Distinct domains of AU-rich elements exert different functions in mRNA destabilization and stabilization by p38 mitogen-activated protein kinase or HuR

Molecular and Cellular Biology

Volumn 24, Issue 11, 2004, Pages 4835-4847

  Winzen, Reinhard ^a   Gowrishankar, Gayatri ^a   Bollig, Frank ^a,b   Redich, Natalie ^a   Resch, Klaus ^a   Holtmann, Helmut ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; AU RICH ELEMENT; BETA GLOBIN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN D; HISTONE; HUR PROTEIN; INTERLEUKIN 8; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; POLYADENYLIC ACID; RNA; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; URACIL;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; GENE OVEREXPRESSION; HELA CELL; HUMAN; HUMAN CELL; ONCOGENE C FOS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STABILITY; STRUCTURE ACTIVITY RELATION;

3' UNTRANSLATED REGIONS; BASE SEQUENCE; HUMANS; INTERLEUKIN-8; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RNA, MESSENGER;

EID: 2442647813     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.11.4835-4847.2004     Document Type: Article

References (50)

1. Atasoy, U., S. L. Curry, I. Lopez De Silanes, A. B. Shyu, V. Casolaro, M. Gorospe, and C. Stellato. 2003. Regulation of eotaxin gene expression by TNF-α and IL-4 through mRNA stabilization: involvement of the RNA-binding protein HuR. J. Immunol. 171:4369-4378.
2. Bakheet, T., M. Frevel, B. R. Williams, W. Greer, and K. S. Khabar. 2001. ARED: human AU-rich element-containing mRNA database reveals an unexpectedly diverse functional repertoire of encoded proteins. Nucleic Acids Res. 29:246-254.
3. Bollig, F., R. Winzen, M. Gaestel, S. Kostka, K. Resch, and H. Holtmann. 2003. Affinity purification of ARE-binding proteins identifies polyA-binding protein 1 as a potential substrate in MK2-induced mRNA stabilization. Biochem. Biophys. Res. Commun. 301:665-670.
4. Bollig, F., R. Winzen, M. Kracht, B. Ghebremedhin, B. Ritter, A. Wilhelm, K. Resch, and H. Holtmann. 2002. Evidence for general stabilization of mRNAs in response to UV light. Eur. J. Biochem. 269:5830-5839.
5. Caput, D., B. Beutler, K. Hartog, R. Thayer, S. Brown-Shimer, and A. Cerami. 1986. Identification of a common nucleotide sequence in the 3′-untranslated region of mRNA molecules specifying inflammatory mediators. Proc. Natl. Acad. Sci. USA 83:1670-1674.
6. Chen, C.-Y., T.-M. Chen, and A.-B. Shyu. 1994. Interplay of two functionally and structurally distinct domains of the c-fos AU-rich element specifies its mRNA-destabilizing function. Mol. Cell. Biol. 14:416-426.
7. 2-terminal kinase pathway. Science 280:1945-1949.
8. Chen, C. Y., R. Gherzi, S. E. Ong, E. L. Chan, R. Raijmakers, G. J. Pruijn, G. Stoecklin, C. Moroni, M. Mann, and M. Karin. 2001. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107:451-464.
9. Chen, C. Y., and A. B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20:465-470.
10. Chen, C. Y., N. Xu, and A. B. Shyu. 2002. Highly selective actions of HuR in antagonizing AU-rich element-mediated mRNA destabilization. Mol. Cell. Biol. 22:7268-7278.
11. Couttet, P., M. Fromont-Racine, D. Steel, R. Pictet, and T. Grange. 1997. Messenger RNA deadenylylation precedes decapping in mammalian cells. Proc. Natl. Acad. Sci. USA 94:5628-5633.
12. Dean, J. L., M. Brook, A. R. Clark, and J. Saklatvala. 1999. p38 mitogen-activated protein kinase regulates cyclooxygenase-2 mRNA stability and transcription in lipopolysaccharide-treated human monocytes. J. Biol. Chem. 274:264-269.
13. Dean, J. L., S. J. Sarsfield, E. Tsounakou, and J. Saklatvala. 2003. p38 mitogen-activated protein kinase stabilizes mRNAs that contain cyclooxygenase-2 and tumor necrosis factor AU-rich elements by inhibiting deadenylation. J. Biol. Chem. 278:39470-39476.
14. Dean, J. L., R. Wait, K. R. Mahtani, G. Sully, A. R. Clark, and J. Saklatvala. 2001. The 3′ untranslated region of tumor necrosis factor alpha mRNA is a target of the mRNA-stabilizing factor HuR. Mol. Cell. Biol. 21:721-730.
15. Fan, X. C., and J. A. Steitz. 1998. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17:3448-3460.
16. Frevel, M. A., T. Bakheet, A. M. Silva, J. G. Hissong, K. S. Khabar, and B. R. Williams. 2003. p38 Mitogen-activated protein kinase-dependent and -independent signaling of mRNA stability of AU-rich element-containing transcripts. Mol. Cell. Biol. 23:425-436.
17. Gallouzi, I. E., and J. A. Steitz. 2001. Delineation of mRNA export pathways by the use of cell-permeable peptides. Science 294:1895-1901.
18. Gossen, M., and H. Bujard. 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA 89:5547-5551.
19. Kotlyarov, A., A. Neininger, C. Schubert, R. Eckert, C. Birchmeier, H. D. Volk, and M. Gaestel. 1999. MAPKAP kinase 2 is essential for LPS-induced TNF-α biosynthesis. Nat. Cell Biol. 1:94-97.
20. Kullmann, M., U. Gopfert, B. Siewe, and L. Hengst. 2002. ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5′ UTR. Genes Dev. 16:3087-3099.
21. Lagnado, C. A., C. Y. Brown, and G. J. Goodall. 1994. AUUUA is not sufficient to promote poly(A) shortening and degradation of an mRNA: the functional sequence within AU-rich elements may be UUAUUUA(U/A) (U/A). Mol. Cell. Biol. 14:7984-7995.
22. Lasa, M., K. R. Mahtani, A. Finch, G. Brewer, J. Saklatvala, and A. R. Clark. 2000. Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol. Cell. Biol. 20:4265-4274.
23. Levy, N. S., S. Chung, H. Furneaux, and A. P. Levy. 1998. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem. 273:6417-6423.
24. Ma, W. J., S. Cheng, C. Campbell, A. Wright, and H. Furneaux. 1996. Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein. J. Biol. Chem. 271:8144-8151.
25. Mahtani, K. R., M. Brook, J. L. E. Dean, G. Sully, J. Saklatvala, and A. R. Clark. 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.
26. Mazan-Mamczarz, K., S. Galban, I. Lopez de Silanes, J. L. Martindale, U. Atasoy, J. D. Keene, and M. Gorospe. 2003. RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc. Natl. Acad. Sci. USA 100:8354-8359.
27. 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.
28. Ming, X. F., G. Stoecklin, M. Lu, R. Looser, and C. Moroni. 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.
29. Miyazawa, K., A. Mori, H. Miyata, M. Akahane, Y. Ajisawa, and H. Okudaira. 1998. Regulation of interleukin-13-induced interleukin-6 gene expression in human fibroblast-like synoviocytes by p38 mitogen-activated protein kinase. J. Biol. Chem. 273:24832-24838.
30. Mukherjee, D., M. Gao, J. P. O'Connor, R. Raijmakers, G. Pruijn, C. S. Lutz, and J. Wilusz. 2002. The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements. EMBO J. 21:165-174.
31. Neininger, A., D. Kontoyiannis, A. Kotlyarov, R. Winzen, R. Eckert, H. D. Volk, H. Holtmann, G. Kollias, and M. Gaestel. 2002. MK2 targets AU-rich elements and regulates biosynthesis of tumor necrosis factor and interleukin-6 independently at different post-transcriptional levels. J. Biol. Chem. 277:3065-3068.
32. Neu-Yilik, G., N. H. Gehring, R. Thermann, U. Frede, M. W. Hentze, and A. E. Kulozik. 2001. Splicing and 3′ end formation in the definition of nonsense-mediated decay-competent human β-globin mRNPs. EMBO J. 20:532-540.
33. Peng, S. S., C. Y. Chen, N. Xu, and A. B. Shyu. 1998. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17:3461-3470.
34. Ridley, S. H., J. L. Dean, S. J. Sarsfield, M. Brook, A. R. Clark, and J. Saklatvala. 1998. A p38 MAP kinase inhibitor regulates stability of interleukin-1-induced cyclooxygenase-2 mRNA. FEBS Lett. 439:75-80.
35. Rodriguez-Pascual, F., M. Hausding, I. Ihrig-Biedert, H. Furneaux, A. P. Levy, U. Forstermann, and H. Kleinert. 2000. Complex contribution of the 3′-untranslated region to the expressional regulation of the human inducible nitric-oxide synthase gene. Involvement of the RNA-binding protein HuR. J. Biol. Chem. 275:26040-26049.
36. Rousseau, S., N. Morrice, M. Peggie, D. G. Campbell, M. Gaestel, and P. Cohen. 2002. Inhibition of SAPK2a/p38 prevents hnRNP A0 phosphorylation by MAPKAP-K2 and its interaction with cytokine mRNAs. EMBO J. 21:6505-6514.
37. Shaw, G., and R. Kamen. 1986. A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46:659-667.
38. Shyu, A. B., J. G. Belasco, and M. E. Greenberg. 1991. Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay. Genes Dev. 5:221-231.
39. Stoecklin, G., M. Lu, B. Rattenbacher, and C. Moroni. 2003. A constitutive decay element promotes tumor necrosis factor alpha mRNA degradation via an AU-rich element-independent pathway. Mol. Cell. Biol. 23:3506-3515.
40. Stoecklin, G., P. Stoeckle, M. Lu, O. Muehlemann, and C. Moroni. 2001. Cellular mutants define a common mRNA degradation pathway targeting cytokine AU-rich elements. RNA 7:1578-1588.
41. Tran, H., F. Maurer, and Y. Nagamine. 2003. Stabilization of urokinase and urokinase receptor mRNAs by HuR is linked to its cytoplasmic accumulation induced by activated mitogen-activated protein kinase-activated protein kinase 2. Mol. Cell. Biol. 23:7177-7188.
42. Wang, W., M. C. Caldwell, S. Lin, H. Furneaux, and M. Gorospe. 2000. HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO J. 19:2340-2350.
43. Wang, W., H. Furneaux, H. Cheng, M. C. Caldwell, D. Hutter, Y. Liu, N. Holbrook, and M. Gorospe. 2000. HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol. 20:760-769.
44. Wilson, T., and R. Treisman. 1988. Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by 3′ AU-rich sequences. Nature 336:396-399.
45. Winzen, R., S. Kafert, B. Preiss, H. A. Mylius-Spencker, K. Resch, and H. Holtmann. 1996. Interaction between the mRNA of the 55-kDa tumor necrosis factor receptor and cellular proteins. Possible involvement in post-transcriptional regulation of receptor expression. J. Biol. Chem. 271:13461-13467.
46. Winzen, R., M. Kracht, B. Ritter, A. Wilhelm, C. Y. Chen, A. B. Shyu, M. Muller, 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.
47. Xu, N., C. Y. Chen, and A. B. Shyu. 1997. Modulation of the fate of cytoplasmic mRNA by AU-rich elements: key sequence features controlling mRNA deadenylation and decay. Mol. Cell. Biol. 17:4611-4621.
48. Xu, N., P. Loflin, C. Y. Chen, and A. B. Shyu. 1998. A broader role for AU-rich element-mediated mRNA turnover revealed by a new transcriptional pulse strategy. Nucleic Acids Res. 26:558-565.
49. Yu, Y., and K. Chadee. 2001. The 3′-untranslated region of human interleukin-8 mRNA suppresses IL-8 gene expression. Immunology 102:498-505.
50. Zubiaga, A. M., J. G. Belasco, and M. E. Greenberg. 1995. The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation. Mol. Cell. Biol. 15:2219-2230.