STA-21, a promising STAT-3 inhibitor that reciprocally regulates Th17 and Treg cells, inhibits osteoclastogenesis in mice and humans and alleviates autoimmune inflammation in an experimental model of rheumatoid arthritis

Arthritis and Rheumatology

Volumn 66, Issue 4, 2014, Pages 918-929

  Park, Jin Sil ^a   Kwok, Seung Ki ^a   Lim, Mi Ae ^a   Kim, Eun Kyung ^a   Ryu, Jun Geol ^a   Kim, Sung Min ^a   Oh, Hye Joa ^a   Ju, Ji Hyeon ^a   Park, Sung Hwan ^a   Kim, Ho Youn ^a   Cho, Mi La ^a  

^a The Catholic University of Korea   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; ANTIRHEUMATIC AGENT; COLONY STIMULATING FACTOR 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; OSTEOCLAST DIFFERENTIATION FACTOR; STA 21; STAT3 PROTEIN; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BONE DESTRUCTION; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; ENZYME ACTIVITY; EXPERIMENTAL ARTHRITIS; MONOCYTE MACROPHAGE PRECURSOR CELL; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; TH17 CELL;

ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; HUMANS; INFLAMMATION; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, KNOCKOUT; OSTEOCLASTS; POLYCYCLIC COMPOUNDS; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 84898645573     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.38305     Document Type: Article

References (49)

1. Feldmann M, Brennan FM, Maini RN,. Rheumatoid arthritis. Cell 1996; 85: 307-10.
2. Firestein GS,. Invasive fibroblast-like synoviocytes in rheumatoid arthritis: passive responders or transformed aggressors? Arthritis Rheum 1996; 39: 1781-90.
3. Molenaar ET, Voskuyl AE, Dinant HJ, Bezemer PD, Boers M, Dijkmans BA,. Progression of radiologic damage in patients with rheumatoid arthritis in clinical remission. Arthritis Rheum 2004; 50: 36-42.
4. Gravallese EM,. Bone destruction in arthritis. Ann Rheum Dis 2002; 61 Suppl 2: 84-6.
5. O'Gradaigh D, Ireland D, Bord S, Compston JE,. Joint erosion in rheumatoid arthritis: interactions between tumour necrosis factor alpha, interleukin 1, and receptor activator of nuclear factor kappaB ligand (RANKL) regulate osteoclasts. Ann Rheum Dis 2004; 63: 354-9.
6. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL,. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 1986; 136: 2348-57.
7. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, et al. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005; 6: 1123-32.
8. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005; 6: 1133-41.
9. Dong C,. Differentiation and function of pro-inflammatory Th17 cells. Microbes Infect 2009; 11: 584-8.
10. Tesmer LA, Lundy SK, Sarkar S, Fox DA,. Th17 cells in human disease. Immunol Rev 2008; 223: 87-113.
11. Lundy SK, Sarkar S, Tesmer LA, Fox DA,. Cells of the synovium in rheumatoid arthritis: T lymphocytes. Arthritis Res Ther 2007; 9: 202.
12. Akira S, Nishio Y, Inoue M, Wang XJ, Wei S, Matsusaka T, et al. Molecular cloning of APRF, a novel IFN-stimulated gene factor 3 p91-related transcription factor involved in the gp130-mediated signaling pathway. Cell 1994; 77: 63-71.
13. Yang XO, Panopoulos AD, Nurieva R, Chang SH, Wang D, Watowich SS, et al. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J Biol Chem 2007; 282: 9358-63.
14. Nowell MA, Richards PJ, Fielding CA, Ognjanovic S, Topley N, Williams AS, et al. Regulation of pre-B cell colony-enhancing factor by STAT-3-dependent interleukin-6 trans-signaling: implications in the pathogenesis of rheumatoid arthritis. Arthritis Rheum 2006; 54: 2084-95.
15. De Hooge AS, van de Loo FA, Koenders MI, Bennink MB, Arntz OJ, Kolbe T, et al. Local activation of STAT-1 and STAT-3 in the inflamed synovium during zymosan-induced arthritis: exacerbation of joint inflammation in STAT-1 gene-knockout mice. Arthritis Rheum 2004; 50: 2014-23.
16. Shouda T, Yoshida T, Hanada T, Wakioka T, Oishi M, Miyoshi K, et al. Induction of the cytokine signal regulator SOCS3/CIS3 as a therapeutic strategy for treating inflammatory arthritis. J Clin Invest 2001; 108: 1781-8.
17. Sawa S, Kamimura D, Jin GH, Morikawa H, Kamon H, Nishihara M, et al. Autoimmune arthritis associated with mutated interleukin (IL)-6 receptor gp130 is driven by STAT3/IL-7-dependent homeostatic proliferation of CD4+ T cells. J Exp Med 2006; 203: 1459-70.
18. Mori T, Miyamoto T, Yoshida H, Asakawa M, Kawasumi M, Kobayashi T, et al. IL-1beta and TNFalpha-initiated IL-6-STAT3 pathway is critical in mediating inflammatory cytokines and RANKL expression in inflammatory arthritis. Int Immunol 2011; 23: 701-12.
19. Murakami M, Hirano T,. A four-step model for the IL-6 amplifier, a regulator of chronic inflammations in tissue-specific MHC class II-associated autoimmune diseases. Front Immunol 2011; 2: 22.
20. Song H, Wang R, Wang S, Lin J,. A low-molecular-weight compound discovered through virtual database screening inhibits Stat3 function in breast cancer cells. Proc Natl Acad Sci U S A 2005; 102: 4700-5.
21. Nguyen LT, Jacobs J, Mathis D, Benoist C,. Where FoxP3-dependent regulatory T cells impinge on the development of inflammatory arthritis. Arthritis Rheum 2007; 56: 509-20.
22. Park JS, Lim MA, Cho ML, Ryu JG, Moon YM, Jhun JY, et al. p53 controls autoimmune arthritis via STAT-mediated regulation of the Th17 cell/Treg cell balance in mice. Arthritis Rheum 2012; 65: 949-59.
23. Park JS, Kwok SK, Lim MA, Oh HJ, Kim EK, Jhun JY, et al. TWEAK promotes osteoclastogenesis in rheumatoid arthritis. Am J Pathol 2013; 183: 857-67.
24. Park JS, Park MK, Oh HJ, Woo YJ, Lim MA, Lee JH, et al. Grape-seed proanthocyanidin extract as suppressors of bone destruction in inflammatory autoimmune arthritis. PLoS One 2012; 7: e51377.
25. Zhang L, Zhao Y,. The regulation of Foxp3 expression in regulatory CD4(+)CD25(+)T cells: multiple pathways on the road. J Cell Physiol 2007; 211: 590-7.
26. Burchill MA, Yang J, Vogtenhuber C, Blazar BR, Farrar MA,. IL-2 receptor beta-dependent STAT5 activation is required for the development of Foxp3+ regulatory T cells. J Immunol 2007; 178: 280-90.
27. Kwok SK, Park MK, Cho ML, Oh HJ, Park EM, Lee DG, et al. Retinoic acid attenuates rheumatoid inflammation in mice. J Immunol 2012; 189: 1062-71.
28. Lorenzo J, Horowitz M, Choi Y,. Osteoimmunology: interactions of the bone and immune system. Endocr Rev 2008; 29: 403-40.
29. Lee SH, Kim TS, Choi Y, Lorenzo J,. Osteoimmunology: cytokines and the skeletal system. BMB Rep 2008; 41: 495-510.
30. Sakaguchi S,. Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 2004; 22: 531-62.
31. Sakaguchi S, Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T,. Regulatory T cells: how do they suppress immune responses? Int Immunol 2009; 21: 1105-11.
32. Gaffen SL,. The role of interleukin-17 in the pathogenesis of rheumatoid arthritis. Curr Rheumatol Rep 2009; 11: 365-70.
33. Peck A, Mellins ED,. Breaking old paradigms: Th17 cells in autoimmune arthritis. Clin Immunol 2009; 132: 295-304.
34. Durant L, Watford WT, Ramos HL, Laurence A, Vahedi G, Wei L, et al. Diverse targets of the transcription factor STAT3 contribute to T cell pathogenicity and homeostasis. Immunity 2010; 32: 605-15.
35. Harris TJ, Grosso JF, Yen HR, Xin H, Kortylewski M, Albesiano E, et al. Cutting edge: an in vivo requirement for STAT3 signaling in TH17 development and TH17-dependent autoimmunity. J Immunol 2007; 179: 4313-7.
36. Yang XP, Ghoreschi K, Steward-Tharp SM, Rodriguez-Canales J, Zhu J, Grainger JR, et al. Opposing regulation of the locus encoding IL-17 through direct, reciprocal actions of STAT3 and STAT5. Nat Immunol 2011; 12: 247-54.
37. Notley CA, Ehrenstein MR,. The yin and yang of regulatory T cells and inflammation in RA. Nat Rev Rheumatol 2010; 6: 572-7.
38. Simmons DL,. Targeting kinases: a new approach to treating inflammatory rheumatic diseases. Curr Opin Pharmacol 2013; 13: 426-34.
39. Traynor K,. FDA approves tofacitinib for rheumatoid arthritis. Am J Health Syst Pharm 2012; 69: 2120.
40. Tanaka Y, Maeshima K, Yamaoka K,. In vitro and in vivo analysis of a JAK inhibitor in rheumatoid arthritis. Ann Rheum Dis 2012; 71 Suppl 2: 70-4.
41. Hulsmans HM, Jacobs JW, van der Heijde DM, van Albada-Kuipers GA, Schenk Y, Bijlsma JW,. The course of radiologic damage during the first six years of rheumatoid arthritis. Arthritis Rheum 2000; 43: 1927-40.
42. Lindqvist E, Jonsson K, Saxne T, Eberhardt K,. Course of radiographic damage over 10 years in a cohort with early rheumatoid arthritis. Ann Rheum Dis 2003; 62: 611-6.
43. Lindqvist E, Saxne T, Geborek P, Eberhardt K,. Ten year outcome in a cohort of patients with early rheumatoid arthritis: health status, disease process, and damage. Ann Rheum Dis 2002; 61: 1055-9.
44. Lipsky PE, van der Heijde DM, St.Clair EW, Furst DE, Breedveld FC, Kalden JR, et al. Infliximab and methotrexate in the treatment of rheumatoid arthritis: Anti-Tumor Necrosis Factor Trial in Rheumatoid Arthritis with Concomitant Therapy study group. N Engl J Med 2000; 343: 1594-602.
45. Klareskog L, van der Heijde D, de Jager JP, Gough A, Kalden J, Malaise M, et al. Therapeutic effect of the combination of etanercept and methotrexate compared with each treatment alone in patients with rheumatoid arthritis: double-blind randomised controlled trial. Lancet 2004; 363: 675-81.
46. Breedveld FC, Weisman MH, Kavanaugh AF, Cohen SB, Pavelka K, van Vollenhoven R, et al. The PREMIER study: a multicenter, randomized, double-blind clinical trial of combination therapy with adalimumab plus methotrexate versus methotrexate alone or adalimumab alone in patients with early, aggressive rheumatoid arthritis who had not had previous methotrexate treatment. Arthritis Rheum 2006; 54: 26-37.
47. O'Brien CA, Gubrij I, Lin SC, Saylors RL, Manolagas SC,. STAT3 activation in stromal/osteoblastic cells is required for induction of the receptor activator of NF-kappaB ligand and stimulation of osteoclastogenesis by gp130-utilizing cytokines or interleukin-1 but not 1,25-dihydroxyvitamin D3 or parathyroid hormone. J Biol Chem 1999; 274: 19301-8.
48. Chung CD, Liao J, Liu B, Rao X, Jay P, Berta P, et al. Specific inhibition of Stat3 signal transduction by PIAS3. Science 1997; 278: 1803-5.
49. Kim K, Lee J, Kim JH, Jin HM, Zhou B, Lee SY, et al. Protein inhibitor of activated STAT 3 modulates osteoclastogenesis by down-regulation of NFATc1 and osteoclast-associated receptor. J Immunol 2007; 178: 5588-94.