c-Jun N-terminal kinase phosphorylates DCP1a to control formation of P bodies

Journal of Cell Biology

Volumn 194, Issue 4, 2011, Pages 581-596

  Rzeczkowski, Katharina ^a   Beuerlein, Knut ^a   Müller, Helmut ^a   Dittrich Breiholz, Oliver ^b   Schneider, Heike ^b   Kettner Buhrow, Daniela ^a   Holtmann, Helmut ^b   Kracht, Michael ^a  

^a JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B ALPHA; INTERLEUKIN 8; MESSENGER RNA; PROTEIN; PROTEIN DCP1A; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR RELA; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UNCLASSIFIED DRUG;

ARTICLE; CELL INCLUSION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROCESSING BODY; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS;

ANIMALS; CYTOPLASMIC GRANULES; ENDORIBONUCLEASES; ENZYME ACTIVATION; EXORIBONUCLEASES; GENE EXPRESSION REGULATION; GENES, REPORTER; HEK293 CELLS; HUMANS; I-KAPPA B KINASE; INFLAMMATION MEDIATORS; INTERLEUKIN-1; INTERLEUKIN-8; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE KINASES; MICE; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; PHOSPHORYLATION; PROTEIN TRANSPORT; PROTEINS; RECEPTORS, INTERLEUKIN-1; RECOMBINANT FUSION PROTEINS; RNA STABILITY; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; TIME FACTORS; TRANS-ACTIVATORS; TRANSCRIPTION FACTOR RELA; TRANSFECTION;

EID: 80052626104     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201006089     Document Type: Article

References (55)

1. Anderson, P., and N. Kedersha. 2009. RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat. Rev. Mol. Cell Biol. 10:430-436.
2. Bai, R.Y., C. Koester, T. Ouyang, S.A. Hahn, M. Hammerschmidt, C. Peschel, and J. Duyster. 2002. SMIF, a Smad4-interacting protein that functions as a co-activator in TGFbeta signalling. Nat. Cell Biol. 4:181-190.
3. Bail, S., and M. Kiledjian. 2006. More than 1 + 2 in mRNA decapping. Nat. Struct. Mol. Biol. 13:7-9.
4. Beelman, C.A., A. Stevens, G. Caponigro, T.E. LaGrandeur, L. Hatfield, D.M. Fortner, and R. Parker. 1996. An essential component of the decapping enzyme required for normal rates of mRNA turnover. Nature. 382:642-646.
5. Bogoyevitch, M.A., and B. Kobe. 2006. Uses for JNK: the many and varied substrates of the c-Jun N-terminal kinases. Microbiol. Mol. Biol. Rev. 70:1061-1095.
6. Buchan, J.R., and R. Parker. 2009. Eukaryotic stress granules: the ins and outs of translation. Mol. Cell. 36:932-941.
7. Buss, H., A. Dörrie, M.L. Schmitz, E. Hoffmann, K. Resch, and M. Kracht. 2004. Constitutive and interleukin-1-inducible phosphorylation of p65 NF-kappaB at serine 536 is mediated by multiple protein kinases including IkappaB kinase (IKK)-alpha, IKKbeta, IKKepsilon, TRAF family member-associated (TANK)-binding kinase 1 (TBK1), and an unknown kinase and couples p65 to TATA-binding protein-associated factor II31-mediated interleukin-8 transcription. J. Biol. Chem. 279:55633-55643.
8. Callebaut, I. 2002. An EVH1/WH1 domain as a key actor in TGFbeta signalling. FEBS Lett. 519:178-180.
9. Chen, C.Y., R. Gherzi, J.S. Andersen, G. Gaietta, K. Jürchott, H.D. Royer, M. Mann, and M. Karin. 2000. Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation. Genes Dev. 14:1236-1248.
10. Cho, H., K.M. Kim, and Y.K. Kim. 2009. Human proline-rich nuclear receptor coregulatory protein 2 mediates an interaction between mRNA surveillance machinery and decapping complex. Mol. Cell. 33:75-86.
11. Cougot, N., S. Babajko, and B. Séraphin. 2004. Cytoplasmic foci are sites of mRNA decay in human cells. J. Cell Biol. 165:31-40.
12. Dérijard, B., M. Hibi, I.H. Wu, T. Barrett, B. Su, T. Deng, M. Karin, and R.J. Davis. 1994. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell. 76:1025-1037.
13. Dhamija, S., A. Doerrie, R. Winzen, O. Dittrich-Breiholz, A. Taghipour, N. Kuehne, M. Kracht, and H. Holtmann. 2010. IL-1-induced posttranscriptional mechanisms target overlapping translational silencing and destabilizing elements in IκBβ mRNA. J. Biol. Chem. 285:29165-29178.
14. Dunckley, T., and R. Parker. 1999. The DCP2 protein is required for mRNA decapping in Saccharomyces cerevisiae and contains a functional MutT motif. EMBO J. 18:5411-5422.
15. Eulalio, A., I. Behm-Ansmant, and E. Izaurralde. 2007a. P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell Biol. 8:9-22.
16. Eulalio, A., I. Behm-Ansmant, D. Schweizer, and E. Izaurralde. 2007b. P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol. Cell. Biol. 27:3970-3981.
17. Fenger-Grøn, M., C. Fillman, B. Norrild, and J. Lykke-Andersen. 2005. Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol. Cell. 20:905-915.
18. Finch, A., W. Davis, W.G. Carter, and J. Saklatvala. 2001. Analysis of mitogenactivated protein kinase pathways used by interleukin 1 in tissues in vivo: activation of hepatic c-Jun N-terminal kinases 1 and 2, and mitogenactivated protein kinase kinases 4 and 7. Biochem. J. 353:275-281.
19. Franks, T.M., and J. Lykke-Andersen. 2008. The control of mRNA decapping and P-body formation. Mol. Cell. 32:605-615.
20. Gaestel, M., A. Kotlyarov, and M. Kracht. 2009. Targeting innate immunity protein kinase signalling in inflammation. Nat. Rev. Drug Discov. 8:480-499.
21. Gupta, S., T. Barrett, A.J. Whitmarsh, J. Cavanagh, H.K. Sluss, B. Dérijard, and R.J. Davis. 1996. Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J. 15:2760-2770.
22. Hoffmann, E., O. Dittrich-Breiholz, H. Holtmann, and M. Kracht. 2002. Multiple control of interleukin-8 gene expression. J. Leukoc. Biol. 72:847-855.
23. Hoffmann, E., A. Thiefes, D. Buhrow, O. Dittrich-Breiholz, H. Schneider, K. Resch, and M. Kracht. 2005. MEK1-dependent delayed expression of Fos-related antigen-1 counteracts c-Fos and p65 NF-kappaB-mediated interleukin-8 transcription in response to cytokines or growth factors. J. Biol. Chem. 280:9706-9718.
24. Holtmann, H., R. Winzen, P. Holland, S. Eickemeier, E. Hoffmann, D. Wallach, N.L. Malinin, J.A. Cooper, K. Resch, and M. Kracht. 1999. Induction of interleukin-8 synthesis integrates effects on transcription and mRNA degradation from at least three different cytokine- or stress-activated signal transduction pathways. Mol. Cell. Biol. 19:6742-6753.
25. Holtmann, H., J. Enninga, S. Kalble, A. Thiefes, A. Dorrie, M. Broemer, R. Winzen, A. Wilhelm, J. Ninomiya-Tsuji, K. Matsumoto, et al. 2001. The MAPK kinase kinase TAK1 plays a central role in coupling the interleukin-1 receptor to both transcriptional and RNA-targeted mechanisms of gene regulation. J. Biol. Chem. 276:3508-3516.
26. Huangfu, W.C., E. Omori, S. Akira, K. Matsumoto, and J. Ninomiya-Tsuji. 2006. Osmotic stress activates the TAK1-JNK pathway while blocking TAK1-mediated NF-kappaB activation: TAO2 regulates TAK1 pathways. J. Biol. Chem. 281:28802-28810.
27. Johnson, G.L., and K. Nakamura. 2007. The c-jun kinase/stress-activated pathway: regulation, function and role in human disease. Biochim. Biophys. Acta. 1773:1341-1348.
28. Kedersha, N., G. Stoecklin, M. Ayodele, P. Yacono, J. Lykke-Andersen, M.J. Fritzler, D. Scheuner, R.J. Kaufman, D.E. Golan, and P. Anderson. 2005. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169:871-884.
29. Korhonen, R., K. Linker, A. Pautz, U. Förstermann, E. Moilanen, and H. Kleinert. 2007. Post-transcriptional regulation of human inducible nitricoxide synthase expression by the Jun N-terminal kinase. Mol. Pharmacol. 71:1427-1434.
30. Kracht, M., O. Truong, N.F. Totty, M. Shiroo, and J. Saklatvala. 1994. Interleukin 1 α activates two forms of p54 α mitogen-activated protein kinase in rabbit liver. J. Exp. Med. 180:2017-2025.
31. Krause, A., H. Holtmann, S. Eickemeier, R. Winzen, M. Szamel, K. Resch, J. Saklatvala, and M. Kracht. 1998. Stress-activated protein kinase/Jun N-terminal kinase is required for interleukin (IL)-1-induced IL-6 and IL-8 gene expression in the human epidermal carcinoma cell line KB. J. Biol. Chem. 273:23681-23689.
32. Kuan, C.Y., D.D. Yang, D.R. Samanta Roy, R.J. Davis, P. Rakic, and R.A. Flavell. 1999. The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron. 22:667-676.
33. Kyriakis, J.M., P. Banerjee, E. Nikolakaki, T. Dai, E.A. Rubie, M.F. Ahmad, J. Avruch, and J.R. Woodgett. 1994. The stress-activated protein kinase subfamily of c-Jun kinases. Nature. 369:156-160.
34. Lykke-Andersen, J. 2002. Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol. Cell. Biol. 22:8114-8121.
35. Ming, X.F., M. Kaiser, and C. Moroni. 1998. c-jun N-terminal kinase is involved in AUUUA-mediated interleukin-3 mRNA turnover in mast cells. EMBO J. 17:6039-6048.
36. Ninomiya-Tsuji, J., T. Kajino, K. Ono, T. Ohtomo, M. Matsumoto, M. Shiina, M. Mihara, M. Tsuchiya, and K. Matsumoto. 2003. A resorcylic acid lactone, 5Z-7-oxozeaenol, prevents inflammation by inhibiting the catalytic activity of TAK1 MAPK kinase kinase. J. Biol. Chem. 278:18485-18490.
37. Ohn, T., N. Kedersha, T. Hickman, S. Tisdale, and P. Anderson. 2008. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat. Cell Biol. 10:1224-1231.
38. Sakurai, H., A. Nishi, N. Sato, J. Mizukami, H. Miyoshi, and T. Sugita. 2002. TAK1-TAB1 fusion protein: a novel constitutively active mitogenactivated protein kinase kinase kinase that stimulates AP-1 and NF-kappaB signaling pathways. Biochem. Biophys. Res. Commun. 297:1277-1281.
39. Sheth, U., and R. Parker. 2003. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science. 300:805-808.
40. Shim, J.H., C. Xiao, A.E. Paschal, S.T. Bailey, P. Rao, M.S. Hayden, K.Y. Lee, C. Bussey, M. Steckel, N. Tanaka, et al. 2005. TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev. 19:2668-2681.
41. Teixeira, D., U. Sheth, M.A. Valencia-Sanchez, M. Brengues, and R. Parker. 2005. Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA. 11:371-382.
42. Thiefes, A., S. Wolter, J.F. Mushinski, E. Hoffmann, O. Dittrich-Breiholz, N. Graue, A. Dörrie, H. Schneider, D. Wirth, B. Luckow, et al. 2005. Simultaneous blockade of NFkappaB, JNK, and p38 MAPK by a kinaseinactive mutant of the protein kinase TAK1 sensitizes cells to apoptosis and affects a distinct spectrum of tumor necrosis factor [corrected] target genes. J. Biol. Chem. 280:27728-27741.
43. Thiefes, A., A. Wolf, A. Doerrie, G.A. Grassl, K. Matsumoto, I. Autenrieth, E. Bohn, H. Sakurai, R. Niedenthal, K. Resch, and M. Kracht. 2006. The Yersinia enterocolitica effector YopP inhibits host cell signalling by inactivating the protein kinase TAK1 in the IL-1 signalling pathway. EMBO Rep. 7:838-844.
44. Tritschler, F., J.E. Braun, C. Motz, C. Igreja, G. Haas, V. Truffault, E. Izaurralde, and O. Weichenrieder. 2009. DCP1 forms asymmetric trimers to assemble into active mRNA decapping complexes in metazoa. Proc. Natl. Acad. Sci. USA. 106:21591-21596.
45. Tscherne, J.S., and S. Pestka. 1975. Inhibition of protein synthesis in intact HeLa cells. Antimicrob. Agents Chemother. 8:479-487.
46. Weber, A., P. Wasiliew, and M. Kracht. 2010. Interleukin-1 (IL-1) pathway. Sci. Signal. 3:cm1.
47. Weston, C.R., and R.J. Davis. 2007. The JNK signal transduction pathway. Curr. Opin. Cell Biol. 19:142-149.
48. Winzen, R., M. Kracht, B. Ritter, A. Wilhelm, C.Y. Chen, A.B. Shyu, M. Müller, M. Gaestel, K. Resch, and H. Holtmann. 1999. The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J. 18:4969-4980.
49. Winzen, R., B.K. Thakur, O. Dittrich-Breiholz, M. Shah, N. Redich, S. Dhamija, M. Kracht, and H. Holtmann. 2007. Functional analysis of KSRP interaction with the AU-rich element of interleukin-8 and identification of inflammatory mRNA targets. Mol. Cell. Biol. 27:8388-8400.
50. Wolter, S., A. Doerrie, A. Weber, H. Schneider, E. Hoffmann, J. von der Ohe, L. Bakiri, E.F. Wagner, K. Resch, and M. Kracht. 2008. c-Jun controls histone modifications, NF-kappaB recruitment, and RNA polymerase II function to activate the ccl2 gene. Mol. Cell. Biol. 28:4407-4423.
51. Yamashita, A., T.C. Chang, Y. Yamashita, W. Zhu, Z. Zhong, C.Y. Chen, and A.B. Shyu. 2005. Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat. Struct. Mol. Biol. 12:1054-1063.
52. Yoon, J.H., E.J. Choi, and R. Parker. 2010. Dcp2 phosphorylation by Ste20 modulates stress granule assembly and mRNA decay in Saccharomyces cerevisiae. J. Cell Biol. 189:813-827.
53. Zhong, J., L.C. Gavrilescu, A. Molnár, L. Murray, S. Garafalo, J.H. Kehrl, A.R. Simon, R.A. Van Etten, and J.M. Kyriakis. 2009. GCK is essential to systemic inflammation and pattern recognition receptor signaling to JNK and p38. Proc. Natl. Acad. Sci. USA. 106:4372-4377.
54. Zhou, D., and S. Chen. 2001. PNRC2 is a 16 kDa coactivator that interacts with nuclear receptors through an SH3-binding motif. Nucleic Acids Res. 29:2003-2011.
55. Zhou, D., K.M. Quach, C. Yang, S.Y. Lee, B. Pohajdak, and S. Chen. 2000. PNRC: a proline-rich nuclear receptor coregulatory protein that modulates transcriptional activation of multiple nuclear receptors including orphan receptors SF1 (steroidogenic factor 1) and ERRalpha1 (estrogen related receptor alpha-1). Mol. Endocrinol. 14:986-998.