Signal transducer and activator of transcription (STAT) 3 inhibition delays the onset of lupus nephritis in MRL/lpr mice

Clinical Immunology

Volumn 158, Issue 2, 2015, Pages 221-230

  Edwards, Lindsay J ^a,b   Mizui, Masayuki ^a,b   Kyttaris, Vasileios ^a,b  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

MRL lpr; Murine lupus; SLE; STAT3; T cells

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CYTOKINE; DOUBLE STRANDED DNA ANTIBODY; IMMUNOGLOBULIN G; IMMUNOMODULATING AGENT; STAT3 PROTEIN; STATTIC; UNCLASSIFIED DRUG; STAT3 PROTEIN, HUMAN; SULFOXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; DRUG TARGETING; HELPER CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUPUS ERYTHEMATOSUS NEPHRITIS; LYMPHADENOPATHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEINURIA; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; INFLAMMATION; KIDNEY; METABOLISM; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; PATHOLOGY;

ANIMALS; CYCLIC S-OXIDES; CYTOKINES; GENE EXPRESSION REGULATION; IMMUNOGLOBULIN G; INFLAMMATION; KIDNEY; LUPUS NEPHRITIS; MICE; MICE, INBRED MRL LPR; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES;

EID: 84928714142     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2015.04.004     Document Type: Article

References (34)

1. Mak A., Kow N.Y. The pathology of T cells in systemic lupus erythematosus. J. Immunol. Res. 2014, 2014:419029. (PubMed PMID: 24864268. Pubmed Central PMCID: 4017881).
2. Furie R., Petri M., Zamani O., Cervera R., Wallace D.J., Tegzova D., et al. A phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus. Arthritis Rheum. Dec 2011, 63(12):3918-3930. (PubMed PMID: 22127708).
3. Markopoulou A., Kyttaris V.C. Small molecules in the treatment of systemic lupus erythematosus. Clin. Immunol. Sep 2013, 148(3):359-368. (PubMed PMID: 23158694. Pubmed Central PMCID: 3587286).
4. Leonard W.J., O'Shea J.J. Jaks and STATs: biological implications. Annu. Rev. Immunol. 1998, 16:293-322. (PubMed PMID: 9597132).
5. Harada T., Kyttaris V., Li Y., Juang Y.T., Wang Y., Tsokos G.C. Increased expression of STAT3 in SLE T cells contributes to enhanced chemokine-mediated cell migration. Autoimmunity Feb 2007, 40(1):1-8. (PubMed PMID: 17364491).
6. Nakou M., Bertsias G., Stagakis I., Centola M., Tassiulas I., Hatziapostolou M., et al. Gene network analysis of bone marrow mononuclear cells reveals activation of multiple kinase pathways in human systemic lupus erythematosus. PLoS One 2010, 5(10):e13351. (PubMed PMID: 20976278. Pubmed Central PMCID: 2954787).
7. Nurieva R.I., Chung Y., Hwang D., Yang X.O., Kang H.S., Ma L., et al. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity Jul 18 2008, 29(1):138-149. (PubMed PMID: 18599325. Pubmed Central PMCID: 2556461).
8. Konforte D., Paige C.J. Identification of cellular intermediates and molecular pathways induced by IL-21 in human B cells. J. Immunol. Dec 15 2006, 177(12):8381-8392. (PubMed PMID: 17142735).
9. Zeng R., Spolski R., Casas E., Zhu W., Levy D.E., Leonard W.J. The molecular basis of IL-21-mediated proliferation. Blood May 15 2007, 109(10):4135-4142. (PubMed PMID: 17234735. Pubmed Central PMCID: 1885510).
10. Crispin J.C., Oukka M., Bayliss G., Cohen R.A., Van Beek C.A., Stillman I.E., et al. Expanded double negative T cells in patients with systemic lupus erythematosus produce IL-17 and infiltrate the kidneys. J. Immunol. Dec 15 2008, 181(12):8761-8766. (PubMed PMID: 19050297. Pubmed Central PMCID: 2596652).
11. Zhang Z., Kyttaris V.C., Tsokos G.C. The role of IL-23/IL-17 axis in lupus nephritis. J. Immunol. Sep 1 2009, 183(5):3160-3169. (PubMed PMID: 19657089. Pubmed Central PMCID: 2766304).
12. Apostolidis S.A., Crispin J.C., Tsokos G.C. IL-17-producing T cells in lupus nephritis. Lupus Feb 2011, 20(2):120-124. (PubMed PMID: 21303828).
13. Wen Z., Xu L., Xu W., Yin Z., Gao X., Xiong S. Interleukin-17 expression positively correlates with disease severity of lupus nephritis by increasing anti-double-stranded DNA antibody production in a lupus model induced by activated lymphocyte derived DNA. PLoS One 2013, 8(3):e58161. (PubMed PMID: 23472149. Pubmed Central PMCID: 3589375).
14. Harris T.J., Grosso J.F., Yen H.R., 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. Oct 1 2007, 179(7):4313-4317. (PubMed PMID: 17878325).
15. Liu X., Lee Y.S., Yu C.R., Egwuagu C.E. Loss of STAT3 in CD4+ T cells prevents development of experimental autoimmune diseases. J. Immunol. May 1 2008, 180(9):6070-6076. (PubMed PMID: 18424728. Pubmed Central PMCID: 2435016).
16. Vila-Coro A.J., Rodriguez-Frade J.M., Martin De Ana A., Moreno-Ortiz M.C., Martinez A.C., Mellado M. The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway. FASEB J. Oct 1999, 13(13):1699-1710. (PubMed PMID: 10506573).
17. Mellado M., Rodriguez-Frade J.M., Aragay A., del Real G., Martin A.M., Vila-Coro A.J., et al. The chemokine monocyte chemotactic protein 1 triggers Janus kinase 2 activation and tyrosine phosphorylation of the CCR2B receptor. J. Immunol. Jul 15 1998, 161(2):805-813. (PubMed PMID: 9670957).
18. Hochberg M.C. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. Sep 1997, 40(9):1725. (PubMed PMID: 9324032).
19. Schust J., Sperl B., Hollis A., Mayer T.U., Berg T. Stattic: a small-molecule inhibitor of STAT3 activation and dimerization. Chem. Biol. Nov 2006, 13(11):1235-1242. (PubMed PMID: 17114005).
20. Gerwien J., Nielsen M., Labuda T., Nissen M.H., Svejgaard A., Geisler C., et al. Cutting edge: TCR stimulation by antibody and bacterial superantigen induces Stat3 activation in human T cells. J. Immunol. Aug 15 1999, 163(4):1742-1745. (PubMed PMID: 10438903).
21. Linterman M.A., Rigby R.J., Wong R.K., Yu D., Brink R., Cannons J.L., et al. Follicular helper T cells are required for systemic autoimmunity. J. Exp. Med. Mar 16 2009, 206(3):561-576. (PubMed PMID: 19221396. Pubmed Central PMCID: 2699132).
22. Simpson N., Gatenby P.A., Wilson A., Malik S., Fulcher D.A., Tangye S.G., et al. Expansion of circulating T cells resembling follicular helper T cells is a fixed phenotype that identifies a subset of severe systemic lupus erythematosus. Arthritis Rheum. Jan 2010, 62(1):234-244. (PubMed PMID: 20039395).
23. Yang X.O., Panopoulos A.D., Nurieva R., Chang S.H., Wang D., Watowich S.S., et al. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J. Biol. Chem. Mar 30 2007, 282(13):9358-9363. (PubMed PMID: 17277312).
24. Milner J.D., Brenchley J.M., Laurence A., Freeman A.F., Hill B.J., Elias K.M., et al. Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature Apr 10 2008, 452(7188):773-776. (PubMed PMID: 18337720. Pubmed Central PMCID: 2864108).
25. Martin J.C., Baeten D.L., Josien R. Emerging role of IL-17 and Th17 cells in systemic lupus erythematosus. Clin. Immunol. May 23 2014, 154(1):1-12. (PubMed PMID: 24858580).
26. Patakas A., Benson R.A., Withers D.R., Conigliaro P., McInnes I.B., Brewer J.M., et al. Th17 effector cells support B cell responses outside of germinal centres. PLoS One 2012, 7(11):e49715. (PubMed PMID: 23166752. Pubmed Central PMCID: 3500323).
27. Hsu H.C., Yang P., Wang J., Wu Q., Myers R., Chen J., et al. Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat. Immunol. Feb 2008, 9(2):166-175. (PubMed PMID: 18157131).
28. Mitsdoerffer M., Lee Y., Jager A., Kim H.J., Korn T., Kolls J.K., et al. Proinflammatory T helper type 17 cells are effective B-cell helpers. Proc. Natl. Acad. Sci. U. S. A. Aug 10 2010, 107(32):14292-14297. (PubMed PMID: 20660725. Pubmed Central PMCID: 2922571).
29. Bleul C.C., Wu L., Hoxie J.A., Springer T.A., Mackay C.R. The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc. Natl. Acad. Sci. U. S. A. Mar 4 1997, 94(5):1925-1930. (PubMed PMID: 9050881. Pubmed Central PMCID: 20019).
30. Hori T., Sakaida H., Sato A., Nakajima T., Shida H., Yoshie O., et al. Detection and delineation of CXCR-4 (fusin) as an entry and fusion cofactor for T-tropic [correction of T cell-tropic] HIV-1 by three different monoclonal antibodies. J. Immunol. Jan 1 1998, 160(1):180-188. (PubMed PMID: 9551970).
31. Wang A., Fairhurst A.M., Tus K., Subramanian S., Liu Y., Lin F., et al. CXCR4/CXCL12 hyperexpression plays a pivotal role in the pathogenesis of lupus. J. Immunol. Apr 1 2009, 182(7):4448-4458. (PubMed PMID: 19299746. Pubmed Central PMCID: 2946082).
32. Wang A., Guilpain P., Chong B.F., Chouzenoux S., Guillevin L., Du Y., et al. Dysregulated expression of CXCR4/CXCL12 in subsets of patients with systemic lupus erythematosus. Arthritis Rheum. Nov 2010, 62(11):3436-3446. (PubMed PMID: 20722038).
33. Wu T., Qin X., Kurepa Z., Kumar K.R., Liu K., Kanta H., et al. Shared signaling networks active in B cells isolated from genetically distinct mouse models of lupus. J. Clin. Invest. Aug 2007, 117(8):2186-2196. (PubMed PMID: 17641780. Pubmed Central PMCID: 1913486).
34. Kyttaris V.C. Kinase inhibitors: a new class of antirheumatic drugs. Drug Des. Dev. Ther. 2012, 6:245-250. (PubMed PMID: 23055694. Pubmed Central PMCID: 3457674).