Protective role of JAK/STAT signaling against renal fibrosis in mice with unilateral ureteral obstruction

Clinical Immunology

Volumn 150, Issue 1, 2014, Pages 78-87

  Koike, Kiyomi ^a   Ueda, Seiji ^a   Yamagishi, Sho ichi ^a   Yasukawa, Hideo ^a   Kaida, Yusuke ^a   Yokoro, Miyuki ^a   Fukami, Kei ^a   Yoshimura, Akihiko ^b   Okuda, Seiya ^a  

^a KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

JAK; MMP 2; Renal fibrosis; SOCS; STAT; UUO

Indexed keywords

BETA1 INTERFERON; COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 3; COLLAGEN TYPE 4; GELATINASE A; INTERLEUKIN 10; INTERLEUKIN 27; JANUS KINASE; MESSENGER RNA; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; IMMUNOHISTOCHEMISTRY; KIDNEY FIBROSIS; KIDNEY PROXIMAL TUBULE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; URETER OBSTRUCTION; WESTERN BLOTTING;

JAK; MMP-2; RENAL FIBROSIS; SOCS; STAT; UUO;

ANIMALS; CELLS, CULTURED; COLLAGEN; CYTOKINES; FEMALE; FIBROSIS; HUMANS; JANUS KINASES; KIDNEY; KIDNEY DISEASES; KIDNEY TUBULES, PROXIMAL; MATRIX METALLOPROTEINASE 2; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; PYRIDINES; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TUMOR NECROSIS FACTOR-ALPHA; URETERAL OBSTRUCTION;

EID: 84890037681     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2013.11.003     Document Type: Article

References (39)

1. Liu Y. Cellular and molecular mechanisms of renal fibrosis. Nat. Rev. Nephrol. 2011, 7:684-696.
2. Hirschberg R. Wound healing in the kidney: complex interactions in renal interstitial fibrogenesis. J. Am. Soc. Nephrol. 2005, 16:9-11.
3. Lee S.B., Kalluri R. Mechanistic connection between inflammation and fibrosis. Kidney Int. Suppl. 2010, S22-S26.
4. Kisseleva T., Brenner D.A. Mechanisms of fibrogenesis. Exp. Biol. Med. (Maywood) 2008, 233:109-122.
5. Chuang P.Y., He J.C. JAK/STAT signaling in renal diseases. Kidney Int. 2010, 78:231-234.
6. O'Shea J.J., Murray P.J. Cytokine signaling modules in inflammatory responses. Immunity 2008, 28:477-487.
7. O'Shea J.J., Gadina M., Schreiber R.D. Cytokine signaling in 2002: new surprises in the Jak/Stat pathway. Cell 2002, 109:S121-S131. (Suppl.).
8. Yoshimura A., Naka T., Kubo M. SOCS proteins, cytokine signalling and immune regulation. Nat. Rev. Immunol. 2007, 7:454-465.
9. Yasukawa H., Sasaki A., Yoshimura A. Negative regulation of cytokine signaling pathways. Annu. Rev. Immunol. 2000, 18:143-164.
10. O'Sullivan L.A., Liongue C., Lewis R.S., Stephenson S.E., Ward A.C. Cytokine receptor signaling through the Jak-Stat-Socs pathway in disease. Mol. Immunol. 2007, 44:2497-2506.
11. Ortiz-Muñoz G., Lopez-Parra V., Lopez-Franco O., Fernandez-Vizarra P., Mallavia B., Flores C., Sanz A., Blanco J., Mezzano S., Ortiz A., Egido J., Gomez-Guerrero C. Suppressors of cytokine signaling abrogate diabetic nephropathy. J. Am. Soc. Nephrol. 2010, 21:763-772.
12. Pang M., Ma L., Gong R., Tolbert E., Mao H., Ponnusamy M., Chin Y.E., Yan H., Dworkin L.D., Zhuang S. A novel STAT3 inhibitor, S3I-201, attenuates renal interstitial fibroblast activation and interstitial fibrosis in obstructive nephropathy. Kidney Int. 2010, 78:257-268.
13. Wang S., Yang N., Zhang L., Huang B., Tan H., Liang Y., Li Y., Yu X. Jak/STAT signaling is involved in the inflammatory infiltration of the kidneys in MRL/lpr mice. Lupus 2010, 19:1171-1180.
14. Marine J., McKay C., Wang D., Topham D., Parganas E., Nakajima H., Pendeville H., Yasukawa H., Sasaki A., Yoshimura A., Ihle J. SOCS3 is essential in the regulation of fetal liver erythropoiesis. Cell 1999, 98:617-627.
15. Yajima T., Yasukawa H., Jeon E.S., Xiong D., Dorner A., Iwatate M., Nara M., Zhou H., Summers-Torres D., Hoshijima M., Chien K.R., Yoshimura A., Knowlton K.U. Innate defense mechanism against virus infection within the cardiac myocyte requiring gp130-STAT3 signaling. Circulation 2006, 114:2364-2373.
16. Matsunaga Y., Inoue H., Fukuyama S., Yoshida H., Moriwaki A., Matsumoto T., Matsumoto K., Asai Y., Kubo M., Yoshimura A., Nakanishi Y. Effects of a Janus kinase inhibitor, pyridone 6, on airway responses in a murine model of asthma. Biochem. Biophys. Res. Commun. 2011, 404:261-267.
17. Matsumoto Y., Ueda S., Yamagishi S., Matsuguma K., Shibata R., Fukami K., Matsuoka H., Imaizumi T., Okuda S. Dimethylarginine dimethylaminohydrolase prevents progression of renal dysfunction by inhibiting loss of peritubular capillaries and tubulointerstitial fibrosis in a rat model of chronic kidney disease. J. Am. Soc. Nephrol. 2007, 18:1525-1533.
18. Middeldorp J., Kamphuis W., Sluijs J.A., Achoui D., Leenaars C.H., Feenstra M.G., van Tijn P., Fischer D.F., Berkers C., Ovaa H., Quinlan R.A., Hol E.M. Intermediate filament transcription in astrocytes is repressed by proteasome inhibition. FASEB J. 2009, 23:2710-2726.
19. Yan S.J., Blomme E.A. In situ zymography: a molecular pathology technique to localize endogenous protease activity in tissue sections. Vet. Pathol. 2003, 40:227-236.
20. Rauch B.H., Bretschneider E., Braun M., Schrör K. Factor Xa releases matrix metalloproteinase-2 (MMP-2) from human vascular smooth muscle cells and stimulates the conversion of pro-MMP-2 to MMP-2: role of MMP-2 in factor Xa-induced DNA synthesis and matrix invasion. Circ. Res. 2002, 90:1122-1127.
21. Takamiya Y., Fukami K., Yamagishi S., Kaida Y., Nakayama Y., Obara N., Iwatani R., Ando R., Koike K., Matsui T., Nishino Y., Ueda S., Cooper M.E., Okuda S. Experimental diabetic nephropathy is accelerated in matrix metalloproteinase-2 knockout mice. Nephrol. Dial. Transplant. 2013, 28:55-62.
22. Du X., Shimizu A., Masuda Y., Kuwahara N., Arai T., Kataoka M., Uchiyama M., Kaneko T., Akimoto T., Iino Y., Fukuda Y. Involvement of matrix metalloproteinase-2 in the development of renal interstitial fibrosis in mouse obstructive nephropathy. Lab. Invest. 2012, 92:1149-1160.
23. Kuratsune M., Masaki T., Hirai T., Kiribayashi K., Yokoyama Y., Arakawa T., Yorioka N., Kohno N. Signal transducer and activator of transcription 3 involvement in the development of renal interstitial fibrosis after unilateral ureteral obstruction. Nephrology (Carlton) 2007, 12:565-571.
24. Kovalovich K., DeAngelis R.A., Li W., Furth E.E., Ciliberto G., Taub R. Increased toxin-induced liver injury and fibrosis in interleukin-6-deficient mice. Hepatology 2000, 31:149-159.
25. Plum W., Tschaharganeh D.F., Kroy D.C., Corsten E., Erschfeld S., Dierssen U., Wasmuth H., Trautwein C., Streetz K.L. Lack of glycoprotein 130/signal transducer and activator of transcription 3-mediated signaling in hepatocytes enhances chronic liver injury and fibrosis progression in a model of sclerosing cholangitis. Am. J. Pathol. 2010, 176:2236-2246.
26. Yoshino J., Monkawa T., Tsuji M., Hayashi M., Saruta T. Leukemia inhibitory factor is involved in tubular regeneration after experimental acute renal failure. J. Am. Soc. Nephrol. 2003, 14:3090-3101.
27. Yarilina A., Park-Min K.H., Antoniv T., Hu X., Ivashkiv L.B. TNF activates an IRF1-dependent autocrine loop leading to sustained expression of chemokines and STAT1-dependent type I interferon-response genes. Nat. Immunol. 2008, 9:378-387.
28. Rosengren S., Corr M., Firestein G.S., Boyle D.L. The JAK inhibitor CP-690,550 (tofacitinib) inhibits TNF-induced chemokine expression in fibroblast-like synoviocytes: autocrine role of type I interferon. Ann. Rheum. Dis. 2012, 71:440-447.
29. Kalliolias G.D., Gordon R.A., Ivashkiv L.B. Suppression of TNF-α and IL-1 signaling identifies a mechanism of homeostatic regulation of macrophages by IL-27. J. Immunol. 2010, 185:7047-7056.
30. Lee A., Qiao Y., Grigoriev G., Chen J., Park-Min K.H., Park S.H., Ivashkiv L.B., Kalliolias G.D. Tumor necrosis factor α induces sustained signaling and a prolonged and unremitting inflammatory response in rheumatoid arthritis synovial fibroblasts. Arthritis Rheum. 2013, 65:928-938.
31. Boisson B., Laplantine E., Prando C., Giliani S., Israelsson E., Xu Z., Abhyankar A., Israël L., Trevejo-Nunez G., Bogunovic D., Cepika A.M., MacDuff D., Chrabieh M., Hubeau M., Bajolle F., Debré M., Mazzolari E., Vairo D., Agou F., Virgin H.W., Bossuyt X., Rambaud C., Facchetti F., Bonnet D., Quartier P., Fournet J.C., Pascual V., Chaussabel D., Notarangelo L.D., Puel A., Israël A., Casanova J.L., Picard C. Immunodeficiency, autoinflammation and amylopectinosis in humans with inherited HOIL-1 and LUBAC deficiency. Nat. Immunol. 2012, 13:1178-1186.
32. Fujita M., Shannon J.M., Morikawa O., Gauldie J., Hara N., Mason R.J. Overexpression of tumor necrosis factor-alpha diminishes pulmonary fibrosis induced by bleomycin or transforming growth factor-beta. Am. J. Respir. Cell Mol. Biol. 2003, 29:669-676.
33. Liu J.Y., Sime P.J., Wu T., Warshamana G.S., Pociask D., Tsai S.Y., Brody A.R. Transforming growth factor-beta(1) overexpression in tumor necrosis factor-alpha receptor knockout mice induces fibroproliferative lung disease. Am. J. Respir. Cell Mol. Biol. 2001, 25:3-7.
34. Morimoto Y., Gai Z., Tanishima H., Kawakatsu M., Itoh S., Hatamura I., Muragaki Y. TNF-alpha deficiency accelerates renal tubular interstitial fibrosis in the late stage of ureteral obstruction. Exp. Mol. Pathol. 2008, 85:207-213.
35. Verjee L.S., Verhoekx J.S., Chan J.K., Krausgruber T., Nicolaidou V., Izadi D., Davidson D., Feldmann M., Midwood K.S., Nanchahal J. Unraveling the signaling pathways promoting fibrosis in Dupuytren's disease reveals TNF as a therapeutic target. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E928-E937.
36. Ortiz L.A., Lasky J., Hamilton R.F., Holian A., Hoyle G.W., Banks W., Peschon J.J., Brody A.R., Lungarella G., Friedman M. Expression of TNF and the necessity of TNF receptors in bleomycin-induced lung injury in mice. Exp. Lung Res. 1998, 24:721-743.
37. Piguet P.F., Vesin C. Treatment by human recombinant soluble TNF receptor of pulmonary fibrosis induced by bleomycin or silica in mice. Eur. Respir. J. 1994, 7:515-518.
38. Nishida M., Okumura Y., Ozawa S., Shiraishi I., Itoi T., Hamaoka K. MMP-2 inhibition reduces renal macrophage infiltration with increased fibrosis in UUO. Biochem. Biophys. Res. Commun. 2007, 354:133-139.
39. Cai G., Zhang X., Hong Q., Shao F., Shang X., Fu B., Feng Z., Lin H., Wang J., Shi S., Yin Z., Chen X. Tissue inhibitor of metalloproteinase-1 exacerbated renal interstitial fibrosis through enhancing inflammation. Nephrol. Dial. Transplant. 2008, 23:1861-1875.