SOCS3 negatively regulates IL-6 signaling in vivo

Nature Immunology

Volumn 4, Issue 6, 2003, Pages 540-545

  Croker, Ben A ^a   Krebs, Danielle L ^a   Zhang, Jian Guo ^a   Wormald, Sam ^a   Willson, Tracy A ^a   Stanley, Edouard G ^b   Robb, Lorraine ^a   Greenhalgh, Christopher J ^a   Förster, Irmgard ^c   Clausen, Björn E ^d   Nicola, Nicos A ^a   Metcalf, Donald ^a   Hilton, Douglas J ^a   Roberts, Andrew W ^a   Alexander, Warren S ^a  

^a Department of Civil and Environmental Engineering   (Australia)

^b MONASH MEDICAL CENTRE   (Australia)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GENE PRODUCT; INTERLEUKIN 6; REGULATOR PROTEIN; STAT1 PROTEIN; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; SUPPRESSOR OF CYTOKINE SIGNALING 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; DNA MICROARRAY; GENE EXPRESSION; GENE TARGETING; IMMUNOREGULATION; IN VIVO STUDY; LIVER; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; CARRIER PROTEINS; DNA-BINDING PROTEINS; FEMALE; INTERFERON TYPE II; INTERLEUKIN-10; INTERLEUKIN-6; LIVER; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PROTEINS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 0037938816     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/ni931     Document Type: Article

References (38)

1. Van Snick, J. Interleukin-6: an overview. Annu. Rev. Immunol. 8, 253-278 (1990).
2. Bernad, A. et al. Interleukin-6 is required in vivo for the regulation of stem cells and committed progenitors of the hematopoietic system. Immunity 1, 725-731 (1994).
3. Ramsay, A.J. et al. The role of interleukin-6 in mucosal IgA antibody responses in vivo. Science 264, 561-563 (1994).
4. Fattori, E. et al. Defective inflammatory response in interleukin 6-deficient mice. J. Exp. Med. 180, 1243-1250 (1994).
5. Hilbert, D.M., Kopf, M., Mock, B.A., Kohler, G. & Rudikoff, S. Interleukin 6 is essential for in vivo development of B lineage neoplasms. J. Exp. Med. 182, 243-248 (1995).
6. Kopf, M. et al. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368, 339-342 (1994).
7. Taga, T. et al. Interleukin-6 triggers the association of its receptor with a possible Signal transducer, gp130. Cell 58, 573-581 (1989).
8. O'Shea, J.J., Gadina, M. & Schreiber, R.D. Cytokine signaling in 2002: new surprises in the Jak/Stat pathway. Cell 109 (suppl.), S121-SI31 (2002).
9. Hemmann, U. et al. Differential activation of acute phase response factor/Stat3 and Stat1 via the cytoplasmic domain of the interleukin 6 signal transducer gp130. 11. Src homology SH2 domains define the specificity of stat factor activation. J. Biol. Chem. 271, 12999-13007 (1996).
10. Alonzi, T. et al. Essential role of STAT3 in the control of the acute-phase response as revealed by inducible gene inactivation in the liver. Mol. Cell. Biol. 21, 1621-1632 (2001).
11. Alexander, W.S. Suppressors of cytokine signalling (SOCS) in the immune system. Nat. Rev, Immunol. 2, 410-416 (2002).
12. Starr, R. et al. A family of cytokine-inducible inhibitors of signalling. Nature 387, 917-921 (1997).
13. Alexander, W.S. et al. SOCS1 is a critical inhibitor of interferon-γ signaling and prevents the potentially fatal neonatal actions of this cytokine. Cell 98, 597-608 (1999).
14. Marine, J.C. et al. SOCS1 deficiency causes a lymphocyte-dependent perinatal lethality. Cell 98, 609-616 (1999).
15. Metcalf, D. et al. Gigantism in mice lacking suppressor of cytokine signalling-2. Nature 405, 1069-1073 (2000).
16. Roberts, A.W. et al. Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3. Proc. Natl. Acad. Sci. 98, 9324-9329 (2001).
17. Takahashi, Y. et al. SOCS3: an essential regulator of LIF receptor signaling in trophoblast giant cell differentiation. EMBO J. 22, 372-384 (2003).
18. Marine, J.C. et al. SOCS3 is essential in the regulation of fetal liver erythropoiesis. Cell 98, 617-627 (1999).
19. Schwenk, F., Baron, U. & Rajewsky, K. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 23, 5080-5081 (1995).
20. Yakar, S. et al. Normal growth and development in the absence of hepatic insulin-like growth factor I. Proc. Natl. Acad. Sci. 96, 7324-7329 (1999).
21. Clausen, B.E., Burkhardt, C., Reith, W., Renkawitz, R. & Forster, I. Conditional gene targeting in macrophages and granulocytes using LysM-cre mice. Transgenic Res. 8, 265-277 (1999).
22. Soriano, P, Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71 (1999).
23. Campbell, J.S. et al. Expression of suppressors of cytokine signaling during liver regeneration. J. Clin. Invest. 107, 1285-1292 (2001).
24. Hong, F. et al. Opposing roles of STAT1 and STAT3 in T cell-mediated hepatitis: regulation by SOCS. J. Clin. Invest. 110, 1503-1513 (2002).
25. Stoiber, D. et al. Lipopolysaccharide induces in macrophages the synthesis of the suppressor of cytokine signaling 3 and suppresses signal transduction in response to the activating factor IFN-γ. J. Immunol. 163, 2640-2647 (1999).
26. Nicholson, S.E. et al. Mutational analyses of the SOCS proteins suggest a dual domain requirement but distinct mechanisms for inhibition of LIF and IL-6 signal transduction. EMBO J. 18, 375-385 (1999).
27. Song, M.M. & Shuai, K. The suppressor of cytokine signaling (SOCS) 1 and SOCS3 but not SOCS2 proteins inhibit interferon-mediated antiviral and antiproliferative activities. J. Biol. Chem. 273, 35056-35062 (1998).
28. Brysha, M. et al. Suppressor of cytokine signaling-1 attenuates the duration of interferon-γ signal transduction in vitro and in vivo. J. Biol. Chem. 276, 22086-22089 (2001).
29. Takeda, K. et al. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 10, 39-49 (1999).
30. waf-1 and arrests macrophage cell cycle, preventing induction of apoptosis. Immunity 11, 103-113 (1999).
31. Cascio, S. & Zaret, K.S. Hepatocyte differentiation initiates during endodermal-mesenchymal interactions prior to liver formation. Development 113, 217-225 (1991).
32. Cressman, D.E. et al. Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science 274, 1379-1383 (1996).
33. Costa-Pereira, A.P. et al. Mutational switch of an IL-6 response to an interferon-γ-like response. Proc. Natl. Acad. Sci. 99, 8043-8047 (2002).
34. Lee, C. et al. STAT3 is a negative regulator of granulopoiesis but is not required for GCSF-dependent differentiation. Immunity 17, 63-72 (2002).
35. Lang, R. et al. SOCS3 regulates the plasticity of gp130 signaling. Nat. Immunol. advance online publication, 18 May 2003 (doi:10.1038/ni932).
36. Finbloom, D.S. & Winestock, K.D. IL-10 inducesthe tyrosine phosphorylation of tyk2 and Jak1 and the differential assembly of STAT1α and STAT3 complexes in human T cells and monocytes. J. Immunol. 155, 1079-1090 (1995). 1
37. Cassatella, M.A. et al. Interleukin-10 (IL-10) selectively enhances CIS3/SOCS3 mRNA expression in human neutrophils: evidence for an IL-10-induced pathway that is independent of STAT protein activation. Blood 94, 2880-2889 (1999).
38. + T lymphocytes but fail to promote survival. Eur. J. Immunol. 28, 221-236