The role of nitric oxide in arthritic joints: A therapeutic target?

Modern Rheumatology

Volumn 10, Issue 2, 2000, Pages 63-67

  Nishida, K ^a   Doi, T ^a   Inoue, H ^a  

^a OKAYAMA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

Nitric oxide; Osteoarthritis; Rheumatoid arthritis; Therapeutic target

Indexed keywords

EID: 33746160780     PISSN: 14397595     EISSN: 14397609     Source Type: Journal    
DOI: 10.3109/s101650050001     Document Type: Review

References (79)

1. Furchgot FtF, Zawadzki JV. The obligatory role of endothelial cells in the relation of arterial smooth muscle by acetylcholine. Nature 1980; 288: 373 – 6.
2. Ignaro LJ, Buga GM, Wood KS, Byrns RE, Chaudfuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 1987; 84: 9265 – 9.
3. Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987; 327: 524 – 6.
4. Hibbs JB Jr, Taintor RR, Vavrin Z. Macrophage cytotoxicity: role of L-arginine deiminase and iminonitrogen oxidation to nitrite. Science 1987; 235: 473 – 6.
5. Christopherson KS, Bredt DS. Prospective series: nitric oxide and nitric oxide synthases. Nitric oxide in excitable tissues: physiologic roles and disease. J Chin Invest 1997; 100: 2424 – 9.
6. Xie OW, Cho HJ, Calaycay J, Mumford RA, Swiderel KM, Lee TD, Ding A, et al. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 1992; 256: 225 – 8.
7. Clancy RM, Abramson SB. Nitric oxide: a novel mediator of inflammation. Soc Exp Biol Med 1995; 210: 93 – 101.
8. Nathan C. Perspective series: nitric oxide and nitric oxide synthases. Inducible nitric oxide synthase: what difference does it make? J Clin Invest 1997; 100: 2417 – 23.
9. Farrel AJ, Blake DR, Palmer MJ, Moncada S. Increased concentrations of nitrite in synovial fluid and serum samples sug-gest increased nitric oxide synthesis in rheumatic diseases. Ann Rheum Dis 1992; 51: 1219 – 22.
10. Stichtenoth DO, Fauler J, Zeidler H, Frölich JC. Urinary nitrate excretion is increased in patients with rheumatoid arthritis and reduced by prednisolone. Ann Rheum Dis 1995; 54: 820 – 4.
11. Ueki Y, Miyake S, Tominaga Y, Eguchi K. Increased nitric oxide levels in patients with rheumatoid arthritis. J Ftheumatol 1996; 23: 230 – 6.
12. Salvatierra J, Escames G, Hernandez P, Cantero J, Crespo E, Leon J, et al. Cartilage and serum levels of nitric oxide in patients with hip osteoarthritis. J Ftheumatol 1999; 26: 2015 – 17.
13. McInnes IB, Leung BP, Field M, Wei XQ, Huag FP, Sturrock RD. Production of nitric oxide in synovial membrane of rheumatoid and osteoarthritis patients. J Exp Med 1996; 184: 1519 – 24.
14. Sakurai H, Kohsaka H, Liu MF, Higashiyama H, Hirata Y, Kanno K, et al. Nitric oxide production and inducible nitric oxide synthase expression in inflammatory arthritides. J Clin Invest 1995; 96: 2357 – 63.
15. St. Clair EW, Wilkinson WE, Lang T, Sanders L, Misukonis MA, Gilkeson GS, et al. Increased expression of blood mononuclear cell nitric oxide synthase type 2 in rheumatoid arthritis patients. J Exp Med 1996; 184: 1173 – 8.
16. Hayashi T, Abe E, Yamate T, Taguchi T, Jasin HE. Nitric oxide production by superficial and deep articular chondrocytes. Arthritis Rheum 1997; 40: 261 – 9.
17. Evans DM, Ralston SH. Nitric oxide and bone. J Bone Min Res 1996; 11: 300 – 5.
18. Stichtenoth DO, Frölich JC. Nitric oxide and inflammatory joint diseases. Br J Rheum 1998; 37: 246 – 57.
19. Amin AR, Di Cesare PE, Vyas P, Attur M, Tzeng E, Billiar TR, et al. The expression and regulation of nitric oxide synthase in human osteoarthritis-affected chondrocytes: evidence for up-regulated neuronal nitric oxide synthase. J Exp Med 1995; 182: 2097 – 102.
20. Miller MJS, Chotinaruemol S, Sadowska-Krowicka H, Kakkis JL, Munshi UK, Zhang XJ, et al. Nitric oxide: the Jekyl and Hyde of gut inflammation. Agents Actions 1993; 39: C180 – 2.
21. Grabowski PS, Macpherson H, Ralston SH. Nitric oxide produc-tion in cells derived from the human joint. Br J Rheum 1996; 35: 207 – 12.
22. Grabowski PS, Wright PK, Van't Hof RJ, Helfrich MH, Ohshima H, Ralston SH. Immunolocalization of inducible nitric oxide syn-thase in synovium and cartilage in rheumatoid arthritis and os-teoarthritis. Br J Rheum 1997; 36: 651 – 5.
23. Lander HM, Sehajpal P, Levine DM, Novogrodsky A. Activation of human peripheral blood mononuclear cells by nitiric oxide-generating compounds. J Immunol 1993; 150: 1509 – 16.
24. Leibovich SJ, Polverini PJ, Fong TW, Harlow LA, Koch AE. Pro-duction of angiogenic activity by human monocytes requires an L-arginine/nitric oxide-synthase-dependent effector mechanism. Proc Natl Acad Sci USA 1994; 91: 4190 – 4.
25. Mayhan WG. Role of nitric oxide in modulating permeability of hamster cheek pouch in response to adenosine 5' -diphosphate and bradykinin. Inflammation 1996; 16: 295 – 305.
26. Ziche M. Role of nitric oxide in the angiogenesis of avascular tissue. Osteoarthritis Cartilage 1999; 7: 403 – 5.
27. Bratt J, Gyllenhammar H. The role of nitric oxide in lipoxin Af-induced polymorphonuclear neutrophil-dependent cytotoxicity to human vascular endothelium in vivo. Arthritis Rheum 1995; 38: 768 – 76.
28. Albina JE, Abate JA, Henry WL Jr. Nitric oxide production is required for murine resident peritoneal macrophages to suppress mitogen-stimulated T cell proliferation: role of IFN-y in the induction of the nitiric oxide-synthesizing pathway. J Immunol 1991; 147: 144 – 8.
29. Belenky SN, Robbins RA, Rubinstein I. Nitric oxide synthase inhibitors attenuate human monocyte chemotaxis in vitro. J Leukocyte Biol 1993; 53: 498 – 503.
30. Kubes P, Suzuki M, Granger DN. Nitric oxide: an endogenous modulater of leukocyte adhesion. Proc Natl Acad Sci USA 1991; 88: 4651 – 5.
31. Hogaboam CM, Befus AD, Wallace JL. Modulation of mast cell reactivity by IL-113. Divergent effects on nitric oxide and platelet-activating factor release. J Immunol 1993; 151: 3767 – 74.
32. Stadler J, Harbrecht BG, Di Silvio M, Curran RD, Jordan ML, Simmons RL, et al. Endogenous nitiric oxide inhibits the synthesis of cyclooxygenase products and interleukin-6 by rat Kupffer cells. J Leukocyte Biol 1993; 53: 165 – 72.
33. Gracie JA, Forsey RJ, Chan WL, Gilmour A, Leung BP, Greer MR, et al. Proinflammatory role for IL-18 in rheumatoid arthritis. J Clin Invest 1999; 104: 1393 – 401.
34. de Caterina R, Libby P, Peng HB, Thannickal VJ, Rajavashisth TB, Gimbrone MA, et al. Nitric oxide decreases cytokine-induced endothelial activation: nitric oxide selectivity reduces endothelial expression of adhesion molecules and proinflammatory cytokines. J Clin Invest 1995; 96: 60 – 8.
35. Lotz M. The role of nitric oxide in articular cartilage damage. Rheum Dis Chin North Am 1999; 25: 269 – 82.
36. Melchiorri C, Meliconi R, Frizzier° L, Silvestri T, Pulsatelli L, Mazzetti I, et al. Enhanced and coordinated in vivo expression of inflammatory cytokines and nitric oxide synthase by chondrocytes from patients with osteoarthritis. Arthritis Rheum 1998; 41: 2165 – 74.
37. Olee T, Hashimoto S, Quach J, Lotz M. IL-18 is produced by articular chondrocytes and induces proinflammatory and catabolic responses. J Immunol 1999; 162: 1096 – 100.
38. Stefanovic-Racic M, Morales TI, Taskiran D, McIntyre LA, Evans CH. The role of nitric oxide in proteoglycan turnover by bovine articular organ cultures. J Immunol 1996; 156: 1213 – 20.
39. Das P, Schurman DJ, Smith RL. Nitric oxide and G proteins mediate the response of bovine articular chondrocytes to fluid-induced shear. J Orthop R 1997; 15: 87 – 93.
40. Taskuran D, Stefanovic-Racic M, Georgescu H, Evans C. Nitric oxide mediates suppression of cartilage proteoglycan synthesis by interleukin-1. Biochem Biophys Res Commun 1994; 200: 142 – 8.
41. Clancy R, Abramson SB, Kohne C, Rediske J. Nitric oxide attenuates cellular hexose monophosphate shunt response to oxidants in articular chondrocytes and acts to promote oxidant injury. J Cell Physiol 1997; 172: 183 – 91.
42. Murel GA, Jang D, Williams RJ. Nitric oxide activates metalloproteinase enzymes in articular cartilage. Biochem Biophys Res Commun 1995; 206: 15 – 21.
43. Sasaki K, Hattori T, Fujisawa T, Takahashi K, Inoue H, Takigawa M. Nitric oxide mediates interleukin-1 -induced gene expression of matrix metalloproteinases and basic fibroblast growth factor in cultured rabbit articular chondrocyte. J Biochem (Tokyo) 1998; 123: 431 – 9.
44. Frears ER, Zhang Z, Blake DR, O'Connel JP, Winyard PG. Inactivation of tissue inhibitor of metalloproteinase-1 by peroxinitrite. FEBS Lett 1996; 381: 21 – 4.
45. Pelletier JP, Mineau F, Ranger P, Tardif G, Martel-Pelletier J. The increased synthesis of inducible nitric oxide inhibits IL-lra syn-thesis by human articular chondrocytes: possible role in osteo-arthritic cartilage degradation. Osteoarthritis Cartilage 1996; 4: 77 – 84.
46. Frankel SR, Clancy RM, Ricci JL, DICeare PE, Rediske JJ, Abramson SB. Effects of nitric oxide on chondrocyte migration, adhesion, and cytoskeletal assembly. Arthritis Rheum 1996; 39: 1905 – 12.
47. Millward-Sadler SJ, Wright MO, Lee H, Nishida K, Caldwell H, Nuki J, et al. Integrin-regulated secretion of interleukin 4: a novel pathway of mechanotransduction in human articular chondrocytes. J Cell Biol 1999; 145: 183 – 9.
48. Blanco FJ, Ochs RL, Schwarz H, Lots M. Chondrocyte apoptosis induced by nitric oxide. Am J Pathol 1995; 146: 75 – 85.
49. Amin AR, Abramson SB. The role of nitric oxide in articular cartilage breakdown in osteoarthritis. Curr Opin Ftheumatol 1998; 10: 263 – 8.
50. Horton WE Jr, Feng L, Adams C. Chondrocyte apoptosis in development, aging and disease. Matrix Biol 1998; 17: 107 – 15.
51. Carson DA, Tan EM. Apoptosis in rheumatic diseases. Bull Rheum Dis 1995; 44: 1 – 3.
52. Hashimoto S, Takahashi K, Amiel D, Coutts R, Lotz M. Chondrocyte apoptosis and nitric oxide production during experimentally induced osteoarthritis. Arthritis Rheum 1998; 41: 1266 – 74.
53. Kim HA, Song YW. Apoptotic chondrocyte death in rheumatoid arthritis. Arthritis Rheum 1999; 42: 1528 – 37.
54. Hashimoto S, Ochs RL, Rosen F, Quach J, McCabe G, SoIan J, et al. Chondrocyte-derived apoptotic bodies and calcification of articular cartilage. Proc Natl Acad Sci USA 1998; 95: 3094 – 9.
55. Erlacher L, Maier R, Ullrich R, Kiener H, Aringer M, Menschik M, et al. Differential expression of protooncogene bc1-2 in normal and osteoarthritic human articular cartilage. J Ftheumatol 69. 1995; 22: 926 – 31.
56. Amin AR, Attur M, Patel RJ, Thakker GD, Marshall PJ, Rediske J, et al. Superinduction of cyclooxygenase-2 activity in human osteoarthritis-affected cartilage. J Clin Invest 1997; 99: 1231 – 7.
57. Henrotin YE, Zheng S, Deby GP, LaBasse AH, Crielaard J, 70. Reginster JL. Nitric oxide down-regulates IL-1(3-stimulated IL-6, IL-8, and PGE2 production by human chondrocytes. J Rheumatol 1998; 25: 1595 – 601.
58. Clancy RM, Amin AR, Abramson SB. The role of nitric oxide in 71. inflammation and immunity. Arthritis Rheum 1998; 41: 1141 – 51.
59. Salvemini D, Misko TP, Masferrer JL, Seibert K, Currie MG, Needleman P. Nitric oxide activated cyclooxygenase enzymes. Proc Natl Acad Sci USA 1993; 90: 7240 – 4.
60. McCartney-Francis N, Allen JB, Mizel DE, Albina JE, Xie Q, 72. Nathan CF, et al. Suppression of arthritis by an inhibitor of nitric oxide synthase. J Exp Med 1993; 178: 749 – 54.
61. Conner JR, Manning PT, Settle S, Moore WM, Jerome GM, 73. Webber RK, et al. Suppression of adjuvant-induced arthritis by selective inhibition of inducible nitric oxide synthase. Eur J Pharmacol 1995; 273: 15 – 24.
62. Pelletier JP, Javanovic D, Fernandes JC, Manning P, Conner JR, 74. Currie MG, et al. Reduced progression of experimental osteoarthritis in vivo by selective inhibition of inducible nitric oxide synthase. Arthritis Rheum 1998; 41: 1275 – 86.
63. St Clair EW. Nitric oxide - friend or foe in arthritis? J Ftheumatol 75. 1998; 25: 1451 – 3.
64. Baeuerle PA, Henkel T. Function and activation of NF-KB in the immune system. Annu Rev Immunol 1994; 12: 141 – 79.
65. Jue DM, Jeon KI, Jeong JY. Nuclear factor kappaB (NF-kappaB) 76. pathway as a therapeutic target in rheumatoid arthritis. J Korean Med Sci 1999; 14: 231 – 8.
66. Asahara H, Asanuma M, Ogawa N, Nishibayashi S, Inoue H. High 77. DNA-binding activity of transcription factor NF-kappaB in synovial membranes of patients with rheumatoid arthritis. Biochem Mol Biol Int 1995; 37: 827 – 32.
67. Palombella VJ, Conner EM, Fuseler JW, Destree A, Davis JM, 78. Laroux FS, et al. Role of the proteasome and NF-kappaB in streptococcal cell wall-induced polyarthritis. Proc Natl Acad Sci USA 1998; 95: 15671-6. 79.
68. Miyazawa K, Mori A, Yamamoto K, Okudaira H. Constitutive transcription of the human interleukin-6 gene by rheumatoid synoviocytes: spontaneous activation of NF-kappaB and CBF1. Am J Pathol 1998; 152: 793 – 803.
69. Sato M, Miyazaki T, Nagaya T, Murata Y, Ida N, Maeda K, et al. Antioxidants inhibit tumor necrosis factor-alpha mediated stimula-tion of interleukin-8, monocyte chemoattractant protein-1, and collagenase expression in cultured human synovial cells. J Ftheumatol 1996; 23: 432 – 8.
70. Crofford LJ, Tan B, McCarthy CJ, Ella T. Involvement of nuclear factor kappa B in the regulation of cyclooxygenase-2 expression by interleukin-1 in rheumatoid synoviocytes. Arthritis Rheum 1997; 40: 226 – 36.
71. Roshak AK, Jackson JR, McGough K, Chabot-Fletcher M, Mochan E, Marshall LA. Manipulation of distinct NF-kappaB proteins alters interleukin-lbeta-induced human rheumatoid synovial fibroblast prostaglandin E2 formation. J Biol Chem 1996; 271: 31496 – 501.
72. Han Z, Boyle DL, Manning AM, Firestein GS. AP-1 and NF-kappaB regulation in rheumatoid arthritis and murine collagen-induced arthritis. Autoimmunity 1998; 28: 197 – 208.
73. Sakurada S, Kato T, Okamoto T. Induction of cytokines and ICAM-1 by proinflammatory cytokines in primary rheumatoid synovial fibroblasts and inhibition by N-acetyl-L-cysteine and aspirin. Int Immunol 1996; 8: 1483 – 93.
74. Marok R, Winyard PG, Coumbe A, Kus ML, Gaffney K, Blades S, et al. Activation of the transcription factor nuclear factor-kappaB in human inflamed synovial tissue. Arthritis Rheum 1996; 39: 583 – 91.
75. Fujisawa K, Aono H, Hasunuma T, Yamamoto K, Mita S, Nishioka K. Activation of transcription factor NF-kappaB in human synovial cells in response to tumor necrosis factor alpha. Arthritis Rheum 1996; 39: 197 – 203.
76. Lee JI, Burckart GJ. Nuclear factor kappa B: important transcription factor and therapeutic target. J Clin Pharmacol 1998; 38: 981 – 93.
77. Tsuji F, Miyake Y, Aono H, Kawashima Y, Mita S. Effects of bucillamine and N-acetyl-L-cysteine on cytokine production and collagen-induced arthritis (CIA). Clin Exp Immunol 1999; 115: 26 – 31.
78. Voll RE, Mikulowska A, Kalden JR, Holmdahl R. Amelioration of type II collagen induced arthritis in rats by treatment with sodium diethyldithiocarbamate. J Ftheumatol 1999; 26: 1352 – 8.
79. Tomita T, Takeuchi E, Tomita N, Morishita R, Kaneko M, Yamamoto K, et al. Suppressed severity of collagen-induced arthritis by in vivo transfection of nuclear factor icB decoy oligo-deoxynudeotides as a gene therapy. Arthritis Rheum 1999; 42: 2532 – 42.