MK2-induced tristetraprolin:14-3-3 Complexes prevent stress granule association and ARE-mRNA decay

EMBO Journal

Volumn 23, Issue 6, 2004, Pages 1313-1324

  Stoecklin, Georg ^a   Stubbs, Tiffany ^a   Kedersha, Nancy ^a   Wax, Stephen ^a   Rigby, William F C ^b   Blackwell, T Keith ^c   Anderson, Paul ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

AU rich element; MAPKAP kinase 2; MRNA turnover; TNF ; TTP

Indexed keywords

ARE BINDING PROTEIN; ARSENIC TRIOXIDE; BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; PROLINE; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELL STRAIN COS7; CONTROLLED STUDY; CYTOPLASM; MACROPHAGE; MOLECULAR DYNAMICS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RNA BINDING; TRANSLATION INITIATION;

14-3-3 PROTEINS; ADENOSINE; ANIMALS; ARSENITES; BINDING SITES; CELL LINE; CERCOPITHECUS AETHIOPS; DNA-BINDING PROTEINS; ENZYME ACTIVATION; HUMANS; IMMEDIATE-EARLY PROTEINS; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MICE; MUTATION; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA STABILITY; RNA, MESSENGER; SERINE; STRESS; TRISTETRAPROLIN; URIDINE;

ANIMALIA;

EID: 1942471656     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600163     Document Type: Article

References (39)

1. Anderson P, Kedersha N (2002) Stressful initiations. J Cell Sci 115: 3227-3234
2. Anderson P, Phillips K, Stoecklin G, Kedersha N (2004) Post-transcriptional regulation of pro-inflammatory proteins. J Leuk Biol, (in press)
3. Blackshear PJ (2002) Tristetraprolin and other CCCH tandem zinc-finger proteins in the regulation of mRNA turnover. Biochem Soc Trans 30: 945-952
4. Brooks SA, Connolly JE, Diegel RJ, Fava RA, Rigby WF (2002) Analysis of the function, expression, and subcellular distribution of human tristetraprolin. Arthritis Rheum 46: 1362-1370
5. Carballo E, Cao H, Lai WS, Kennington EA, Campbell D, Blackshear PJ (2001) Decreased sensitivity of tristetraprolin-deficient cells to p38 inhibitors suggests the involvement of tristetraprolin in the p38 signaling pathway. J Biol Chem 276: 42580-42587
6. Carballo E, Lai WS, Blackshear PJ (1998) Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science 281: 1001-1005
7. Chen C-YA, Shyu A-B (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci 20: 465-470
8. Chen CY, Gherzi R, Ong SE, Chan EL, Raijmakers R, Pruijn GJ, Stoecklin G, Moroni C, Mann M, Karin M (2001) AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107: 451-464
9. Chrestensen CA, Schroeder MJ, Shabanowitz J, Hunt DF, Pelo JW, Worthington MT, Sturgill TW (2004) MK2 phosphorylates tristetraprolin on in vivo sites including S178, a site required for 14-3-3 binding. J Biol Chem, (in press)
10. Civelli O, Vincent A, Maundrell K, Buri J, Scherrer K (1980) The translational repression of globin mRNA in free cytoplasmic ribonucleoprotein complexes. Eur J Biochem 107: 577-585
11. Clemens MJ (2001) Initiation factor eIF2 alpha phosphorylation in stress responses and apoptosis. Prog Mol Subcell Biol 27: 57-89
12. Fan XC, Steitz JA (1998) Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J 17: 3448-3460
13. Gaestel M (2002) sHsp-phosphorylation: enzymes, signaling pathways and functional implications. Prog Mol Subcell Biol 28: 151-169
14. Harding HP, Ron D (2002) Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes 51 (Suppl 3): S455-S461
15. Hinnebusch AG, Natarajan K (2002) Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryot Cell 1: 22-32
16. Johnson BA, Geha M, Blackwell TK (2000) Similar but distinct effects of the tristetraprolin/TIS11 immediate-early proteins on cell survival. Oncogene 19: 1657-1664
17. Johnson BA, Stehn JR, Yaffe MB, Blackwell TK (2002) Cytoplasmic localization of tristetraprolin involves 14-3-3-dependent and -independent mechanisms. J Biol Chem 277: 18029-18036
18. Kedersha N, Anderson P (2001) Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem Soc Trans 30: 963-969
19. Kedersha N, Chen S, Gilks N, Li W, Miller IJ, Stahl J, Anderson P (2002) Evidence that ternary complex (eIF2-GTP-tRNA(i)(Met))-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol Biol Cell 13: 195-210
20. Kedersha N, Cho MR, Li W, Yacono PW, Chen S, Gilks N, Golan DE, Anderson P (2000) Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J Cell Biol 151: 1257-1268
21. Kedersha NL, Gupta M, Li W, Miller I, Anderson P (1999) RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J Cell Biol 147: 1431-1442
22. Lai WS, Carballo E, Strum JR, Kennington EA, Phillips RS, Blackshear PJ (1999) Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol Cell Biol 19: 4311-4323
23. Mahtani KR, Brook M, Dean JL, Sully G, Saklatvala J, Clark AR (2001) Mitogen-activated protein kinase p38 controls the expression and posttranslational modification of tristetraprolin, a regulator of tumor necrosis factor alpha mRNA stability. Mol Cell Biol 21: 6461-6469
24. Ming XF, Kaiser M, Moroni C (1998) c-jun N-terminal kinase is involved in AUUUA-mediated interleukin-3 mRNA turnover in mast cells. EMBO J 17: 6039-6048
25. Ming XF, Stoecklin G, Lu M, Looser R, Moroni C (2001) Parallel and independent regulation of interleukin-3 mRNA turnover by phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase. Mol Cell Biol 21: 5778-5789
26. Nover L, Scharf KD, Neumann D (1989) Cytoplasmic heat shock granules are formed from precursor particles and are associated with a specific set of mRNAs. Mol Cell Biol 9: 1298-1308
27. Peng SS, Chen CY, Xu N, Shyu AB (1998) RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J 17: 3461-3470
28. Sheth U, Parker R (2003) Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300: 805-808
29. Stoecklin G, Colombi M, Raineri I, Leuenberger S, Mallaun M, Schmidlin M, Gross B, Lu M, Kitamura T, Moroni C (2002) Functional cloning of BRF1, a regulator of ARE-dependent mRNA turnover. EMBO J 21: 4709-4718
30. Stoecklin G, Ming XF, Looser R, Moroni C (2000) Somatic mRNA turnover mutants implicate tristetraprolin in the interleukin-3 mRNA degradation pathway. Mol Cell Biol 20: 3753-3763
31. Stoecklin G, Stoeckle P, Lu M, Muehlemann O, Moroni C (2001) Cellular mutants define a common mRNA degradation pathway targeting cytokine AU-rich elements. RNA 7: 1578-1588
32. Taylor GA, Carballo E, Lee DM, Lai WS, Thompson MJ, Patel DD, Schenkman DI, Gilkeson GS, Broxmeyer HE, Haynes BF, Blackshear PJ (1996) A pathogenetic role for TNF alpha in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency. Immunity 4: 445-454
33. Taylor GA, Thompson MJ, Lai WS, Blackshear PJ (1995) Phosphorylation of tristetraprolin, a potential zinc finger transcription factor, by mitogen stimulation in intact cells and by mitogen-activated protein kinase in vitro. J Biol Chem 270: 13341-13347
34. Tzivion G, Avruch J (2002) 14-3-3 proteins: active cofactors in cellular regulation by serine/threonine phosphorylation. J Biol Chem 277: 3061-3064
35. Waskiewicz AJ, Johnson JC, Penn B, Mahalingam M, Kimball SR, Cooper JA (1999) Phosphorylation of the cap-binding protein eukaryotic translation initiation factor 4E by protein kinase Mnk1 in vivo. Mol Cell Biol 19: 1871-1880
36. Winzen R, Kracht M, Ritter B, Wilhelm A, Chen CY, Shyu AB, Muller M, Gaestel M, Resch K, Holtmann H (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
37. Xu N, Loflin P, Chen CY, Shyu AB (1998) A broader role for AU-rich element-mediated mRNA turnover revealed by a new transcriptional pulse strategy. Nucleic Acids Res 26: 558-565
38. Yaffe MB, Rittinger K, Volinia S, Caron PR, Aitken A, Leffers H, Gamblin SJ, Smerdon SJ, Cantley LC (1997) The structural basis for 14-3-3: phosphopeptide binding specificity. Cell 91: 961-971
39. Zhu W, Brauchle MA, Di Padova F, Gram H, New L, Ono K, Downey JS, Han J (2001) Gene suppression by tristetraprolin and release by the p38 pathway. Am J Physiol Lung Cell Mol Physiol 281: L499-L508