MSK1 regulates the transcription of IL-1ra in response to TLR activation in macrophages

Biochemical Journal

Volumn 425, Issue 3, 2010, Pages 595-602

  Darragh, Joanne ^a   Ananieva, Olga ^a   Courtney, Alan ^a   Elcombe, Suzanne ^a   Arthur, J Simon C ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Extracellular signal regulated kinase 1 2 (ERK1 2); Interleukin 1 (IL 1); Interleukin 10 (IL 10); Lipopolysaccharide (LPS); Macrophage; Mitogen and stress activated kinase 1 (MSK1); Nuclear factor B (NF B)

Indexed keywords

EXTRACELLULAR- SIGNAL-REGULATED KINASE 1/2; INTERLEUKIN-1; INTERLEUKIN-10; LIPOPOLYSACCHARIDE (LPS); LIPOPOLYSACCHARIDES; MITOGENS; NUCLEAR FACTORS; STRESS-ACTIVATED KINASE;

MACROPHAGES; PROTEINS; TRANSCRIPTION;

ENZYME ACTIVITY;

INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; LIPOPOLYSACCHARIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN AND STRESS ACTIVATED KINASE 1; MITOGEN AND STRESS ACTIVATED KINASE 2; PROTEIN SERINE THREONINE KINASE; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; IN VIVO STUDY; INFLAMMATION; KNOCKOUT MOUSE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; FEMALE; GENE EXPRESSION REGULATION; INFLAMMATION; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; TOLL-LIKE RECEPTORS;

MUS;

EID: 74349101011     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20091062     Document Type: Article

References (57)

1. Arend, W. P. (2002) The balance between IL-1 and IL-1Ra in disease. Cytokine Growth Factor Rev. 13, 323-340
2. Dinarello, C. A. (2009) Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 27, 519-550
3. Dinarello, C. A. (2004) Therapeutic strategies to reduce IL-1 activity in treating local and systemic inflammation. Curr. Opin. Pharmacol. 4, 378-385
4. Dayer, J. M. (2003) The pivotal role of interleukin-1 in the clinical manifestations of rheumatoid arthritis. Rheumatology 42 (Suppl. 2) ii3-ii10
5. Kay, J. and Calabrese, L. (2004) The role of interleukin-1 in the pathogenesis of rheumatoid arthritis. Rheumatology 43 (Suppl. 3) iii2-iii9
6. Dunne, A. and O'Neill, L. A. (2003) The interleukin-1 receptor/Toll-like receptor superfamily: signal transduction during inflammation and host defense. Sci. STKE 2003, re3
7. O'Neill, L. A. and Greene, C. (1998) Signal transduction pathways activated by the IL-1 receptor family: ancient signaling machinery in mammals, insects, and plants. J. Leukocyte Biol. 63, 650-657
8. Arend, W. P. and Gabay, C. (2000) Physiologic role of interleukin-1 receptor antagonist. Arthritis Res. 2, 245-248
9. Arend, W. P., Malyak, M., Guthridge, C. J. and Gabay, C. (1998) Interleukin-1 receptor antagonist: role in biology. Annu. Rev. Immunol. 16, 27-55
10. Niki, Y., Yamada, H., Seki, S., Kikuchi, T., Takaishi, H., Toyama, Y., Fujikawa, K. and Tada, N. (2001) Macrophage- and neutrophil-dominant arthritis in human IL-1α transgenic mice. J. Clin. Invest. 107, 1127-1135
11. Iwakura, Y. (2002) Roles of IL-1 in the development of rheumatoid arthritis: consideration from mouse models. Cytokine Growth Factor Rev. 13, 341-355
12. Horai, R., Nakajima, A., Habiro, K., Kotani, M., Nakae, S., Matsuki, T., Nambu, A., Saijo, S., Kotaki, H., Sudo, K. et al. (2004) TNF-α is crucial for the development of autoimmune arthritis in IL-1 receptor antagonist-deficient mice. J. Clin. Invest. 114, 1603-1611
13. Kalliolias, G. D. and Liossis, S. N. (2008) The future of the IL-1 receptor antagonist anakinra: from rheumatoid arthritis to adult-onset Still's disease and systemic-onset juvenile idiopathic arthritis. Expert Opin. Investig. Drugs 17, 349-359
14. Burns, K., Martinon, F. and Tschopp, J. (2003) New insights into the mechanism of IL-1β maturation. Curr. Opin. Immunol. 15, 26-30
15. Fenton, M. J. (1992) Review: transcriptional and post-transcriptional regulation of interleukin 1 gene expression. Int. J. Immunopharmacol. 14, 401-411
16. Dinarello, C. A. (1996) Biologic basis for interleukin-1 in disease. Blood 87, 2095-2147
17. Lennard, A. C. (1995) Interleukin-1 receptor antagonist. Crit. Rev. Immunol. 15, 77-105
18. Takeda, K. and Akira, S. (2007) Toll-like receptors, Curr. Protoc. Immunol. Chapter 14, Unit 14.12
19. Smith, Jr, M. F., Eidlen, D., Brewer, M. T., Eisenberg, S. P., Arend, W. P. and Gutierrez-Hartmann, A. (1992) Human IL-1 receptor antagonist promoter. Cell type-specific activity and identification of regulatory regions. J. Immunol. 149, 2000-2007
20. Butcher, C., Steinkasserer, A., Tejura, S. and Lennard, A. C. (1994) Comparison of two promoters controlling expression of secreted or intracellular IL-1 receptor antagonist. J. Immunol. 153, 701-711
21. Malyak, M., Smith, Jr, M. F., Abel, A. A., Hance, K. R. and Arend, W. P. (1998) The differential production of three forms of IL-1 receptor antagonist by human neutrophils and monocytes. J. Immunol. 161, 2004-2010
22. Malyak, M., Guthridge, J. M., Hance, K. R., Dower, S. K., Freed, J. H. and Arend, W. P. (1998) Characterization of a low molecular weight isoform of IL-1 receptor antagonist. J. Immunol. 161, 1997-2003
23. Smith, Jr, M. F., Carl, V. S., Lodie, T. and Fenton, M. J. (1998) Secretory interleukin-1 receptor antagonist gene expression requires both a PU.1 and a novel composite NF-κB/PU.1/GA-binding protein binding site. J. Biol. Chem. 273, 24272-24279
24. Smith, Jr, M. F., Eidlen, D., Arend, W. P. and Gutierrez-Hartmann, A. (1994) LPS-induced expression of the human IL-1 receptor antagonist gene is controlled by multiple interacting promoter elements. J. Immunol. 153, 3584-3593
25. Carl, V. S., Brown-Steinke, K., Nicklin, M. J. and Smith, Jr, M. F. (2002) Toll-like receptor 2 and 4 (TLR2 and TLR4) agonists differentially regulate secretory interleukin-1 receptor antagonist gene expression in macrophages. J. Biol. Chem. 277, 17448-17456
26. Carl, V. S., Gautam, J. K., Comeau, L. D. and Smith, Jr, M. F. (2004) Role of endogenous IL-10 in LPS-induced STAT3 activation and IL-1 receptor antagonist gene expression. J. Leukocyte Biol. 76, 735-742
27. Ohmori, Y., Smith, Jr, M. F. and Hamilton, T. A. (1996) IL-4-induced expression of the IL-1 receptor antagonist gene is mediated by STAT6. J. Immunol. 157, 2058-2065
28. Dreyer, M. G., Juge-Aubry, C. E., Gabay, C., Lang, U., Rohner-Jeanrenaud, F., Dayer, J. M. and Meier, C. A. (2003) Leptin activates the promoter of the interleukin-1 receptor antagonist through p42/44 mitogen-activated protein kinase and a composite nuclear factor ?B/PU.1 binding site. Biochem. J. 370, 591-599
29. Roux, P. P. and Blenis, J. (2004) ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 68, 320-344
30. Arthur, J. S. C. (2008) MSK activation and physiological roles. Front. Biosci. 13, 5866-5879
31. McCoy, C. E., Campbell, D. G., Deak, M., Bloomberg, G. B. and Arthur, J. S. C. (2005) MSK1 activity is controlled by multiple phosphorylation sites. Biochem. J. 387, 507-517
32. McCoy, C. E., Macdonald, A., Morrice, N. A., Campbell, D. G., Deak, M., Toth, R., McIlrath, J. and Arthur, J. S. C. (2007) Identification of novel phosphorylation sites in MSK1 by precursor ion scanning MS. Biochem. J. 402, 491-501
33. Arthur, J. S. C. and Cohen, P. (2000) MSK1 is required for CREB phosphorylation in response to mitogens in mouse embryonic stem cells. FEBS Lett. 482, 44-48
34. Wiggin, G. R., Soloaga, A., Foster, J. M., Murray-Tait, V., Cohen, P. and Arthur, J. S. C. (2002) MSK1 and MSK2 are required for the mitogen- and stress-induced phosphorylation of CREB and ATF1 in fibroblasts. Mol. Cell. Biol. 22, 2871-2881
35. Song, K. S., Lee, W. J., Chung, K. C., Koo, J. S., Yang, E. J., Choi, J. Y. and Yoon, J. H. (2003) Interleukin-1β and tumor necrosis factor-α induce MUC5AC overexpression through a mechanism involving ERK/p38 mitogen-activated protein kinases-MSK1-CREB activation in human airway epithelial cells. J. Biol. Chem. 278, 23243-23250
36. Schuck, S., Soloaga, A., Schratt, G., Arthur, J. S. and Nordheim, A. (2003) The kinase MSK1 is required for induction of c-fos by lysophosphatidic acid in mouse embryonic stem cells. BMC Mol. Biol. 4, 6
37. Soloaga, A., Thomson, S., Wiggin, G. R., Rampersaud, N., Dyson, M. H., Hazzalin, C. A., Mahadevan, L. C. and Arthur, J. S. (2003) MSK2 and MSK1 mediate the mitogen- and stress-induced phosphorylation of histone H3 and HMG-14. EMBO J. 22, 2788-2797
38. Darragh, J., Soloaga, A., Beardmore, V. A., Wingate, A. D., Wiggin, G. R., Peggie, M. and Arthur, J. S. (2005) MSKs are required for the transcription of the nuclear orphan receptors Nur77, Nurr1 and Nor1 downstream of MAPK signalling. Biochem. J. 390, 749-759
39. Vermeulen, L., De Wilde, G., Van Damme, P., Vanden Berghe, W. and Haegeman, G. (2003) Transcriptional activation of the NF-κB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J. 22, 1313-1324
40. Dyson, M. H., Thomson, S., Inagaki, M., Goto, H., Arthur, S. J., Nightingale, K., Iborra, F. J. and Mahadevan, L. C. (2005) MAP kinase-mediated phosphorylation of distinct pools of histone H3 at S10 or S28 via mitogen- and stress-activated kinase 1/2. J. Cell Sci. 118, 2247-2259
41. Davie, J. R. (2003) MSK1 and MSK2 mediate mitogen- and stress-induced phosphorylation of histone H3: a controversy resolved. Sci. STKE 2003, pe33
42. Dunn, K. L., Espino, P. S., Drobic, B., He, S. and Davie, J. R. (2005) The Ras-MAPK signal transduction pathway, cancer and chromatin remodeling. Biochem. Cell. Biol. 83, 1-14
43. Brami-Cherrier, K., Valjent, E., Herve, D., Darragh, J., Corvol, J. C., Pages, C., Arthur, S. J., Girault, J. A. and Caboche, J. (2005) Parsing molecular and behavioral effects of cocaine in mitogen- and stress-activated protein kinase-1-deficient mice. J. Neurosci. 25, 11444-11454
44. Chandramohan, Y., Droste, S. K., Arthur, J. S. C. and Reul, J. M. (2008) The forced swimming-induced behavioural immobility response involves histone H3 phospho-acetylation and c-Fos induction in dentate gyrus granule neurons via activation of the N-methyl-D-aspartate/ extracellular signal-regulated kinase/mitogen- and stress-activated kinase signalling pathway. Eur. J. Neurosci. 27, 2701-2713
45. Chwang, W. B., Arthur, J. S. C., Schumacher, A. and Sweatt, J. D. (2007) The nuclear kinase mitogen- and stress-activated protein kinase 1 regulates hippocampal chromatin remodeling in memory formation. J. Neurosci. 27, 12732-12742
46. Ananieva, O., Darragh, J., Johansen, C., Carr, J. M., McIlrath, J., Park, J. M., Wingate, A., Monk, C. E., Toth, R., Santos, S. G. et al. (2008) The kinases MSK1 and MSK2 act as negative regulators of Toll-like receptor signaling. Nat. Immunol. 9, 1028-1036
47. Kuhn, R., Lohler, J., Rennick, D., Rajewsky, K. and Muller, W. (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263-274
48. Beardmore, V. A., Hinton, H. J., Eftychi, C., Apostolaki, M., Armaka, M., Darragh, J., McIlrath, J., Carr, J. M., Armit, L. J., Clacher, C. et al. (2005) Generation and characterization of p38β (MAPK11) gene-targeted mice. Mol. Cell. Biol. 25, 10454-10464
49. La, E. and Fischer, S. M. (2001) Transcriptional regulation of intracellular IL-1 receptor antagonist gene by IL-1a in primary mouse keratinocytes. J. Immunol. 166, 6149-6155
50. Kim, C., Sano, Y., Todorova, K., Carlson, B. A., Arpa, L., Celada, A., Lawrence, T., Otsu, K., Brissette, J. L., Arthur, J. S. C. and Park, J. M. (2008) The kinase p38α serves cell type-specific inflammatory functions in skin injury and coordinates pro- and anti-inflammatory gene expression. Nat. Immunol. 9, 1019-1027
51. Seidel, H. M., Milocco, L. H., Lamb, P., Darnell, Jr, J. E., Stein, R. B. and Rosen, J. (1995) Spacing of palindromic half sites as a determinant of selective STAT (signal transducers and activators of transcription) DNA binding and transcriptional activity. Proc. Natl. Acad. Sci. U.S.A. 92, 3041-3045
52. Cieslik, K. A., Zhu, Y., Shtivelband, M. and Wu, K. K. (2005) Inhibition of p90 ribosomal S6 kinase-mediated CCAAT/enhancer-binding protein β activation and cyclooxygenase-2 expression by salicylate. J. Biol. Chem. 280, 18411-18417
53. Buck, M., Poli, V., van der Geer, P., Chojkier, M. and Hunter, T. (1999) Phosphorylation of rat serine 105 or mouse threonine 217 in C/EBPβ is required for hepatocyte proliferation induced by TGFa. Mol. Cell 4, 1087-1092
54. Wingate, A. D., Campbell, D. G., Peggie, M. and Arthur, J. S. C. (2006) Nur77 is phosphorylated in cells by RSK in response to mitogenic stimulation. Biochem. J. 393, 715-724
55. Anrather, J., Racchumi, G. and Iadecola, C. (2005) cis-acting, element-specific transcriptional activity of differentially phosphorylated nuclear factor-κB. J. Biol. Chem. 280, 244-252
56. Reber, L., Vermeulen, L., Haegeman, G. and Frossard, N. (2009) Ser276 phosphorylation of NF-κB p65 by MSK1 controls SCF expression in inflammation. PLoS One 4, e4393
57. Dong, J., Jimi, E., Zhong, H., Hayden, M. S. and Ghosh, S. (2008) Repression of gene expression by unphosphorylated NF-κB p65 through epigenetic mechanisms. Genes Dev. 22, 1159-1173