Interleukin-10 inhibits lipopolysaccharide-induced tumor necrosis factor-α translation through a SHIP1-dependent pathway

Journal of Biological Chemistry

Volumn 287, Issue 45, 2012, Pages 38020-38027

  Chan, Catherine S ^a,b   Ming Lum, Andrew ^a,b   Golds, Gary B ^a,b   Lee, Shaina J ^a,b   Anderson, Raymond J ^b   Mui, Alice L F ^a,b  

^a VANCOUVER COASTAL HEALTH RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-INFLAMMATORY RESPONSE; INTERLEUKIN-10; REGULATORY MECHANISM; TUMOR NECROSIS FACTORS;

BIOCHEMISTRY;

BIOLOGY;

INTERLEUKIN 10; MAPK SIGNAL INTEGRATING KINASE 1; PHOSPHATASE; PHOSPHOTRANSFERASE; SH2 DOMAIN CONTAINING INOSITOL 5' PHOSPHATASE 1; STAT3 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME REGULATION; GENE EXPRESSION REGULATION; HUMAN; IMMUNE RESPONSE; POLYSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CELLS, CULTURED; FEMALE; IMMUNOBLOTTING; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84868322918     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.348599     Document Type: Article

References (46)

1. Chow, J. C., Young, D. W., Golenbock, D. T., Christ, W. J., and Gusovsky, F. (1999) Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem. 274, 10689-10692
2. Kruys, V., Kemmer, K., Shakhov, A., Jongeneel, V., and Beutler, B. (1992) Constitutive activity of the tumor necrosis factor promoter is canceled by the 3'-untranslated region in nonmacrophage cell lines; a trans-dominant factor overcomes this suppressive effect. Proc. Natl. Acad. Sci. U.S.A. 89, 673-677
3. Lai, W. S., Carballo, E., Strum, J. R., Kennington, E. A., Phillips, R. S., and Blackshear, P. J. (1999) Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor-α mRNA. Mol. Cell. Biol. 19, 4311-4323 (Pubitemid 29242006)
4. Piecyk, M., Wax, S., Beck, A. R., Kedersha, N., Gupta, M., Maritim, B., Chen, S., Gueydan, C., Kruys, V., Streuli, M., and Anderson, P. (2000) TIA-1 is a translational silencer that selectively regulates the expression of TNFα. EMBO J. 19, 4154-4163 (Pubitemid 30608553)
5. Buxadé, M., Parra, J. L., Rousseau, S., Shpiro, N., Marquez, R., Morrice, N., Bain, J., Espel, E., and Proud, C. G. (2005) The Mnks are novel components in the control of TNFα biosynthesis and phosphorylate and regulate hn- RNP A1. Immunity 23, 177-189 (Pubitemid 41169287)
6. Beisang, D., and Bohjanen, P. R. (2012) Perspectives on the ARE as it turns 25 years old. Wiley Interdiscip. Rev. RNA 3, 719-731
7. Cargnello, M., and Roux, P. P. (2011) Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol. Mol. Biol. Rev. 75, 50-83
8. Buxade, M., Parra-Palau, J. L., and Proud, C. G. (2008) The Mnks: MAP kinase-interacting kinases (MAP kinase signal-integrating kinases). Front. Biosci. 13, 5359-5373
9. Flynn, A., and Proud, C. G. (1995) Serine 209, not serine 53, is the major site of phosphorylation in initiation factor eIF4E in serum-treated Chinese hamster ovary cells. J. Biol. Chem. 270, 21684-21688
10. Joshi, B., Cai, A. L., Keiper, B. D., Minich, W. B., Mendez, R., Beach, C. M., Stepinski, J., Stolarski, R., Darzynkiewicz, E., and Rhoads, R. E. (1995) Phosphorylation of eukaryotic protein synthesis initiation factor 4E at Ser-209. J. Biol. Chem. 270, 14597-14603
11. Kühn, R., Löhler, J., Rennick, D., Rajewsky, K., and Müller, W. (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263-274 (Pubitemid 23320290)
12. Glocker, E. O., Kotlarz, D., Klein, C., Shah, N., and Grimbacher, B. (2012) IL-10 and IL-10 receptor defects in humans. Ann. N.Y. Acad. Sci. 1246, 102-107
13. Franke, A., Balschun, T., Karlsen, T. H., Sventoraityte, J., Nikolaus, S., Mayr, G., Domingues, F. S., Albrecht, M., Nothnagel, M., Ellinghaus, D., Sina, C., Onnie, C. M., Weersma, R. K., Stokkers, P. C., Wijmenga, C., Gazouli, M., Strachan, D., McArdle, W. L., Vermeire, S., Rutgeerts, P., Rosenstiel, P., Krawczak, M., Vatn, M. H., IBSEN study group, Mathew, C. G., and Schreiber, S. (2008) Sequence variants in IL10, ARPC2, and multiple other loci contribute to ulcerative colitis susceptibility. Nat. Genet. 40, 1319-1323
14. Spencer, S. D., Di Marco, F., Hooley, J., Pitts-Meek, S., Bauer, M., Ryan, A. M., Sordat, B., Gibbs, V. C., and Aguet, M. (1998) The orphan receptor CRF2-4 is an essential subunit of the interleukin-10 receptor. J. Exp. Med. 187, 571-578 (Pubitemid 28093359)
15. Murray, P. J. (2006) Understanding and exploiting the endogenous interleukin- 10/STAT3-mediated anti-inflammatory response. Curr. Opin. Pharmacol. 6, 379-386
16. El Kasmi, K. C., Holst, J., Coffre, M., Mielke, L., de Pauw, A., Lhocine, N., Smith, A. M., Rutschman, R., Kaushal, D., Shen, Y., Suda, T., Donnelly, R. P., Myers, M. G., Jr., Alexander, W., Vignali, D. A., Watowich, S. S., Ernst, M., Hilton, D. J., and Murray, P. J. (2006) General nature of the STAT3-activated anti-inflammatory response. J. Immunol. 177, 7880-7888 (Pubitemid 44846303)
17. Murray, P. J. (2005) The primary mechanism of the IL-10-regulated antiinflammatory response is to selectively inhibit transcription. Proc. Natl. Acad. Sci. U.S.A. 102, 8686-8691 (Pubitemid 40862796)
18. Murray, P. J. (2006) STAT3-mediated anti-inflammatory signaling. Biochem. Soc. Trans. 34, 1028-1031
19. Hutchins, A. P., Poulain, S., and Miranda-Saavedra, D. (2012) Genomewide analysis of STAT3 binding in vivo predicts effectors of the antiinflammatory response in macrophages. Blood 119, e110-e119
20. Kuwata, H., Watanabe, Y., Miyoshi, H., Yamamoto, M., Kaisho, T., Takeda, K., and Akira, S. (2003) IL-10-inducible Bcl-3 negatively regulates LPS-induced TNFα production in macrophages. Blood 102, 4123-4129 (Pubitemid 37486997)
21. Schaljo, B., Kratochvill, F., Gratz, N., Sadzak, I., Sauer, I., Hammer, M., Vogl, C., Strobl, B., Müller, M., Blackshear, P. J., Poli, V., Lang, R., Murray, P. J., and Kovarik, P. (2009) Tristetraprolin is required for full anti-inflammatory response of murine macrophages to IL-10. J. Immunol. 183, 1197-1206
22. El Kasmi, K. C., Smith, A. M., Williams, L., Neale, G., Panopolous, A., Watowich, S. S., Häcker, H., Foxwell, B. M., and Murray, P. J. (2007) Cutting edge: a transcriptional repressor and corepressor induced by the STAT3-regulated anti-inflammatory signaling pathway. J. Immunol. 179, 7215-7219
23. Kerr, W. G. (2011) Inhibitor and activator: dual functions for SHIP in immunity and cancer. Ann. N.Y. Acad. Sci. 1217, 1-17
24. Sly, L. M., Ho, V., Antignano, F., Ruschmann, J., Hamilton, M., Lam, V., Rauh, M. J., and Krystal, G. (2007) The role of SHIP in macrophages. Front. Biosci. 12, 2836-2848
25. Kontoyiannis, D., Kotlyarov, A., Carballo, E., Alexopoulou, L., Blackshear, P. J., Gaestel, M., Davis, R., Flavell, R., and Kollias, G. (2001) Interleukin-10 targets p38 MAPK to modulate ARE-dependent TNF mRNA translation and limit intestinal pathology. EMBO J. 20, 3760-3770 (Pubitemid 32691787)
26. Andersson, K., and Sundler, R. (2006) Post-transcriptional regulation of TNFα expression via eukaryotic initiation factor 4E (eIF4E) phosphorylation in mouse macrophages. Cytokine 33, 52-57 (Pubitemid 43220353)
27. Wan, Y., Xiao, H., Affolter, J., Kim, T. W., Bulek, K., Chaudhuri, S., Carlson, D., Hamilton, T., Mazumder, B., Stark, G. R., Thomas, J., and Li, X. (2009) Interleukin-1 receptor-associated kinase 2 is critical for lipopolysaccharide- mediated post-transcriptional control. J. Biol. Chem. 284, 10367-10375
28. Rowlett, R. M., Chrestensen, C. A., Schroeder, M. J., Harp, M. G., Pelo, J. W., Shabanowitz, J., DeRose, R., Hunt, D. F., Sturgill, T. W., and Worthington, M. T. (2008) Inhibition of tristetraprolin deadenylation by poly(A)-binding protein. Am. J. Physiol. Gastrointest. Liver Physiol. 295, G421-G430
29. Stamou, P., and Kontoyiannis, D. L. (2010) Post-transcriptional regulation of TNF mRNA: a paradigm of signal-dependent mRNA utilization and its relevance to pathology. Curr. Dir. Autoimmun. 11, 61-79
30. Ong, C. J., Ming-Lum, A., Nodwell, M., Ghanipour, A., Yang, L., Williams, D. E., Kim, J., Demirjian, L., Qasimi, P., Ruschmann, J., Cao, L. P., Ma, K., Chung, S. W., Duronio, V., Andersen, R. J., Krystal, G., and Mui, A. L. (2007) Small-molecule agonists of SHIP1 inhibit the phosphoinositide 3-kinase pathway in hematopoietic cells. Blood 110, 1942-1949 (Pubitemid 47443908)
31. Denys, A., Udalova, I. A., Smith, C., Williams, L. M., Ciesielski, C. J., Campbell, J., Andrews, C., Kwaitkowski, D., and Foxwell, B. M. (2002) Evidence for a dual mechanism for IL-10 suppression of TNFα production that does not involve inhibition of p38 mitogen-activated protein kinase or NF-κB in primary human macrophages. J. Immunol. 168, 4837-4845 (Pubitemid 34495944)
32. Ronkina, N., Menon, M. B., Schwermann, J., Tiedje, C., Hitti, E., Kotlyarov, A., and Gaestel, M. (2010) MAPKAP kinases MK2 and MK3 in inflammation: complex regulation of TNF biosynthesis via expression and phosphorylation of tristetraprolin. Biochem. Pharmacol. 80, 1915-1920
33. Polunovsky, V. A., and Bitterman, P. B. (2006) The cap-dependent translation apparatus integrates and amplifies cancer pathways. RNA Biol. 3, 10-17
34. Rowlett, R. M., Chrestensen, C. A., Nyce, M., Harp, M. G., Pelo, J. W., Cominelli, F., Ernst, P. B., Pizarro, T. T., Sturgill, T. W., and Worthington, M. T. (2008) MNK kinases regulate multiple TLR pathways and innate proinflammatory cytokines in macrophages. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G452-G459 (Pubitemid 351253336)
35. Scheper, G. C., and Proud, C. G. (2002) Does phosphorylation of the capbinding protein eIF4E play a role in translation initiation? Eur. J. Biochem. 269, 5350-5359 (Pubitemid 35365524)
36. Hay, N. (2010) Mnk earmarks eIF4E for cancer therapy. Proc. Natl. Acad. Sci. U.S.A. 107, 13975-13976
37. Hou, J., Lam, F., Proud, C., and Wang, S. (2012) Targeting Mnks for cancer therapy. Oncotarget 3, 118-131
38. Ueda, T., Watanabe-Fukunaga, R., Fukuyama, H., Nagata, S., and Fukunaga, R. (2004) Mnk2 and Mnk1 are essential for constitutive and inducible phosphorylation of eukaryotic initiation factor 4E but not for cell growth or development. Mol. Cell. Biol. 24, 6539-6549 (Pubitemid 38944335)
39. Yanagiya, A., Suyama, E., Adachi, H., Svitkin, Y. V., Aza-Blanc, P., Imataka, H., Mikami, S., Martineau, Y., Ronai, Z. A., and Sonenberg, N. (2012) Translational homeostasis via the mRNA cap-binding protein, eIF4E. Mol. Cell 46, 847-858
40. Gingras, A. C., Kennedy, S. G., O'Leary, M. A., Sonenberg, N., and Hay, N. (1998) 4E-BP1, a repressor of mRNA translation, is phosphorylated and inactivated by the Akt(PKB) signaling pathway. Genes Dev. 12, 502-513 (Pubitemid 28101013)
41. Monick, M. M., Carter, A. B., Robeff, P. K., Flaherty, D. M., Peterson, M. W., and Hunninghake, G. W. (2001) Lipopolysaccharide activates Akt in human alveolar macrophages, resulting in nuclear accumulation and transcriptional activity of β-catenin. J. Immunol. 166, 4713-4720 (Pubitemid 32233759)
42. Lopez de Silanes, I., Galban, S., Martindale, J. L., Yang, X., Mazan-Mamczarz, K., Indig, F. E., Falco, G., Zhan, M., and Gorospe, M. (2005) Identification and functional outcome of mRNAs associated with RNA-binding protein TIA-1. Mol. Cell. Biol. 25, 9520-9531 (Pubitemid 41507852)
43. Gueydan, C., Droogmans, L., Chalon, P., Huez, G., Caput, D., and Kruys, V. (1999) Identification of TIAR as a protein binding to the translational regulatory AU-rich element of tumor necrosis factor-α mRNA. J. Biol. Chem. 274, 2322-2326
44. Mukhopadhyay, D., Houchen, C. W., Kennedy, S., Dieckgraefe, B. K., and Anant, S. (2003) Coupled mRNA stabilization and translational silencing of cyclooxygenase-2 by a novel RNA-binding protein, CUGBP2. Mol. Cell 11, 113-126 (Pubitemid 36126595)
45. Anderson, P., and Kedersha, N. (2007) On again, off again: the SRC-3 transcriptional coactivator moonlights as a translational corepressor. Mol. Cell 25, 796-797 (Pubitemid 46436536)
46. Qi, M. Y., Wang, Z. Z., Zhang, Z., Shao, Q., Zeng, A., Li, X. Q., Li, W. Q., Wang, C., Tian, F. J., Li, Q., Zou, J., Qin, Y. W., Brewer, G., Huang, S., and Jing, Q. (2012) AU-rich element-dependent translation repression requires the cooperation of tristetraprolin and RCK/P54. Mol. Cell. Biol. 32, 913-928