IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages

Nature Immunology

Volumn 4, Issue 6, 2003, Pages 551-556

  Yasukawa, Hideo ^a,e   Ohishi, Masanobu ^b   Mori, Hiroyuki ^b   Murakami, Masaaki ^c   Chinen, Takatoshi ^b   Aki, Daisuke ^b   Hanada, Toshikatsu ^b   Takeda, Kiyoshi ^d   Akira, Shizuo ^d   Hoshijima, Masahiko ^a   Hirano, Toshio ^c   Chien, Kenneth R ^a   Yoshimura, Akihiko ^b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b KYUSHU UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d OSAKA UNIVERSITY   (Japan)

^e KURUME UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; REGULATOR PROTEIN; STAT PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; BINDING SITE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE MUTATION; IMMUNOREGULATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; DNA-BINDING PROTEINS; FEMALE; IMMUNOBLOTTING; INTERLEUKIN-10; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MACROPHAGES, PERITONEAL; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEINS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0037600741     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/ni938     Document Type: Article

References (37)

1. Ishihara, K. & Hirano, T. IL-6 in autoimmune disease and chronic inflammatory proliferative disease. Cytokine Growth Factor Rev. 13, 357-368 (2002).
2. Atreya, R. et al. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn disease and experimental colitis in vivo. Nat. Med. 6, 583-588 (2000).
3. Alonzi, T. et al. Interleukin 6 is required for the development of collagen-induced arthritis. J. Exp. Med. 187, 461-468 (1998).
4. Moore, K.W., de Waal Malefyt, R., Coffman, R.L. & O'Garra, A. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19, 683-765 (2001).
5. Huber, T.S. et al. Anticytokine therapies for acute inflammation and the systemic inflammatory response syndrome: IL-10 and ischemia/reperfusion injury as a new paradigm. Shock 13, 425-434 (2000).
6. Hirano, T., Ishihara, K. & Hibi, M. Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors. Oncogene 19, 2548-2556 (2000).
7. Riley, J.K., Takeda, K., Akira, S. & Schreiber, R.D. Interleukin-10 receptor signaling through the JAK-STAT pathway. Requirement for two distinct receptor-derived signals for anti-inflammatory action. J. Biol. Chem. 274, 16513-16521 (1999).
8. Weber-Nordt, R.M. et al. Stat3 recruitment by two distinct ligand-induced, tyrosine-phosphorylated docking sites in the interleukin-10 receptor intracellular domain. J. Biol. Chem. 271, 27954-27961 (1996).
9. 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).
10. Yasukawa, H, Sasaki, A. & Yoshimura A. Negative regulation of cytokine signaling pathways. Annu. Rev. Immunol. 18, 143-164 (2000).
11. 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).
12. 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).
13. Bode, J.G., et al. LPS and TNFα induce SOCS3 mRNA and inhibit IL-6-induced activation of STAT3 in macrophages. FEBS Lett. 463, 365-370 (1999).
14. Lehmann, U. et al. SHP2 and SOCS3 contribute to Tyr-759-dependent attenuation of interleukin-6 signaling through gp130. J. Biol. Chem. 278, 661-671 (2003).
15. Nicholson, S.E. et al. Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130. Proc. Natl. Acad. Sci. USA. 97, 6493-6498 (2000).
16. Niemand, C. et al. Activation of STAT3 by IL-6 and IL-10 in primary human macrophages is differentially modulated by suppressor of cytokine signaling 3. J. Immunol. 170, 3263-3272 (2003).
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. Roberts, A.W. et al. Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3. Proc. Natl. Acad. Sci. USA. 98, 9324-9329 (2001).
19. Clausen, B.E., Burkhardt, C., Reith, W., Renkawitz, R. & Förster, I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8, 265-277(1999).
20. Sasaki, A. et al. The N-terminal truncated isoform of SOCS3 translated from an alternative initiation AUG codon under stress conditions is stable due to the lack of a major ubiquitination site, Lys-6. J. Biol. Chem. 278, 2432-2436 (2003).
21. Atsumi, T. et al. A point mutation of Tyr-759 in interleukin 6 family cytokine receptor subunit gp130 causes autoimmune arthritis. J. Exp. Med.196, 979-990 (2002).
22. Lehmann, U. etal. SHP2 and SOCS3 contribute to Tyr-759-dependent attenuation of interleukin-6 signaling through gp130. J. Blol. Chem. 278, 661-671 (2003).
23. Lee, T.S. & Chau, L.Y. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat. Med. 8, 240-246 (2002).
24. Akira, S., Takeda, K. & Kaisho, T. Toll-like receptor: critical proteins linking innate and acquired immunity. Nat. Immunol. 2, 675-680 (2001).
25. Medzhitov, R. & Janeway, C. Jr. Innate immunity. N. Engl. J. Med. 343, 338-344 (2000).
26. Berlato, C. et al. Involvement of suppressor of cytokine signaling-3 as a mediator of the inhibitory effects of IL-10 on lipopolysaccharide-induced macrophage activation. J. Immunol. 168, 6404-64011 (2002).
27. Shouda, T. et al. Induction of the cytokine signal regulator SOCS3/CIS3 as a therapeutic strategy for treating inflammatory arthritis. J. Clin. Invest. 108, 1781-1788 (2001).
28. Suzuki, R. et al. CIS3 and JAB have different regulatory roles in interleukin-6 mediated differentiation and STAT3 activation in M1 leukemia cells. Oncogene 17, 2271-2278 (1998).
29. Masuhara, M. et al. Cloning and characterization of novel CIS family genes. Biochem. Biophys. Res. Commun. 239, 439-446 (1997).
30. Nakajima, K. et al. A central role for Stat3 in L-6-induced regulation of growth and differentiation in M1 leukemia cells. EMBO J. 15, 3651-3658 (1996).
31. Traverse, S., Gomez, N., Paterson, H., Marshall, C. & Cohen, P. Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Comparison of the effects of nerve growth factor and epidermal growth factor. Biochem. J. 288, 351-355 (1992).
32. Chen, J. et al. Ventricular muscle-restricted targeting of the RXRα gene reveals a non-cell-autonomous requirement in cardiac chamber morphogenesis. Development 126, 4223-4234 (1998).
33. Kinjyo, I. et al. SOCS1/JAB is a negative regulator of LPS-induced macrophage activation. Immunity 17, 583-591 (2002).
34. Nagai, Y. et al. Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat. Immunol. 3, 667-672 (2002).
35. Yamanaka, Y., Nakajima, K., Fukada, T., Hibi, M. & Hirano, T. Differentiation and growth arrest signals are generated through the cytoplasmic region of gp130 that is essential for Stat3 activation. EMBO J. 15, 1557-1565 (1996).
36. Yokouchi, M. et al. Cloning and characterization of APS, an adaptor molecule containing PH and SH2 domains that is tyrosine phosphorylated upon B-cell receptor stimulation. Oncogene 15, 7-15 (1997).
37. Sasaki, A. et al. CIS3/SOCS3 suppresses erythropoietin signaling by binding the EPO receptor and JAK2. J. Biol. Chem. 275, 29338-29347 (2000).