IL-6 promotes acute and chronic inflammatory disease in the absence of SOCS3

Immunology and Cell Biology

Volumn 90, Issue 1, 2012, Pages 124-129

  Croker, Ben A ^a,b   Kiu, Hiu ^b,c   Pellegrini, Marc ^b,c   Toe, Jesse ^c   Preston, Simon ^b   Metcalf, Donald ^b,c   O'Donnell, Joanne A ^b,c   Cengia, Louise H ^c   McArthur, Kate ^b,c   Nicola, Nicos A ^b,c   Alexander, Warren S ^b,c   Roberts, Andrew W ^b,c  

^a Institute of Medical Research   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

IL 1b; IL 6; SOCS3; suppressor of cytokine signalling 3

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ACUTE DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CHRONIC DISEASE; CONTROLLED STUDY; IMMUNE RESPONSE; IN VIVO STUDY; INFLAMMATION; LYMPH NODE CELL; LYMPHOCYTIC CHORIOMENINGITIS; MOUSE; NONHUMAN; PROTEIN FUNCTION; SPLEEN LYMPHOCYTE; SURVIVAL TIME; T LYMPHOCYTE;

ACUTE DISEASE; ANIMALS; APOPTOSIS; CD8-POSITIVE T-LYMPHOCYTES; CHRONIC DISEASE; CYTOKINES; FEMALE; FLOW CYTOMETRY; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; LYMPHOCYTES; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; SURVIVAL ANALYSIS;

LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MUS;

EID: 84855469919     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2011.29     Document Type: Article

References (35)

1. Liu F, Poursine-Laurent J, Wu HY, Link DC Interleukin-6 and the granulocyte colony-stimulating factor receptor are major independent regulators of granulopoiesis in vivo but are not required for lineage commitment or terminal differentiation. Blood 1997; 90: 2583-2590. (Pubitemid 27413467)
2. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006; 441: 235-238.
3. Cressman DE, Greenbaum LE, De Angelis RA, Ciliberto G, Furth EE, Poli V et al. Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science 1996; 274: 1379-1383. (Pubitemid 26391463)
4. Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, Kishimoto T et al. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 1994; 368: 339-342. (Pubitemid 24104268)
5. Pflegerl P, Vesely P, Hantusch B, Schlederer M, Zenz R, Janig E et al. Epidermal loss of Jun B leads to a SLE phenotype due to hyper IL-6 signaling. Proc Natl Acad Sci USA 2009; 106: 20423-20428.
6. Kishimoto T. Interleukin-6: from basic science to medicine\-40 years in immunology. Annu Rev Immunol 2005; 23: 1-21. (Pubitemid 40563163)
7. Eriksson U, Kurrer MO, Schmitz N, Marsch SC, Fontana A, Eugster HP et al. Inter-leukin-6-deficient mice resistdevelopment ofautoimmune myocarditis associated with impaired upregulation of complement C3. Circulation 2003; 107: 320-325. (Pubitemid 36135231)
8. Samoilova EB, Horton JL, Hilliard B, Liu TS, Chen Y. IL-6-deficient miceareresistantto experimental autoimmune encephalomyelitis: roles of IL-6 in the activation and differentiation of autoreactive Tcells. J Immunol 1998; 161: 6480-6486. (Pubitemid 28562184)
9. Ohshima S, Saeki Y, Mima T, Sasai M, Nishioka K, Nomura S et al. Interleukin 6 plays a keyrole inthedevelopmentofantigen-induced arthritis. Proc Natl Acad Sci USA 1998; 95: 8222-8226. (Pubitemid 28326094)
10. Alonzi T, Fattori E, Lazzaro D, Costa P, Probert L, Kollias G et al. Interleukin 6 is required for the development of collagen-induced arthritis. J Exp Med 1998; 187: 461-468. (Pubitemid 28093348)
11. Deng C, Goluszko E, Tuzun E, Yang H, Christadoss P. Resistance to experimental autoimmune myasthenia gravis in IL-6-deficient mice is associated with reduced germinal center formation and C3 production. JImmunol 2002; 169: 1077-1083. (Pubitemid 34753468)
12. Richards HB, Satoh M, Shaw M, Libert C, Poli V, Reeves WH. Interleukin 6dependence of anti-DNA antibody production: evidence for two pathways of autoantibody formation in pristane-induced lupus. J Exp Med 1998; 188: 985-990. (Pubitemid 28433425)
13. Poffenberger MC, Straka N, El Warry N, Fang D, Shanina I, Horwitz MS. Lack of IL-6 during coxsackievirus infection heightens the early immune response resulting in increased severity of chronic autoimmune myocarditis. PLo S ONE 2009; 4: e6207.
14. Xing Z, Gauldie J, Cox G, Baumann H, Jordana M, Lei XF et al. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J Clin Invest 1998; 101: 311-320. (Pubitemid 28067327)
15. Fattori E, Cappelletti M, Costa P, Sellitto C, Cantoni L, Carelli M et al. Defective inflammatory response in interleukin 6-deficient mice. J Exp Med 1994; 180: 1243-1250. (Pubitemid 24289598)
16. Tilg H, Trehu E, Atkins MB, Dinarello CA, Mier JW. Interleukin-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood 1994; 83: 113-118. (Pubitemid 24016522)
17. Matsuyama M, Suzuki T, Tsuboi H, Ito S, Mamura M, Goto D et al. Anti-interleukin-6 receptor antibody (tocilizumab) treatment of multicentric Castleman's disease. Intern Med (Tokyo, Japan) 2007; 46: 771-774. (Pubitemid 46902277)
18. Yokota S, Imagawa T, Mori M, Miyamae T, Aihara Y, Takei S et al. Efficacy and safety of tocilizumab in patientswith systemic-onset juvenile idiopathic arthritis: A randomised, double-blind, placebo-controlled, withdrawal phase III trial. Lancet 2008; 371: 998-1006. (Pubitemid 351389534)
19. Smolen JS, Beaulieu A, Rubbert-Roth A, Ramos-Remus C, Rovensky J, Alecock E et al. Effect of interleukin-6 receptor inhibition with tocilizumab in patients with rheumatoid arthritis (OPTION study): A double-blind, placebo-controlled, randomised trial. Lancet 2008; 371: 987-997. (Pubitemid 351392039)
20. Croker BA, Krebs DL, Zhang JG, Wormald S, Willson TA, Stanley EG et al. SOCS3 negatively regulates IL-6 signaling in vivo. Nat Immunol 2003; 4: 540-545. (Pubitemid 36701336)
21. Lang R, Pauleau AL, Parganas E,Takahashi Y, Mages J, Ihle JN et al. SOCS3 regulates the plasticity of gp130 signaling. Nat Immunol 2003; 4: 546-550. (Pubitemid 36701337)
22. Yasukawa H, Ohishi M, Mori H, Murakami M, Chinen T, Aki D et al. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat Immunol 2003; 4: 551-556. (Pubitemid 36701338)
23. Nicholson SE, De Souza D, Fabri LJ, Corbin J, Willson TA, Zhang JG 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 2000; 97: 6493-6498. (Pubitemid 30412741)
24. Ohtani T, Ishihara K, Atsumi T, Nishida K, Kaneko Y, Miyata T et al. Dissection of signaling cascades through gp130 in vivo: reciprocal roles for STAT3- and SHP2-mediated signals in immune responses. Immunity 2000; 12: 95-105. (Pubitemid 30069218)
25. Croker BA, Metcalf D, Robb L, Wei W, Mifsud S, Di Rago L et al. SOCS3 is a critical physiological negative regulator of G-CSF signaling and emergency granulopoiesis. Immunity 2004; 20: 153-165. (Pubitemid 38258392)
26. Wong PK, Egan PJ, Croker BA, O'Donnell K, Sims NA, Drake S et al. SOCS-3 negatively regulates innate and adaptive immune mechanisms in acute IL-1-dependent inflam-matoryarthritis. J Clin Invest 2006; 116: 1571-1581.
27. Gainsford T, Roberts AW, Kimura S, Metcalf D, Dranoff G, Mulligan RC et al. Cytokine production and function in c-mpl-deficient mice: no physiologic role for interleukin-3 in residual megakaryocyte and platelet production. Blood 1998; 91: 2745-2752. (Pubitemid 28227524)
28. 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 inflamma-toryarthritis. JClin Invest 2001; 108: 1781-1788. (Pubitemid 34015123)
29. Wilson EB, Brooks DG. Translating insights from persistent LCMV infection into anti-HIV immunity. Immunol Res 2010; 48: 3-13.
30. Pellegrini M, Calzascia T, Elford AR, Shahinian A, Lin AE, Dissanayake D et al. Adjuvant IL-7 antagonizes multiple cellular and molecular inhibitory networks to enhance immunotherapies. Nat Med 2009; 15: 528-536.
31. Croker BA, Mielke LA, Wormald S, Metcalf D, Kiu H, Alexander WS et al. Socs3 maintains the specificity of biological responses to cytokine signals during granulocyte and macrophage differentiation. Exp Hematol 2008; 36: 786-798.
32. Lu Y, Fukuyama S, Yoshida R, Kobayashi T, Saeki K, Shiraishi H et al. Loss of SOCS3 gene expression converts STAT3 function from anti-apoptotic to pro-apoptotic. J Biol Chem 2006; 281: 36683-36690. (Pubitemid 46042135)
33. Wang SD, Huang KJ, Lin YS, Lei HY. Sepsis-induced apoptosis of the thymocytes in mice. J Immunol 1994; 152: 5014-5021.
34. Ahmed R, Salmi A, Butler LD, Chiller JM, Oldstone MB. Selection of geneticvariantsof lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J Exp Med1984; 160:521-540. (Pubitemid 14052514)
35. Battegay M, Cooper S, Althage A, Banziger J, Hengartner H, Zinkernagel RM. Quantification of lymphocytic choriomeningitis virus with an immunological focus assay in 24- or 96-well plates. J Virol Methods 1991; 33: 191-198.