Hyaluronan modulates accumulation of hypoxia-inducible factor-1 alpha, inducible nitric oxide synthase, and matrix metalloproteinase-3 in the synovium of rat adjuvant-induced arthritis model

Arthritis Research and Therapy

Volumn 13, Issue 3, 2011, Pages

  Chou, Li Wei ^a,b   Wang, John ^c,d   Chang, Pei Lin ^a   Hsieh, Yueh Ling ^a  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^d HUNGKUANG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

FREUND ADJUVANT; HYALURONIC ACID; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE; PLACEBO; STROMELYSIN; HIF1A PROTEIN, RAT; NOS2 PROTEIN, RAT; VISCOSUPPLEMENT;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRALGIA; ARTHRITIS; ARTICLE; CONTROLLED STUDY; EDEMA; FOLLOW UP; GENE OVEREXPRESSION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATION; MALE; NONHUMAN; PAIN ASSESSMENT; PROTEIN EXPRESSION; RAT; SYNOVIUM; ANIMAL; DRUG EFFECT; IMMUNOLOGY; INTRAARTICULAR DRUG ADMINISTRATION; METABOLISM; NOCICEPTION; PAIN THRESHOLD; SPRAGUE DAWLEY RAT;

ANIMALS; ARTHRALGIA; ARTHRITIS, EXPERIMENTAL; EDEMA; FREUND'S ADJUVANT; HYALURONIC ACID; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INJECTIONS, INTRA-ARTICULAR; MALE; MATRIX METALLOPROTEINASE 3; NITRIC OXIDE SYNTHASE TYPE II; NOCICEPTION; PAIN THRESHOLD; RATS; RATS, SPRAGUE-DAWLEY; SYNOVIAL MEMBRANE; VISCOSUPPLEMENTS;

EID: 79959214002     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3365     Document Type: Article

References (47)

1. Peters CL, Morris CJ, Mapp PI, Blake DR, Lewis CE, Winrow VR. The transcription factors hypoxia-inducible factor 1alpha and Ets-1 colocalize in the hypoxic synovium of inflamed joints in adjuvant-induced arthritis. Arthritis Rheum 2004, 50:291-296. 10.1002/art.11473, 14730627.
2. Boyd HK, Lappin TR, Bell AL. Evidence for impaired erythropoietin response to anaemia in rheumatoid disease. Br J Rheumatol 1991, 30:255-259. 10.1093/rheumatology/30.4.255, 1863821.
3. Oliver KM, Taylor CT, Cummins EP. Hypoxia. Regulation of NFkappaB signalling during inflammation: the role of hydroxylases. Arthritis Res Ther 2009, 11:215. 10.1186/ar2575, 2688226, 19291263.
4. Paleolog EM. Angiogenesis in rheumatoid arthritis. Arthritis Res 2002, 4(Suppl 3):S81-S90. 10.1186/ar575, 12110126.
5. Brouwer E, Gouw AS, Posthumus MD, van Leeuwen MA, Boerboom AL, Bijzet J, Bos R, Limburg PC, Kallenberg CG, Westra J. Hypoxia inducible factor-1-alpha (HIF-1alpha) is related to both angiogenesis and inflammation in rheumatoid arthritis. Clin Exp Rheumatol 2009, 27:945-951.
6. Giatromanolaki A, Sivridis E, Maltezos E, Athanassou N, Papazoglou D, Gatter KC, Harris AL, Koukourakis MI. Upregulated hypoxia inducible factor-1alpha and -2alpha pathway in rheumatoid arthritis and osteoarthritis. Arthritis Res Ther 2003, 5:R193-201. 10.1186/ar756, 165055, 12823854.
7. Hollander AP, Corke KP, Freemont AJ, Lewis CE. Expression of hypoxia-inducible factor 1alpha by macrophages in the rheumatoid synovium: implications for targeting of therapeutic genes to the inflamed joint. Arthritis Rheum 2001, 44:1540-1544. 10.1002/1529-0131(200107)44:7<1540::AID-ART277>3.0.CO;2-7, 11465705.
8. Jeon CH, Ahn JK, Chai JY, Kim HJ, Bae EK, Park SH, Cho EY, Cha HS, Ahn KS, Koh EM. Hypoxia appears at pre-arthritic stage and shows co-localization with early synovial inflammation in collagen induced arthritis. Clin Exp Rheumatol 2008, 26:646-648.
9. Oyanagui Y. Nitric oxide and superoxide radical are involved in both initiation and development of adjuvant arthritis in rats. Life Sci 1994, 54:PL285-289. 10.1016/0024-3205(94)00858-2, 8164499.
10. Hashimoto K, Fukuda K, Yamazaki K, Yamamoto N, Matsushita T, Hayakawa S, Munakata H, Hamanishi C. Hypoxia-induced hyaluronan synthesis by articular chondrocytes: the role of nitric oxide. Inflamm Res 2006, 55:72-77. 10.1007/s00011-005-0012-6, 16612567.
11. Ahn JK, Koh EM, Cha HS, Lee YS, Kim J, Bae EK, Ahn KS. Role of hypoxia-inducible factor-1alpha in hypoxia-induced expressions of IL-8, MMP-1 and MMP-3 in rheumatoid fibroblast-like synoviocytes. Rheumatology (Oxford) 2008, 47:834-839.
12. Farrell AJ, Blake DR, Palmer RM, Moncada S. Increased concentrations of nitrite in synovial fluid and serum samples suggest increased nitric oxide synthesis in rheumatic diseases. Ann Rheum Dis 1992, 51:1219-1222. 10.1136/ard.51.11.1219, 1012459, 1466599.
13. Cawston T. Matrix metalloproteinases and TIMPs: properties and implications for the rheumatic diseases. Mol Med Today 1998, 4:130-137. 10.1016/S1357-4310(97)01192-1, 9575496.
14. Tetlow LC, Wolley DE. Comparative immuno-localization studies of collagenase-1 and collagenase 3 production in the rheumatoid lesion, and by human chondrocytes and synoviocytes in vitro. Br J Rheumatol 1998, 37:64-70. 10.1093/rheumatology/37.1.64, 9487253.
15. Yoshihara Y, Nakamura H, Obata K, Yamada H, Hayakawa T, Fujikawa K, Okada Y. Matrix metalloproteinases and tissue inhibitors of metalloproteinases in synovial fluids from patients with rheumatoid arthritis or osteoarthritis. Ann Rheum Dis 2000, 59:455-461. 10.1136/ard.59.6.455, 1753174, 10834863.
16. Keyszer G, Lambiri I, Nagel R, Keysser C, Keysser M, Gromnica-Ihle E, Franz J, Burmester GR, Jung K. Circulating levels of matrix metalloproteinases MMP-3 and MMP-1, tissue inhibitor of metalloproteinases 1 (TIMP-1), and MMP-1/TIMP-1 complex in rheumatic disease. Correlation with clinical activity of rheumatoid arthritis versus other surrogate markers. J Rheumatol 1999, 26:251-258.
17. Fraisl P, Aragones J, Carmeliet P. Inhibition of oxygen sensors as a therapeutic strategy for ischaemic and inflammatory disease. Nat Rev Drug Discov 2009, 8:139-152. 10.1038/nrd2761, 19165233.
18. Chen W, Ostrowski RP, Obenaus A, Zhang JH. Prodeath or prosurvival: two facets of hypoxia inducible factor-1 in perinatal brain injury. Exp Neurol 2009, 216:7-15. 10.1016/j.expneurol.2008.10.016, 2672430, 19041643.
19. Miltner O, Schneider U, Siebert CH, Niedhart C, Niethard FU. Efficacy of intraarticular hyaluronic acid in patients with osteoarthritis-a prospective clinical trial. Osteoarthritis Cartilage 2002, 10:680-686. 10.1053/joca.2002.0815, 12202120.
20. Schimizzi AL, Massie JB, Murphy M, Perry A, Kim CW, Garfin SR, Akeson WH. High-molecular-weight hyaluronan inhibits macrophage proliferation and cytokine release in the early wound of a preclinical postlaminectomy rat model. Spine J 2006, 6:550-556. 10.1016/j.spinee.2005.12.005, 16934726.
21. Saito S, Momohara S, Taniguchi A, Yamanaka H. The intra-articular efficacy of hyaluronate injections in the treatment of rheumatoid arthritis. Mod Rheumatol 2009, 19:643-651. 10.1007/s10165-009-0207-8, 19649562.
22. Oliveira PG, Brenol CV, Edelweiss MI, Brenol JC, Petronilho F, Roesler R, Dal-Pizzol F, Schwartsmann G, Xavier RM. Effects of an antagonist of the bombesin/gastrin-releasing peptide receptor on complete Freund's adjuvant-induced arthritis in rats. Peptides 2008, 29:1726-1731. 10.1016/j.peptides.2008.05.031, 18590783.
23. Brauer R, Kittlick PD, Thoss K, Henzgen S. Different immunological mechanisms contribute to cartilage destruction in antigen-induced arthritis. Exp Toxicol Pathol 1994, 46:383-388.
24. Smith MM, Cake MA, Ghosh P, Schiavinato A, Read RA, Little CB. Significant synovial pathology in a meniscectomy model of osteoarthritis: modification by intra-articular hyaluronan therapy. Rheumatology (Oxford) 2008, 47:1172-1178.
25. Ferraccioli G, Bracci-Laudiero L, Alivernini S, Gremese E, Tolusso B, De Benedetti F. Interleukin-1beta and Interleukin-6 in arthritis animal models. Roles in the early phase of transition from the acute to chronic inflammation and relevance for human rheumatoid arthritis. Mol Med 2010, 16:552-557. 2972398, 20683549.
26. Morris CJ. Carrageenan-induced paw edema in the rat and mouse. Methods Mol Biol 2003, 225:115-121.
27. Campo GM, Avenoso A, Campo S, Ferlazzo AM, Altavilla D, Calatroni A. Efficacy of treatment with glycosaminoglycans on experimental collagen-induced arthritis in rats. Arthritis Res Ther 2003, 5:R122-131. 10.1186/ar748, 165044, 12723984.
28. Petrella RJ. Hyaluronic acid for the treatment of knee osteoarthritis: long-term outcomes from a naturalistic primary care experience. Am J Phys Med Rehabil 2005, 84:278-283; quiz 284, 293. 10.1097/01.PHM.0000156899.18885.06, 15785261.
29. Henderson EB, Smith EC, Pegley F, Blake DR. Intra-articular injections of 750 kD hyaluronan in the treatment of osteoarthritis: a randomised single centre double-blind placebo-controlled trial of 91 patients demonstrating lack of efficacy. Ann Rheum Dis 1994, 53:529-534. 10.1136/ard.53.8.529, 1005394, 7944639.
30. Puttick MP, Wade JP, Chalmers A, Connell DG, Rangno KK. Acute local reactions after intraarticular hylan for osteoarthritis of the knee. J Rheumatol 1995, 22:1311-1314.
31. Hamburger MI, Lakhanpal S, Mooar PA, Oster D. Intra-articular hyaluronans: a review of product-specific safety profiles. Semin Arthritis Rheum 2003, 32:296-309. 10.1053/sarh.2002.50008, 12701040.
32. Balazs EA. Analgesic effect of elastoviscous hyaluronan solutions and the treatment of arthritic pain. Cells Tissues Organs 2003, 174:49-62. 10.1159/000070574, 12784041.
33. Aihara S, Murakami N, Ishii R, Kariya K, Azuma Y, Hamada K, Umemoto J, Maeda S. Effects of sodium hyaluronate on the nociceptive response of rats with experimentally induced arthritis. Nippon Yakurigaku Zasshi 1992, 100:359-365. 10.1254/fpj.100.359, 1446887.
34. Pozo MA, Balazs EA, Belmonte C. Reduction of sensory responses to passive movements of inflamed knee joints by hylan, a hyaluronan derivative. Exp Brain Res 1997, 116:3-9. 10.1007/PL00005742, 9305809.
35. Gomis A, Pawlak M, Balazs EA, Schmidt RF, Belmonte C. Effects of different molecular weight elastoviscous hyaluronan solutions on articular nociceptive afferents. Arthritis Rheum 2004, 50:314-326. 10.1002/art.11421, 14730630.
36. Hashizume M, Koike N, Yoshida H, Suzuki M, Mihara M. High molecular weight hyaluronic acid relieved joint pain and prevented the progression of cartilage degeneration in a rabbit osteoarthritis model after onset of arthritis. Mod Rheumatol 2010, 20:432-438. 10.1007/s10165-010-0299-1, 20407800.
37. Ozkan FU, Ozkan K, Ramadan S, Guven Z. Chondroprotective effect of N-acetylglucosamine and hyaluronate in early stages of osteoarthritis-an experimental study in rabbits. Bull NYU Hosp Jt Dis 2009, 67:352-357.
38. Roth A, Mollenhauer J, Wagner A, Fuhrmann R, Straub A, Venbrocks RA, Petrow P, Bräuer R, Schubert H, Ozegowski J, Peschel G, Müller PJ, Kinne RW. Intra-articular injections of high-molecular-weight hyaluronic acid have biphasic effects on joint inflammation and destruction in rat antigen-induced arthritis. Arthritis Res Ther 2005, 7:R677-686. 10.1186/ar1725, 1174961, 15899053.
39. Tung JT, Venta PJ, Caron JP. Inducible nitric oxide expression in equine articular chondrocytes: effects of antiinflammatory compounds. Osteoarthritis Cartilage 2002, 10:5-12. 10.1053/joca.2001.0476, 11795978.
40. Takahashi K, Hashimoto S, Kubo T, Hirasawa Y, Lotz M, Amiel D. Hyaluronan suppressed nitric oxide production in the meniscus and synovium of rabbit osteoarthritis model. J Orthop Res 2001, 19:500-503. 10.1016/S0736-0266(00)90024-X, 11398866.
41. Lee YT, Shao HJ, Wang JH, Liu HC, Hou SM, Young TH. Hyaluronic acid modulates gene expression of connective tissue growth factor (CTGF), transforming growth factor-beta1 (TGF-beta1), and vascular endothelial growth factor (VEGF) in human fibroblast-like synovial cells from advanced-stage osteoarthritis in vitro. J Orthop Res 2010, 28:492-496.
42. Waddell DD, Kolomytkin OV, Dunn S, Marino AA. Hyaluronan suppresses IL-1beta-induced metalloproteinase activity from synovial tissue. Clin Orthop Relat Res 2007, 465:241-248.
43. Gaber T, Dziurla R, Tripmacher R, Burmester GR, Buttgereit F. Hypoxia inducible factor (HIF) in rheumatology: low O2! See what HIF can do!. Ann Rheum Dis 2005, 64:971-980. 10.1136/ard.2004.031641, 1755583, 15800008.
44. Muz B, Khan MN, Kiriakidis S, Paleolog EM. Hypoxia. The role of hypoxia and HIF-dependent signalling events in rheumatoid arthritis. Arthritis Res Ther 2009, 11:201. 10.1186/ar2568, 2688222, 19222864.
45. Issekutz AC, Sapru K. Modulation of adjuvant arthritis in the rat by 2-methoxyestradiol: an effect independent of an anti-angiogenic action. Int Immunopharmacol 2008, 8:708-716. 10.1016/j.intimp.2008.01.016, 18387513.
46. Westra J, Brouwer E, van Roosmalen IA, Doornbos-van der Meer B, van Leeuwen MA, Posthumus MD, Kallenberg CG. Expression and regulation of HIF-1alpha in macrophages under inflammatory conditions; significant reduction of VEGF by CaMKII inhibitor. BMC Musculoskelet Disord 2010, 11:61. 10.1186/1471-2474-11-61, 2851671, 20353560.
47. Rice JW, Veal JM, Fadden RP, Barabasz AF, Partridge JM, Barta TE, Dubois LG, Huang KH, Mabbett SR, Silinski MA, Steed PM, Hall SE. Small molecule inhibitors of Hsp90 potently affect inflammatory disease pathways and exhibit activity in models of rheumatoid arthritis. Arthritis Rheum 2008, 58:3765-3775. 10.1002/art.24047, 19035474.