SOCS3 modulates interleukin-6R signaling preference in dermal fibroblasts

Journal of Interferon and Cytokine Research

Volumn 32, Issue 5, 2012, Pages 207-215

  Luckett Chastain, Lerin R ^a   Ihnat, Michael A ^a   Mickle Kawar, Bethany M ^a   Gallucci, Randle Michael ^a  

^a UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE A; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SERINE; SMALL INTERFERING RNA; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROBLAST; GENE EXPRESSION; GENE SILENCING; IMMUNOHISTOLOGY; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; CELLS, CULTURED; DERMIS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLASTS; GENE EXPRESSION REGULATION; INTERLEUKIN-6; MATRIX METALLOPROTEINASE 2; MICE; MICE, KNOCKOUT; P120 GTPASE ACTIVATING PROTEIN; PHOSPHORYLATION; RECEPTORS, INTERLEUKIN-6; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

MUS;

EID: 84861376072     PISSN: 10799907     EISSN: 15577465     Source Type: Journal    
DOI: 10.1089/jir.2011.0086     Document Type: Article

References (45)

1. Abe K, Hirai M, Mizuno K, Higashi N, Sekimoto T, Miki T, Hirano T, Nakajima K. 2001. The YXXQ motif in gp 130 is crucial for STAT3 phosphorylation at Ser727 through an H7-sensitive kinase pathway. Oncogene 20(27):3464-3474. (Pubitemid 32619401)
2. Auernhammer CJ, Melmed S. 2001. The central role of SOCS-3 in integrating the neuro-immunoendocrine interface. J Clin Invest 108(12):1735-1740. (Pubitemid 34015116)
3. Bansal MB, Kovalovich K, Gupta R, Li W, Agarwal A, Radbill B, Alvarez CE, Safadi R, Fiel MI, Friedman SL, Taub RA. 2005. Interleukin-6 protects hepatocytes from CCl4-mediated necrosis and apoptosis in mice by reducing MMP-2 expression. JHepatol 42(4):548-556. (Pubitemid 40342935)
4. Cacalano NA, Sanden D, Johnston JA. 2001. Tyrosinephosphorylated SOCS-3 inhibits STAT activation but binds to p120 RasGAP and activates Ras. Nat Cell Biol 3(5):460-465. (Pubitemid 32422081)
5. Chung J, Uchida E, Grammer TC, Blenis J. 1997. STAT3 serine phosphorylation by ERK-dependent and -independent pathways negatively modulates its tyrosine phosphorylation. Mol Cell Biol 17(11):6508-6516. (Pubitemid 27451197)
6. Cressman DE, Diamond RH, Taub R. 1995. Rapid activation of the Stat3 transcription complex in liver regeneration. Hepatology 21(5):1443-1449.
7. Daniels JT, Cambrey AD, Occleston NL, Garrett Q, Tarnuzzer RW, Schultz GS, Khaw PT. 2003. Matrix metalloproteinase inhibition modulates fibroblast-mediated matrix contraction and collagen production in vitro. Invest Ophthalmol Vis Sci 44(3):1104-1110. (Pubitemid 36297828)
8. Decker T, Kovarik P. 2000. Serine phosphorylation of STATs. Oncogene 19(21):2628-2637. (Pubitemid 30339219)
9. DiCosmo BF, Picarella D, Flavell RA. 1994. Local production of human IL-6 promotes insulitis but retards the onset of insulindependent diabetes mellitus in non-obese diabetic mice. Int Immunol 6(12):1829-1837.
10. Fischer P, Lehmann U, Sobota RM, Schmitz J, Niemand C, Linnemann S, Haan S, Behrmann I, Yoshimura A, Johnston JA, Muller-Newen G, Heinrich PC, Schaper F. 2004. The role of the inhibitors of interleukin-6 signal transduction SHP2 and SOCS3 for desensitization of interleukin-6 signalling. Biochem J 378(Pt 2):449-460. (Pubitemid 38367235)
11. Gallucci RM, Lee EG, Tomasek JJ. 2006. IL-6 Modulates Alpha-Smooth Muscle Actin Expression in Dermal Fibroblasts from IL-6-Deficient Mice. J Invest Dermatol 126(3):561-568. (Pubitemid 43255642)
12. Gallucci RM, Simeonova PP, Matheson JM, Kommineni C, Guriel JL, Sugawara T, Luster MI. 2000. Impaired cutaneous wound healing in interleukin-6-deficient and immunosuppressed mice. Faseb J 14(15):2525-2531.
13. Gallucci RM, Sloan DK, Heck JM, Murray AR, O'Dell SJ. 2004a. Interleukin 6 indirectly induces keratinocyte migration. J Invest Dermatol 122(3):764-772. (Pubitemid 38471347)
14. Gallucci RM, Sloan DK, O'Dell SJ, Reinke LA. 2004b. Differential expression of liver interleukin-6 receptor-alpha in female versus male ethanol-consuming rats. Alcohol Clin Exp Res 28(3):365-373. (Pubitemid 38380738)
15. Greenhalgh CJ, Hilton DJ. 2001. Negative regulation of cytokine signaling. J Leukoc Biol 70(3):348-356. (Pubitemid 32826121)
16. Haan S, Ferguson P, Sommer U, Hiremath M, McVicar DW, Heinrich PC, Johnston JA, Cacalano NA. 2003. Tyrosine phosphorylation disrupts elongin interaction and accelerates SOCS3 degradation. J Biol Chem 278(34):31972-31979. (Pubitemid 37048385)
17. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F. 2003. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 374(Pt 1):1-20. (Pubitemid 37046923)
18. Hibi M, Murakami M, Saito M, Hirano T, Taga T, Kishimoto T. 1990. Molecular cloning and expression of an IL-6 signal transducer, gp130. Cell 63(6):1149-1157. (Pubitemid 120035064)
19. Johnston JA. 2004. Are SOCS suppressors, regulators, and degraders? J Leukoc Biol 75(5):743-748. (Pubitemid 38580053)
20. Jones SA, Rose-John S. 2002. The role of soluble receptors in cytokine biology: the agonistic properties of the sIL-6R/IL-6 complex. Biochim Biophys Acta 1592(3):251-263. (Pubitemid 35284882)
21. Kado S, Nagase T, Nagata N. 1999. Circulating levels of interleukin-6, its soluble receptor and interleukin-6/interleukin-6 receptor complexes in patients with type 2 diabetes mellitus. Acta Diabetol 36(1-2):67-72.
22. Kamat CD, Green DE, Warnke L, Thorpe JE, Ceriello A, Ihnat MA. 2007. Mutant p53 facilitates pro-angiogenic, hyperproliferative phenotype in response to chronic relative hypoxia. Cancer letters 249(2):209-219. (Pubitemid 46452929)
23. Kamimura D, Ishihara K, Hirano T. 2003. IL-6 signal transduction and its physiological roles: the signal orchestration model. Rev Physiol Biochem Pharmacol 149:1-38.
24. Kamura T, Sato S, Haque D, Liu L, Kaelin WG, Jr., Conaway RC, Conaway JW. 1998. The Elongin BC complex interacts with the conserved SOCS-box motif present in members of the SOCS, ras, WD-40 repeat, and ankyrin repeat families. Genes Dev 12(24):3872-3881. (Pubitemid 29024849)
25. Kaplanski G, Marin V, Montero-Julian F, Mantovani A, Farnarier C. 2003. IL-6: a regulator of the transition from neutrophil to monocyte recruitment during inflammation. Trends Immunol 24(1):25-29. (Pubitemid 35462110)
26. Kile BT, Schulman BA, Alexander WS, Nicola NA, Martin HM, Hilton DJ. 2002. The SOCS box: a tale of destruction and degradation. Trends Biochem Sci 27(5):235-241. (Pubitemid 34655444)
27. Kopf M, Ramsay A, Brombacher F, Baumann H, Freer G, Galanos C, Gutierrez-Ramos JC, Kohler G. 1995. Pleiotropic defects of IL-6-deficient mice including early hematopoiesis, Tand B cell function, and acute phase responses. Ann N Y Acad Sci 762:308-318.
28. Lang R, Pauleau AL, Parganas E, Takahashi Y, Mages J, Ihle JN, Rutschman R, Murray PJ. 2003. SOCS3 regulates the plasticity of gp130 signaling. Nat Immunol 4(6):546-550. (Pubitemid 36701337)
29. Larsen L, Ropke C. 2002. Suppressors of cytokine signalling: SOCS. APMIS 110(12):833-844. (Pubitemid 36177279)
30. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)) Method. Methods 25(4):402-408. (Pubitemid 34164012)
31. Luckett LR, Gallucci RM. 2007. Interleukin-6 (IL-6) modulates migration and matrix metalloproteinase function in dermal fibroblasts from IL-6KO mice. Br J Dermatol 156(6):1163-1171. (Pubitemid 47029806)
32. Madlener M, Parks WC, Werner S. 1998. Matrix metalloproteinases (MMPs) and their physiological inhibitors (TIMPs) are differentially expressed during excisional skin wound repair. Exp Cell Res 242(1):201-210. (Pubitemid 28366535)
33. Narazaki M, Yasukawa K, Saito T, Ohsugi Y, Fukui H, Koishihara Y, Yancopoulos GD, Taga T, Kishimoto T. 1993. Soluble forms of the interleukin-6 signal-transducing receptor component gp130 in human serum possessing a potential to inhibit signals through membrane-anchored gp130. Blood 82(4):1120-1126. (Pubitemid 23253984)
34. O'Rourke L, Shepherd PR. 2002. Biphasic regulation of extracellular-signal-regulated protein kinase by leptin in macrophages: role in regulating STAT3 Ser727 phosphorylation and DNA binding. Biochem J 364(Pt 3):875-879. (Pubitemid 34680866)
35. Pamonsinlapatham P, Hadj-Slimane R, Lepelletier Y, Allain B, Toccafondi M, Garbay C, Raynaud F. 2009. P120-Ras GTPase activating protein (RasGAP): a multi-interacting protein in downstream signaling. Biochimie 91(3):320-328.
36. Paschoud S, Dogar AM, Kuntz C, Grisoni-Neupert B, Richman L, Kuhn LC. 2006. Destabilization of interleukin-6 mRNA requires a putative RNA stem-loop structure, an AU-rich element, and the RNA-binding protein AUF1. Mol Cell Biol 26(22):8228-8241. (Pubitemid 44748560)
37. Peraldi P, Filloux C, Emanuelli B, Hilton DJ, Van Obberghen E. 2001. Insulin induces suppressor of cytokine signaling-3 tyrosine phosphorylation through janus-activated kinase. J Biol Chem 276(27):24614-24620.
38. Sasaki A, Yasukawa H, Suzuki A, Kamizono S, Syoda T, Kinjyo I, Sasaki M, Johnston JA, Yoshimura A. 1999. Cytokineinducible SH2 protein-3 (CIS3/SOCS3) inhibits Janus tyrosine kinase by binding through the N-terminal kinase inhibitory region as well as SH2 domain. Genes Cells 4(6):339-351. (Pubitemid 29359449)
39. Schuringa JJ, Jonk LJ, Dokter WH, Vellenga E, Kruijer W. 2000. Interleukin-6-induced STAT3 transactivation and Ser727 phosphorylation involves Vav, Rac-1 and the kinase SEK-1/ MKK-4 as signal transduction components. Biochem J 347(Pt 1):89-96. (Pubitemid 30199045)
40. Sehgal PB. 1990. Interleukin-6: molecular pathophysiology. J Invest Dermatol 94(6 Suppl):2S-6S. (Pubitemid 20213060)
41. Sengupta TK, Talbot ES, Scherle PA, Ivashkiv LB. 1998. Rapid inhibition of interleukin-6 signaling and Stat3 activation mediated by mitogen-activated protein kinases. Proc Natl Acad Sci U S A 95(19):11107-11112. (Pubitemid 28450089)
42. Song H, Wang R, Wang S, Lin J. 2005. A low-molecular-weight compound discovered through virtual database screening inhibits Stat3 function in breast cancer cells. Proc Natl Acad Sci U S A 102(13):4700-4705. (Pubitemid 40471517)
43. Venkatasubbarao K, Choudary A, Freeman JW. 2005. Farnesyl transferase inhibitor (R115777)-induced inhibition of STAT3 (Tyr705) phosphorylation in human pancreatic cancer cell lines require extracellular signal-regulated kinases. Cancer Res 65(7):2861-2871. (Pubitemid 40490090)
44. Yasukawa H, Misawa H, Sakamoto H, Masuhara M, Sasaki A, Wakioka T, Ohtsuka S, Imaizumi T, Matsuda T, Ihle JN, Yoshimura A. 1999. The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop. EMBO J 18(5):1309-1320. (Pubitemid 29110315)
45. Zhang JG, Farley A, Nicholson SE, Willson TA, Zugaro LM, Simpson RJ, Moritz RL, Cary D, Richardson R, Hausmann G, Kile BJ, Kent SB, Alexander WS, Metcalf D, Hilton DJ, Nicola NA, Baca M. 1999. The conserved SOCS box motif in suppressors of cytokine signaling binds to elongins B and C and may couple bound proteins to proteasomal degradation. Proc Natl Acad Sci U S A 96(5):2071-2076. (Pubitemid 29117869)