (2001) 907-916
5. Cannon G.W., Openshaw S.J., Hibbs Jr. J.B., Hoidal J.R., Huecksteadt T.P., and Griffiths M.M. Nitric oxide production during adjuvant-induced and collagen-induced arthritis. Arthritis Rheum 39 (1996) 1677-1684
6. Chanock S.J., El-Benna J., Smith R.M., and Babior B.M. The respiratory burst oxidase. J. Biol. Chem. 269 (1994) 24519-24522
7. Chen W., Syldath U., Bellmann K., Burkart V., and Kolb H. Human 60-kDa heat-shock protein: a danger signal to the innate immune system. J. Immunol. 162 (1999) 3212-3219
8. Dalton D.K., Haynes L., Chu C.Q., Swain S.L., and Wittmer S. Interferon gamma eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4T cells. J. Exp. Med. 192 (2000) 117-122
9. Dang P.M., Stensballe A., Boussetta T., Raad H., Dewas C., Kroviarski Y., Hayem G., Jensen O.N., Gougerot-Pocidalo M.A., and El-Benna J. A specific p47phox-serine phosphorylated by convergent MAPKs mediates neutrophil NADPH oxidase priming at inflammatory sites. J. Clin. Invest. 116 (2006) 2033-2043
10. 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
11. Gelderman K.A., Hultqvist M., Holmberg J., Olofsson P., and Holmdahl R. T cell surface redox levels determine T cell reactivity and arthritis susceptibility. Proc. Natl. Acad. Sci. USA 103 (2006) 12831-12836
12. Green L.C., Wagner D.A., Glogowski J., Skipper P.L., Wishnok J.S., and Tannenbaum S.R. Analysis of nitrate, nitrite, and (15N) nitrate in biological fluids. Anal. Biochem. 126 (1982) 131-138
13. Griffiths H.R. ROS as signalling molecules in T cells-evidence for abnormal redox signalling in the autoimmune disease, rheumatoid arthritis. Redox. Rep. 10 (2005) 273-280
14. Griffiths M.M., Eichwald E.J., Martin J.H., Smith C.B., and DeWitt C.W. Immunogenetic control of experimental type II collagen-induced arthritis. Arthritis Rheum 24 (1981) 781-790
15. Hamuro J., Murata Y., Suzuki M., Takatsuki F., and Suga T. The triggering and healing of tumor stromal inflammatory reactions regulated by oxidative and reductive macrophages. Gann. Monograph. Cancer Res. 48 (1999) 153-164
16. Hattori T., Fujisawa T., Sasaki K., Yutani Y., Nakanishi T., Takahashi K., and Takigawa M. Isolation and characterization of a rheumatoid arthritis-specific antigen (RA-A47) from a human chondrocytic cell line (HCS-2/8). Biochem. Biophys. Res. Commun. 245 (1998) 679-683
17. Hattori T., Kawaki H., Kubota S., Yutani Y., de Crombrugghe B., von der Mark K., and Takigawa M. Downregulation of a rheumatoid arthritis-related antigen (RA-A47) by ra-a47 antisense oligonucleotides induces inflammatory factors in chondrocytes. J. Cell. Physiol. 197 (2003) 94-102
18. 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
19. Hildeman D.A., Mitchell T., Teague T.K., Henson P., Day B.J., Kappler J., and Marrack P.C. Reactive oxygen species regulate activation-induced T cell apoptosis. Immunity 10 (1999) 735-744
20. Hitchon C.A., and El-Gabalawy H.S. Oxidation in rheumatoid arthritis. Arthritis Res. Ther. 6 (2004) 265-278
21. Howard J.C., Varallo V.M., Ross D.C., Faber K.J., Roth J.H., Seney S., and Gan B.S. Wound healing-associated proteins Hsp47 and fibronectin are elevated in Dupuytren's contracture. J. Surg. Res. 117 (2004) 232-238
22. Hultqvist M., Olofsson P., Gelderman K.A., Holmberg J., and Holmdahl R. A new arthritis therapy with oxidative burst inducers. PLoS Med 3 (2006) e348
23. Hultqvist M., Olofsson P., Holmberg J., Backstrom B.T., Tordsson J., and Holmdahl R. Enhanced autoimmunity, arthritis, and encephalomyelitis in mice with a reduced oxidative burst due to a mutation in the Ncf1 gene. Proc. Natl. Acad. Sci. USA 101 (2004) 12646-12651
24. Kingston A.E., Hicks C.A., Colston M.J., and Billingham M.E. A 71-kD heat shock protein (hsp) from Mycobacterium tuberculosis has modulatory effects on experimental rat arthritis. Clin. Exp. Immunol. 103 (1996) 77-82
25. Kroncke K.D., Fehsel K., and Kolb-Bachofen V. Inducible nitric oxide synthase in human diseases. Clin. Exp. Immunol. 113 (1998) 147-156
26. Lahdenpohja N., Savinainen K., and Hurme M. Pre-exposure to oxidative stress decreases the nuclear factor-κB-dependent transcription in T lymphocytes. J. Immunol. 160 (1998) 1354-1358
27. Lotito A.P., Muscara M.N., Kiss M.H., Teixeira S.A., Novaes G.S., Laurindo I.M., Silva C.A., and Mello S.B. Nitric oxide-derived species in synovial fluid from patients with juvenile idiopathic arthritis. J. Rheumatol. 31 (2004) 992-997
28. MacMicking J., Xie Q.W., and Nathan C. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15 (1997) 323-350
29. Matsue H., Edelbaum D., Shalhevet D., Mizumoto N., Yang C., Mummert M.E., Oeda J., Masayasu H., and Takashima A. Generation and function of reactive oxygen species in dendritic cells during antigen presentation. J. Immunol. 171 (2003) 3008-3010
30. McCartney-Francis N., Allen J.B., Mizel D.E., Albina J.E., Xie Q.W., Nathan C.F., and Wahl S.M. Suppression of arthritis by an inhibitor of nitric oxide synthase. J. Exp. Med. 178 (1993) 749-754
31. Miesel R., Hartung R., and Kroeger H. Priming of NADPH oxidase by tumor necrosis factor alpha in patients with inflammatory and autoimmune rheumatic diseases. Inflammation 20 (1996) 427-438
32. Miletić T., Kovačević-Jovanović V., Stanojević S., Vujić V., Kosec D., Mitić K., and Dimitrijević M. Strain differences and the role for HSP47 and HSP70 in adjuvant arthritis in rats. Scand. J. Immunol. 64 (2006) 623-632
33. Olofsson P., Holmberg J., Tordsson J., Lu S., Akerstrom B., and Holmdahl R. Positional identification of Ncf1 as a gene that regulates arthritis severity in rats. Nat. Genet. 33 (2003) 25-32
34. Panjwani N.N., Popova L., and Srivastava P.K. Heat shock proteins gp96 and hsp70 activate the release of nitric oxide by APCs. J. Immunol. 168 (2002) 2997-3003
35. Pick E., Charon J., and Mizel D. A rapid densitometric microassay for the nitroblue tetrazolium reduction and application of the microassay to macrophages. J. Reticuloendothel. Soc. 30 (1981) 581-593
36. Remans P.H., van Oosterhout M., Smeets T.J., Sanders M., Frederiks W.M., Reedquist K.A., Tak P.P., Breedveld F.C., and van Laar J.M. Intracellular free radical production in synovial T lymphocytes from patients with rheumatoid arthritis. Arthritis Rheum 52 (2005) 2003-2009
37. Reth M. Hydrogen peroxide as second messenger in lymphocyte activation. Nat. Immunol. 3 (2002) 1129-1134
38. Sakurai H., Kohsaka H., Liu M.F., Higashiyama H., Hirata Y., Kanno K., Saito I., and Miyasaka N. Nitric oxide production and inducible nitric oxide synthase expression in inflammatory arthritides. J. Clin. Invest. 96 (1995) 2357-2363
39. Schreck R., Rieber P., and Baeuerle P.A. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J 10 (1991) 2247-2258
40. Taylor-Robinson A.W., Liew F.Y., Severn A., Xu D., McSorley S.J., Garside P., Padron J., and Phillips R.S. Regulation of the immune response by nitric oxide differentially produced by T helper type 1 and T helper type 2 cells. Eur. J. Immunol. 24 (1994) 980-984
41. Thoma-Uszynski S., Stenger S., Takeuchi O., Ochoa M.T., Engele M., Sieling P.A., Barnes P.F., Rollinghoff M., Bolcskei P.L., Wagner M., Akira S., Norgard M.V., Belisle J.T., Godowski P.J., Bloom B.R., and Modlin R.L. Induction of direct antimicrobial activity through mammalian toll-like receptors. Science 291 (2001) 1544-1547
42. Ueki Y., Miyake S., Tominaga Y., and Eguchi K. Increased nitric oxide levels in patients with rheumatoid arthritis. J. Rheumatol. 23 (1996) 230-236
43. Van de Loo F.A., Bennink M.B., Arntz O.J., Smeets R.L., Lubberts E., Joosten L.A., van Lent P.L., Coenen-de Roo C.J., Cuzzocrea S., Segal B.H., Holland S.M., and van den Berg W.B. Deficiency of NADPH oxidase components p47phox and gp91phox caused granulomatous synovitis and increased connective tissue destruction in experimental arthritis models. Am. J. Pathol. 163 (2003) 1525-1537
44. Zidek Z., Frankova D., and Otova B. Lack of causal relationship between inducibility/severity of adjuvant arthritis in the rat and disease associated changes in production of nitric oxide by macrophages. Ann. Rheum. Dis. 54 (1995) 325-327