High mobility group box protein 1 in complex with lipopolysaccharide or IL-1 promotes an increased inflammatory phenotype in synovial fibroblasts

Arthritis Research and Therapy

Volumn 13, Issue 4, 2011, Pages

  Wähämaa, Heidi ^a   Schierbeck, Hanna ^a   Hreggvidsdottir, Hulda S ^a   Palmblad, Karin ^a   Aveberger, Anne Charlotte ^a   Andersson, Ulf ^a   Harris, Helena E ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; STROMELYSIN; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR;

ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; OSTEOARTHRITIS; PHENOTYPE; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SYNOVIOCYTE;

EID: 80053261217     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3450     Document Type: Article

References (52)

1. Yang H, Wang H, Tracey KJ. HMG-1 rediscovered as a cytokine. Shock 2001, 15:247-253. 10.1097/00024382-200115040-00001, 11303722.
2. Andersson U, Wang H, Palmblad K, Aveberger AC, Bloom O, Erlandsson-Harris H, Janson A, Kokkola R, Zhang M, Yang H, Tracey KJ. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med 2000, 192:565-570. 10.1084/jem.192.4.565, 2193240, 10952726.
3. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002, 418:191-195. 10.1038/nature00858, 12110890.
4. Fiuza C, Bustin M, Talwar S, Tropea M, Gerstenberger E, Shelhamer JH, Suffredini AF. Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells. Blood 2003, 101:2652-2660. 10.1182/blood-2002-05-1300, 12456506.
5. Treutiger CJ, Mullins GE, Johansson AS, Rouhiainen A, Rauvala HM, Erlandsson-Harris H, Andersson U, Yang H, Tracey KJ, Andersson J, Palmblad JE. High mobility group 1 B-box mediates activation of human endothelium. J Intern Med 2003, 254:375-385. 10.1046/j.1365-2796.2003.01204.x, 12974876.
6. Yang D, Chen Q, Yang H, Tracey KJ, Bustin M, Oppenheim JJ. High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin. J Leukoc Biol 2007, 81:59-66.
7. Rovere-Querini P, Capobianco A, Scaffidi P, Valentinis B, Catalanotti F, Giazzon M, Dumitriu IE, Müller S, Iannacone M, Traversari C, Bianchi ME, Manfredi AA. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep 2004, 5:825-830. 10.1038/sj.embor.7400205, 1299116, 15272298.
8. Messmer D, Yang H, Telusma G, Knoll F, Li J, Messmer B, Tracey KJ, Chiorazzi N. High mobility group box protein 1: an endogenous signal for dendritic cell maturation and Th1 polarization. J Immunol 2004, 173:307-313.
9. Dumitriu IE, Baruah P, Valentinis B, Voll RE, Herrmann M, Nawroth PP, Arnold B, Bianchi ME, Manfredi AA, Rovere-Querini P. Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. J Immunol 2005, 174:7506-7515.
10. Locher C, Rusakiewicz S, Tesnière A, Ghiringhelli F, Apetoh L, Kroemer G, Zitvogel L. Witch hunt against tumor cells enhanced by dendritic cells. Ann N Y Acad Sci 2009, 1174:51-60. 10.1111/j.1749-6632.2009.04940.x, 19769736.
11. Sundberg E, Fasth AE, Palmblad K, Harris HE, Andersson U. High mobility group box chromosomal protein 1 acts as a proliferation signal for activated T lymphocytes. Immunobiology 2009, 214:303-309. 10.1016/j.imbio.2008.09.006, 19201506.
12. Andersson U, Tracey KJ. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol 2011, 29:139-162. 10.1146/annurev-immunol-030409-101323, 21219181, 21219181.
13. Yang H, Hreggvidsdottir HS, Palmblad K, Wang H, Ochani M, Li J, Lu B, Chavan S, Rosas-Ballina M, Al-Abed Y, Akira S, Bierhaus A, Erlandsson-Harris H, Andersson U, Tracey KJ. A critical cysteine is required for HMGB1 binding to Toll-like receptor 4 and activation of macrophage cytokine release. Proc Natl Acad Sci USA 2010, 107:11942-11947. 10.1073/pnas.1003893107, 2900689, 20547845.
14. Kazama H, Ricci JE, Herndon JM, Hoppe G, Green DR, Ferguson TA. Induction of immunological tolerance by apoptotic cells requires caspase-dependent oxidation of high-mobility group box-1 protein. Immunity 2008, 29:21-32. 10.1016/j.immuni.2008.05.013, 2704496, 18631454.
15. Ivanov S, Dragoi AM, Wang X, Dallacosta C, Louten J, Musco G, Sitia G, Yap GS, Wan Y, Biron CA, Bianchi ME, Wang H, Chu WM. A novel role for HMGB1 in TLR9-mediated inflammatory responses to CpG-DNA. Blood 2007, 110:1970-1981. 10.1182/blood-2006-09-044776, 1976374, 17548579.
16. Tian J, Avalos AM, Mao SY, Chen B, Senthil K, Wu H, Parroche P, Drabic S, Golenbock D, Sirois C, Hua J, An LL, Audoly L, La Rosa G, Bierhaus A, Naworth P, Marshak-Rothstein A, Crow MK, Fitzgerald KA, Latz E, Kiener PA, Coyle AJ. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 2007, 8:487-496.
17. Sha Y, Zmijewski J, Xu Z, Abraham E. HMGB1 develops enhanced proinflammatory activity by binding to cytokines. J Immunol 2008, 180:2531-2537.
18. Hreggvidsdottir HS, Ostberg T, Wähämaa H, Schierbeck H, Aveberger AC, Klevenvall L, Palmblad K, Ottosson L, Andersson U, Harris HE. The alarmin HMGB1 acts in synergy with endogenous and exogenous danger signals to promote inflammation. J Leukoc Biol 2009, 86:655-662. 10.1189/jlb.0908548, 19564572.
19. Urbonaviciute V, Fürnrohr BG, Meister S, Munoz L, Heyder P, De Marchis F, Bianchi ME, Kirschning C, Wagner H, Manfredi AA, Kalden JR, Schett G, Rovere-Querini P, Herrmann M, Voll RE. Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: implications for the pathogenesis of SLE. J Exp Med 2008, 205:3007-3018. 10.1084/jem.20081165, 2605236, 19064698.
20. Kwak MS, Wu J, Kim ES, Ji Y, Min HJ, Yoo JH, Choi JE, Cho HS, Shin JS. Identification of lipopolysaccharide-binding peptide regions within HMGB1 and their effects on subclinical endotoxemia in a mouse model. Eur J Immunol 2011,
21. Kokkola R, Sundberg E, Ulfgren AK, Palmblad K, Li J, Wang H, Ulloa L, Yang H, Yan XJ, Furie R, Chiorazzi N, Tracey KJ, Andersson U, Harris HE. High mobility group box chromosomal protein 1: a novel proinflammatory mediator in synovitis. Arthritis Rheum 2002, 46:2598-2603. 10.1002/art.10540, 12384917.
22. Palmblad K, Sundberg E, Diez M, Söderling R, Aveberger AC, Andersson U, Harris HE. Morphological characterization of intra-articular HMGB1 expression during the course of collagen-induced arthritis. Arthritis Res Ther 2007, 9:R35. 10.1186/ar2155, 1906813, 17397533.
23. Taniguchi N, Kawahara K, Yone K, Hashiguchi T, Yamakuchi M, Goto M, Inoue K, Yamada S, Ijiri K, Matsunaga S, Nakajima T, Komiya S, Maruyama I. High mobility group box chromosomal protein 1 plays a role in the pathogenesis of rheumatoid arthritis as a novel cytokine. Arthritis Rheum 2003, 48:971-981. 10.1002/art.10859, 12687539.
24. Hamada T, Torikai M, Kuwazuru A, Tanaka M, Horai N, Fukuda T, Yamada S, Nagayama S, Hashiguchi K, Sunahara N, Fukuzaki K, Nagata R, Komiya S, Maruyama I, Fukuda T, Abeyama K. Extracellular high mobility group box chromosomal protein 1 is a coupling factor for hypoxia and inflammation in arthritis. Arthritis Rheum 2008, 58:2675-2685. 10.1002/art.23729, 18759291.
25. Garcia-Arnandis I, Guillén MI, Gomar F, Pelletier JP, Martel-Pelletier J, Alcaraz MJ. High mobility group box 1 potentiates the pro-inflammatory effects of interleukin-1beta in osteoarthritic synoviocytes. Arthritis Res Ther 2010, 12:R165. 10.1186/ar3124, 2945068, 20799933.
26. Heinola T, Kouri VP, Clarijs P, Ciferska H, Sukura A, Salo J, Konttinen YT. High mobility group box-1 (HMGB-1) in osteoarthritic cartilage. Clin Exp Rheumatol 2010, 28:511-518.
27. Pullerits R, Jonsson IM, Verdrengh M, Bokarewa M, Andersson U, Erlandsson-Harris H, Tarkowski A. High mobility group box chromosomal protein 1, a DNA binding cytokine, induces arthritis. Arthritis Rheum 2003, 48:1693-1700. 10.1002/art.11028, 12794838.
28. Kokkola R, Li J, Sundberg E, Aveberger AC, Palmblad K, Yang H, Tracey KJ, Andersson U, Harris HE. Successful treatment of collagen-induced arthritis in mice and rats by targeting extracellular high mobility group box chromosomal protein 1 activity. Arthritis Rheum 2003, 48:2052-2058. 10.1002/art.11161, 12847700.
29. Pisetsky DS, Erlandsson-Harris H, Andersson U. High-mobility group box protein 1 (HMGB1): an alarmin mediating the pathogenesis of rheumatic disease. Arthritis Res Ther 2008, 10:209. 10.1186/ar2440, 2483460, 18598385.
30. Ostberg T, Kohki K, Shigekazu N, Huan Y, Sangeeta C, Lena K, Marco B, Helena Erlandssson H, Ulf A, Karin P. Protective targeting of high mobility group box chromosomal protein 1 in a spontaneous arthritis model. Arthritis Rheum 2010, 62:2963-2972. 10.1002/art.27590, 20533288.
31. Schierbeck H, Lundbäck P, Palmblad K, Klevenvall L, Erlandsson-Harris H, Andersson U, Ottosson L. Monoclonal anti-HMGB1 antibody protection in two experimental arthritis models. Mol Med 2011,
32. Mor A, Abramson SB, Pillinger MH. The fibroblast-like synovial cell in rheumatoid arthritis: a key player in inflammation and joint destruction. Clin Immunol 2005, 115:118-128. 10.1016/j.clim.2004.12.009, 15885632.
33. Pap T, Müller-Ladner U, Gay RE, Gay S. Fibroblast biology. Role of synovial fibroblasts in the pathogenesis of rheumatoid arthritis. Arthritis Res 2000, 2:361-367. 10.1186/ar113, 130137, 11094449.
34. Brentano F, Kyburz D, Schorr O, Gay R, Gay S. The role of Toll-like receptor signalling in the pathogenesis of arthritis. Cell Immunol 2005, 233:90-96. 10.1016/j.cellimm.2005.04.018, 15963480.
35. Ospelt C, Brentano F, Rengel Y, Stanczyk J, Kolling C, Tak PP, Gay RE, Gay S, Kyburz D. Overexpression of toll-like receptors 3 and 4 in synovial tissue from patients with early rheumatoid arthritis: toll-like receptor expression in early and longstanding arthritis. Arthritis Rheum 2008, 58:3684-3692. 10.1002/art.24140, 19035519.
36. Jung YO, Cho ML, Kang CM, Jhun JY, Park JS, Oh HJ, Min JK, Park SH, Kim HY. Toll-like receptor 2 and 4 combination engagement upregulate IL-15 synergistically in human rheumatoid synovial fibroblasts. Immunol Lett 2007, 109:21-27. 10.1016/j.imlet.2006.12.006, 17289161.
37. Kay J, Calabrese L. The role of interleukin-1 in the pathogenesis of rheumatoid arthritis. Rheumatology (Oxford) 2004, 43:iii2-iii9.
38. Farahat MN, Yanni G, Poston R, Panayi GS. Cytokine expression in synovial membranes of patients with rheumatoid arthritis and osteoarthritis. Ann Rheum Dis 1993, 52:870-875. 10.1136/ard.52.12.870, 1005218, 8311538.
39. Smith MD, Triantafillou S, Parker A, Youssef PP, Coleman M. Synovial membrane inflammation and cytokine production in patients with early osteoarthritis. J Rheumatol 1997, 24:365-371.
40. Kahle P, Saal JG, Schaudt K, Zacher J, Fritz P, Pawelec G. Determination of cytokines in synovial fluids: correlation with diagnosis and histomorphological characteristics of synovial tissue. Ann Rheum Dis 1992, 51:731-734. 10.1136/ard.51.6.731, 1004735, 1616355.
41. Melief MJ, Hoijer MA, Van Paassen HC, Hazenberg MP. Presence of bacterial flora-derived antigen in synovial tissue macrophages and dendritic cells. Br J Rheumatol 1995, 34:1112-1116. 10.1093/rheumatology/34.12.1112, 8608350.
42. Kempsell KE, Cox CJ, Hurle M, Wong A, Wilkie S, Zanders ED, Gaston JS, Crowe JS. Reverse transcriptase-PCR analysis of bacterial rRNA for detection and characterization of bacterial species in arthritis synovial tissue. Infect Immun 2000, 68:6012-6026. 10.1128/IAI.68.10.6012-6026.2000, 101566, 10992514.
43. Glennås A, Thorsrud AK, Rugstad HE, Jellum E. Mapping of proteins from cultured fibroblasts of synovial and subcutaneous origin by high resolution two-dimensional polyacrylamide gel electrophoresis. Ann Rheum Dis 1985, 44:302-306. 10.1136/ard.44.5.302, 1001636, 4004359.
44. Paonessa G, Frank R, Cortese R. Nucleotide sequence of rat liver HMG1 cDNA. Nucleic Acids Res 1987, 15:9077. 10.1093/nar/15.21.9077, 306425, 3684582.
45. Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, Manogue KR, Faist E, Abraham E, Andersson J, Andersson U, Molina PE, Abumrad NN, Sama A, Tracey KJ. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999, 285:248-251. 10.1126/science.285.5425.248, 10398600.
46. Yu M, Wang H, Ding A, Golenbock DT, Latz E, Czura CJ, Fenton MJ, Tracey KJ, Yang H. HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock 2006, 26:174-179. 10.1097/01.shk.0000225404.51320.82, 16878026.
47. Antoine DJ, Williams DP, Kipar A, Laverty H, Park BK. Diet restriction inhibits apoptosis and HMGB1 oxidation and promotes inflammatory cell recruitment during acetaminophen hepatotoxicity. Mol Med 2010, 16:479-490. 2972397, 20811657.
48. Youn JH, Oh YJ, Kim ES, Choi JE, Shin J. High mobility group box 1 protein binding to lipopolysaccharide facilitates transfer of lipopolysaccharide to CD14 and enhances lipopolysaccharide-mediated TNF-alpha production in human monocytes. J Immunol 2008, 180:5067-5074.
49. Kim KW, Cho ML, Lee SH, Oh HJ, Kang CM, Ju JH, Min SY, Cho YG, Park SH, Kim H. Human rheumatoid synovial fibroblasts promote osteoclastogenic activity by activating RANKL via TLR-2 and TLR-4 activation. Immunol Lett 2007, 110:54-64. 10.1016/j.imlet.2007.03.004, 17467812.
50. Hou FF, Jiang JP, Guo JQ, Wang GB, Zhang X, Stern DM, Schmidt AM, Owen WF. Receptor for advanced glycation end products on human synovial fibroblasts: role in the pathogenesis of dialysis-related amyloidosis. J Am Soc Nephrol 2002, 13:1296-1306.
51. Steenvoorden MM, Toes RE, Ronday HK, Huizinga TW, Degroot J. RAGE activation induces invasiveness of RA fibroblast-like synoviocytes in vitro. Clin Exp Rheumatol 2007, 25:740-742.
52. Richette P, François M, Vicaut E, Fitting C, Bardin T, Corvol M, Savouret JF, Rannou F. A high interleukin 1 receptor antagonist/IL-1beta ratio occurs naturally in knee osteoarthritis. J Rheumatol 2008, 35:1650-1654.