Overexpression of a minimal domain of calpastatin suppresses il-6 production and th17 development via reduced nf-κb and increased stat5 signals

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Iguchi Hashimoto, Mikiko ^a   Usui, Takashi ^a   Yoshifuji, Hajime ^a   Shimizu, Masakazu ^a   Kobayashi, Shio ^a   Ito, Yoshinaga ^a   Murakami, Kosaku ^a   Shiomi, Aoi ^a   Yukawa, Naoichiro ^a   Kawabata, Daisuke ^a   Nojima, Takaki ^a   Ohmura, Koichiro ^a   Fujii, Takao ^a   Mimori, Tsuneyo ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CALPASTATIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 6; RETINOID RELATED ORPHAN RECEPTOR GAMMA; RETINOID RELATED ORPHAN RECEPTOR GAMMA T; STAT3 PROTEIN; STAT5 PROTEIN; UNCLASSIFIED DRUG; CALCIUM BINDING PROTEIN; IL6 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FIBROBLAST; HELPER CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; RHEUMATOID ARTHRITIS; TH1 CELL; TH17 CELL; TH2 CELL; UPREGULATION; BIOSYNTHESIS; CELL CULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INFLAMMATION; METABOLISM; PATHOLOGY; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

ARTHRITIS, RHEUMATOID; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INTERLEUKIN-17; INTERLEUKIN-6; NF-KAPPA B; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; TH17 CELLS;

EID: 80055115845     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027020     Document Type: Article

References (62)

1. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, et al. (2005) Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6: 1123-1132.
2. Park H, Li Z, Yang XO, Chang SH, Nurieva R, et al. (2005) A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 6: 1133-1141.
3. Usui T, (2007) [Transcription factors that regulate helper T cell differentiation]. Nihon Rinsho Meneki Gakkai Kaishi 30: 419-427.
4. Nishikomori R, Usui T, Wu CY, Morinobu A, O'Shea JJ, et al. (2002) Activated STAT4 has an essential role in Th1 differentiation and proliferation that is independent of its role in the maintenance of IL-12R beta 2 chain expression and signaling. J Immunol 169: 4388-4398.
5. Usui T, Nishikomori R, Kitani A, Strober W, (2003) GATA-3 suppresses Th1 development by downregulation of Stat4 and not through effects on IL-12Rbeta2 chain or T-bet. Immunity 18: 415-428.
6. Usui T, Preiss JC, Kanno Y, Yao ZJ, Bream JH, et al. (2006) T-bet regulates Th1 responses through essential effects on GATA-3 function rather than on IFNG gene acetylation and transcription. J Exp Med 203: 755-766.
7. Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, et al. (2006) The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133.
8. Mangan PR, Harrington LE, O'Quinn DB, Helms WS, Bullard DC, et al. (2006) Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441: 231-234.
9. Yang XO, Panopoulos AD, Nurieva R, Chang SH, Wang D, et al. (2007) STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J Biol Chem 282: 9358-9363.
10. Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F, (2007) Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol 8: 942-949.
11. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, et al. (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
12. Lubberts E, Joosten LA, Oppers B, van den Bersselaar L, Coenen-de Roo CJ, et al. (2001) IL-1-independent role of IL-17 in synovial inflammation and joint destruction during collagen-induced arthritis. J Immunol 167: 1004-1013.
13. Lubberts E, Koenders MI, Oppers-Walgreen B, van den Bersselaar L, Coenen-de Roo CJ, et al. (2004) Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of collagen-induced arthritis reduces joint inflammation, cartilage destruction, and bone erosion. Arthritis Rheum 50: 650-659.
14. Yamada H, Nakashima Y, Okazaki K, Mawatari T, Fukushi JI, et al. (2008) Th1 but not Th17 cells predominate in the joints of patients with rheumatoid arthritis. Ann Rheum Dis 67: 1299-1304.
15. Ito Y, Usui T, Kobayashi S, Iguchi-Hashimoto M, Ito H, et al. (2009) Gamma/delta T cells are the predominant source of interleukin-17 in affected joints in collagen-induced arthritis, but not in rheumatoid arthritis. Arthritis Rheum 60: 2294-2303.
16. Suzuki A, Yamada R, Chang X, Tokuhiro S, Sawada T, et al. (2003) Functional haplotypes of PADI4, encoding citrullinating enzyme peptidylarginine deiminase 4, are associated with rheumatoid arthritis. Nat Genet 34: 395-402.
17. Cho YG, Cho ML, Min SY, Kim HY, (2007) Type II collagen autoimmunity in a mouse model of human rheumatoid arthritis. Autoimmun Rev 7: 65-70.
18. Schaller M, Burton DR, Ditzel HJ, (2001) Autoantibodies to GPI in rheumatoid arthritis: linkage between an animal model and human disease. Nat Immunol 2: 746-753.
19. Mimori T, Suganuma K, Tanami Y, Nojima T, Matsumura M, et al. (1995) Autoantibodies to calpastatin (an endogenous inhibitor for calcium-dependent neutral protease, calpain) in systemic rheumatic diseases. Proc Natl Acad Sci U S A 92: 7267-7271.
20. Despres N, Talbot G, Plouffe B, Boire G, Menard HA, (1995) Detection and expression of a cDNA clone that encodes a polypeptide containing two inhibitory domains of human calpastatin and its recognition by rheumatoid arthritis sera. J Clin Invest 95: 1891-1896.
21. Matsushita Y, Shimada Y, Kawara S, Takehara K, Sato S, (2005) Autoantibodies directed against the protease inhibitor calpastatin in psoriasis. Clin Exp Immunol 139: 355-362.
22. Iwaki-Egawa S, Matsuno H, Yudoh K, Nakazawa F, Miyazaki K, et al. (2004) High diagnostic value of anticalpastatin autoantibodies in rheumatoid arthritis detected by ELISA using human erythrocyte calpastatin as antigen. J Rheumatol 31: 17-22.
23. Lackner KJ, Schlosser U, Lang B, Schmitz G, (1998) Autoantibodies against human calpastatin in rheumatoid arthritis: epitope mapping and analysis of patient sera. Br J Rheumatol 37: 1164-1171.
24. Yasuhiko Kanazawa YK, Sawa Masayo, Yasuoka Hidekata, Nojima Takaki, Ohosone Yasuo, Mimori Tuneyo, (2000) Domain reactivity of autoantibodies to calpastatin in patients with systemic rheumatic diseases. Modern Rheumatology 10: 38-44.
25. Vittecoq O, Salle V, Jouen-Beades F, Krzanowska K, Menard JF, et al. (2001) Autoantibodies to the 27 C-terminal amino acids of calpastatin are detected in a restricted set of connective tissue diseases and may be useful for diagnosis of rheumatoid arthritis in community cases of very early arthritis. Rheumatology (Oxford) 40: 1126-1134.
26. Goll DE, Thompson VF, Li H, Wei W, Cong J, (2003) The calpain system. Physiol Rev 83: 731-801.
27. Fukui I, Tanaka K, Murachi T, (1989) Extracellular appearance of calpain and calpastatin in the synovial fluid of the knee joint. Biochem Biophys Res Commun 162: 559-566.
28. Szomor Z, Shimizu K, Fujimori Y, Yamamoto S, Yamamuro T, (1995) Appearance of calpain correlates with arthritis and cartilage destruction in collagen induced arthritic knee joints of mice. Ann Rheum Dis 54: 477-483.
29. Suzuki K, Shimizu K, Hamamoto T, Nakagawa Y, Murachi T, et al. (1992) Characterization of proteoglycan degradation by calpain. Biochem J 285: 857-862.
30. Cuzzocrea S, McDonald MC, Mazzon E, Siriwardena D, Serraino I, et al. (2000) Calpain inhibitor I reduces the development of acute and chronic inflammation. Am J Pathol 157: 2065-2079.
31. Stewart MP, McDowall A, Hogg N, (1998) LFA-1-mediated adhesion is regulated by cytoskeletal restraint and by a Ca2+-dependent protease, calpain. J Cell Biol 140: 699-707.
32. Selliah N, Brooks WH, Roszman TL, (1996) Proteolytic cleavage of alpha-actinin by calpain in T cells stimulated with anti-CD3 monoclonal antibody. J Immunol 156: 3215-3221.
33. Yoshifuji H, Umehara H, Maruyama H, Itoh M, Tanaka M, et al. (2005) Amelioration of experimental arthritis by a calpain-inhibitory compound: regulation of cytokine production by E-64-d in vivo and in vitro. Int Immunol 17: 1327-1336.
34. Usui T, Wakatsuki Y, Matsunaga Y, Kaneko S, Koseki H, et al. (1997) Overexpression of B cell-specific activator protein (BSAP/Pax-5) in a late B cell is sufficient to suppress differentiation to an Ig high producer cell with plasma cell phenotype. J Immunol 158: 3197-3204.
35. Sasaki T, Kishi M, Saito M, Tanaka T, Higuchi N, et al. (1990) Inhibitory effect of di- and tripeptidyl aldehydes on calpains and cathepsins. J Enzyme Inhib 3: 195-201.
36. Tamai M, Matsumoto K, Omura S, Koyama I, Ozawa Y, et al. (1986) In vitro and in vivo inhibition of cysteine proteinases by EST, a new analog of E-64. J Pharmacobiodyn 9: 672-677.
37. Emori Y, Kawasaki H, Imajoh S, Minami Y, Suzuki K, (1988) All four repeating domains of the endogenous inhibitor for calcium-dependent protease independently retain inhibitory activity. Expression of the cDNA fragments in Escherichia coli. J Biol Chem 263: 2364-2370.
38. Hayakawa M, Hayakawa H, Matsuyama Y, Tamemoto H, Okazaki H, et al. (2009) Mature interleukin-33 is produced by calpain-mediated cleavage in vivo. Biochem Biophys Res Commun 387: 218-222.
39. Li C, Chen S, Yue P, Deng X, Lonial S, et al. (2010) Proteasome inhibitor PS-341 (bortezomib) induces calpain-dependent IkappaB(alpha) degradation. J Biol Chem 285: 16096-16104.
40. Noguchi M, Sarin A, Aman MJ, Nakajima H, Shores EW, et al. (1997) Functional cleavage of the common cytokine receptor gamma chain (gammac) by calpain. Proc Natl Acad Sci U S A 94: 11534-11539.
41. Letavernier E, Dansou B, Lochner M, Perez J, Bellocq A, et al. (2011) Critical role of the calpain/calpastatin balance in acute allograft rejection. Eur J Immunol 41: 473-484.
42. Laurence A, Tato CM, Davidson TS, Kanno Y, Chen Z, et al. (2007) Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 26: 371-381.
43. Chen F, Demers LM, Vallyathan V, Lu Y, Castranova V, et al. (2000) Impairment of NF-kappaB activation and modulation of gene expression by calpastatin. Am J Physiol Cell Physiol 279: 709-716.
44. Chen F, Lu Y, Kuhn DC, Maki M, Shi X, et al. (1997) Calpain contributes to silica-induced I kappa B-alpha degradation and nuclear factor-kappa B activation. Arch Biochem Biophys 342: 383-388.
45. Milligan SA, Owens MW, Grisham MB, (1996) Inhibition of IkappaB-alpha and IkappaB-beta proteolysis by calpain inhibitor I blocks nitric oxide synthesis. Arch Biochem Biophys 335: 388-395.
46. Yamamoto S, Shimizu K, Suzuki K, Nakagawa Y, Yamamuro T, (1992) Calcium-dependent cysteine proteinase (calpain) in human arthritic synovial joints. Arthritis Rheum 35: 1309-1317.
47. Suzuki K, Shimizu K, Hamamoto T, Nakagawa Y, Hamakubo T, et al. (1990) Biochemical demonstration of calpains and calpastatin in osteoarthritic synovial fluid. Arthritis Rheum 33: 728-732.
48. Hayashi M, Koshihara Y, Ishibashi H, Yamamoto S, Tsubuki S, et al. (2005) Involvement of calpain in osteoclastic bone resorption. J Biochem 137: 331-338.
49. Liu ZQ, Kunimatsu M, Yang JP, Ozaki Y, Sasaki M, et al. (1996) Proteolytic processing of nuclear factor kappa B by calpain in vitro. FEBS Lett 385: 109-113.
50. Schaecher K, Goust JM, Banik NL, (2004) The effects of calpain inhibition on IkB alpha degradation after activation of PBMCs: identification of the calpain cleavage sites. Neurochem Res 29: 1443-1451.
51. Lee FY, Kim DW, Karmin JA, Hong D, Chang SS, et al. (2005) mu-Calpain regulates receptor activator of NF-kappaB ligand (RANKL)-supported osteoclastogenesis via NF-kappaB activation in RAW 264.7 cells. J Biol Chem 280: 29929-29936.
52. Brozik M, Rosztoczy I, Meretey K, Balint G, Gaal M, et al. (1992) Interleukin 6 levels in synovial fluids of patients with different arthritides: correlation with local IgM rheumatoid factor and systemic acute phase protein production. J Rheumatol 19: 63-68.
53. Choy EH, Isenberg DA, Garrood T, Farrow S, Ioannou Y, et al. (2002) Therapeutic benefit of blocking interleukin-6 activity with an anti-interleukin-6 receptor monoclonal antibody in rheumatoid arthritis: a randomized, double-blind, placebo-controlled, dose-escalation trial. Arthritis Rheum 46: 3143-3150.
54. Nishimoto N, Miyasaka N, Yamamoto K, Kawai S, Takeuchi T, et al. (2009) Study of active controlled tocilizumab monotherapy for rheumatoid arthritis patients with an inadequate response to methotrexate (SATORI): significant reduction in disease activity and serum vascular endothelial growth factor by IL-6 receptor inhibition therapy. Mod Rheumatol 19: 12-19.
55. Nishimoto N, Hashimoto J, Miyasaka N, Yamamoto K, Kawai S, et al. (2007) Study of active controlled monotherapy used for rheumatoid arthritis, an IL-6 inhibitor (SAMURAI): evidence of clinical and radiographic benefit from an x ray reader-blinded randomised controlled trial of tocilizumab. Ann Rheum Dis 66: 1162-1167.
56. Han Z, Boyle DL, Manning AM, Firestein GS, (1998) AP-1 and NF-kappaB regulation in rheumatoid arthritis and murine collagen-induced arthritis. Autoimmunity 28: 197-208.
57. Handel ML, McMorrow LB, Gravallese EM, (1995) Nuclear factor-kappa B in rheumatoid synovium. Localization of p50 and p65. Arthritis Rheum 38: 1762-1770.
58. Benito MJ, Murphy E, Murphy EP, van den Berg WB, FitzGerald O, et al. (2004) Increased synovial tissue NF-kappa B1 expression at sites adjacent to the cartilage-pannus junction in rheumatoid arthritis. Arthritis Rheum 50: 1781-1787.
59. Gupta SC, Sundaram C, Reuter S, Aggarwal BB, (2010) Inhibiting NF-kappaB activation by small molecules as a therapeutic strategy. Biochim Biophys Acta 1799: 775-787.
60. Nakae S, Nambu A, Sudo K, Iwakura Y, (2003) Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J Immunol 171: 6173-6177.
61. Leipe J, Grunke M, Dechant C, Reindl C, Kerzendorf U, et al. (2011) Role of Th17 cells in human autoimmune arthritis. Arthritis Rheum 62: 2876-2885.
62. Hueber W, Patel DD, Dryja T, Wright AM, Koroleva I, et al. (2010) Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci Transl Med 2: 52-72.