p38 mitogen-activated protein kinase/Hog1p regulates translation of the AU-rich-element-bearing MFA2 transcript

Molecular and Cellular Biology

Volumn 25, Issue 22, 2005, Pages 9753-9763

  Vasudevan, Shobha ^a,b   Garneau, Nicole ^a   Khounh, Danny Tu ^a   Peltz, Stuart W ^a  

^a UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

^b YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; HU ANTIGEN; INITIATION FACTOR 4G; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE HOG1P; MITOGEN ACTIVATED PROTEIN KINASE P38; NUCLEIC ACID BINDING PROTEIN; POLYADENYLIC ACID BINDING PROTEIN; PROTEIN PUB1P; PROTEIN TIA 1; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; AU RICH ELEMENT; CONTROLLED STUDY; DNA STRUCTURE; FUNGAL GENE; FUNGAL STRAIN; FUNGUS GROWTH; GENE REPRESSION; GENETIC CONSERVATION; MFA2 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PUB1 GENE; REPORTER GENE; RNA STABILITY; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TRANSLATION REGULATION;

3' UNTRANSLATED REGIONS; CARBON; CROSS-LINKING REAGENTS; DNA; FUNGAL PROTEINS; GENE EXPRESSION REGULATION; GENES, FUNGAL; GENES, REPORTER; GENOTYPE; GLUCOSE; GLYCEROL; LIPOPROTEINS; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHEROMONES; PLASMIDS; POLY(A)-BINDING PROTEINS; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 27644541470     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.22.9753-9763.2005     Document Type: Article

References (57)

1. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 2001. Current protocols in molecular biology, vol. 2, p. 13.1-13.13. John Wiley and Sons, New York, N.Y.
2. Bollig, F., R. Winzen, M. Gaestel, S. Kostka, K. Resch, and H. Holtmann. 2003. Affinity purification of ARE-binding proteins identifies poly(A)-binding protein 1 as a potential substrate in MK2-induced mRNA stabilization. Biochem. Biophys. Res. Commun. 301:665-670.
3. Chen, C. Y., and A. B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20:465-470.
4. Czaplinski, K., M. J. Ruiz-Echevarria, S. V. Paushkin, X. Han, Y. Weng, H. A. Perlick, H. C. Dietz, M. D. Ter-Avanesyan, and S. W. Peltz. 1998. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev. 12:1665-1677.
5. Ernst, T. J., A. R. Ritchie, G. D. Demetri, and J. D. Griffin. 1989. Regulation of granulocyte- and monocyte-colony stimulating factor mRNA levels in human blood monocytes is mediated primarily at a post-transcriptional level. J. Biol. Chem. 264:5700-5703.
6. Gallouzi, I. E., C. M. Brennan, M. G. Stenberg, M. S. Swanson, A. Eversole, N. Maizels, and J. A. Steitz. 2000. HuR binding to cytoplasmic mRNA is perturbed by heat shock. Proc. Natl. Acad. Sci. USA 97:3073-3078.
7. Gallouzi, I. E., and J. A. Steitz. 2001. Delineation of mRNA export pathways by the use of cell-permeable peptides. Science 294:1895-1901.
8. Gavin, A. C., M. Bosche, R. Krause, P. Grandi, M. Marzioch, A. Bauer, J. Schultz, J. M. Rick, A. M. Michon, C. M. Cruciat, M. Remor, C. Hofert, M. Schelder, M. Brajenovic, H. Ruffner, A. Merino, K. Klein, M. Hudak, D. Dickson, T. Rudi, V. Gnau, A. Bauch, S. Bastuck, B. Huhse, C. Leutwein, M. A. Heurtier, R. R. Copley, A. Edelmann, E. Querfurth, V. Rybin, G. Drewes, M. Raida, T. Bouwmeester, P. Bork, B. Seraphin, B. Kuster, G. Neubauer, and G. Superti-Furga. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415:141-147.
9. Graft, G., I. Sela, and G. Galili. 1993. Translational regulation of human beta Interferon mRNA: association of the 3′ AU-rich sequence with the poly(A) tail reduces translation efficiency in vitro. Mol. Cell. Biol. 13:3487-3493.
10. Gray, N. K., and M. Wickens. 1998. Control of translation initiation in animals. Annu. Rev. Cell Dev. Biol. 14:399-458.
11. Gray, N. K., J. M. Coller, K. S. Dickson, and M. Wickens. 2000. Multiple portions of poly(A)-binding protein stimulate translation in vivo. EMBO J. 19:4723-4733.
12. Greenberg, M. E., A. B. Shyu, and J. G. Belasco. 1990. Deadenylylation: a mechanism controlling c-fos mRNA decay. Enzyme 44:181-192.
13. Grigull, J., S. Mnaimneh, J. Pootoolal, M. D. Robinson, and T. R. Hughes. 2004. Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol. Cell. Biol. 24:5534-5547.
14. Gueydan, C., L. Droogmans, P. Chalon, G. Huez, D. Caput, and V. Kruys. 1999. Identification of TIAR as a protein binding to the translational regulatory AU-rich element of tumor necrosis factor alpha mRNA. J. Biol. Chem. 274:2322-2326.
15. Hagan, K. W., M. J. Ruiz-Echevarria, Y. Quan, and S. W. Peltz. 1995. Characterization of cis-acting sequences and decay intermediates involved in nonsense-mediated mRNA turnover. Mol. Cell. Biol. 15:809-823.
16. Hilleren, P., and R. Parker. 1999. Mechanisms of mRNA surveillance in eukaryotes. Annu. Rev. Genet. 33:229-260.
17. Ho, Y., A. Gruhler, A. Heilbut, G. D. Bader, L. Moore, S. L. Adams, A. Millar, P. Taylor, K. Heimelt, K. Boutilier, L. Yang, C. Wolting, L. Donaldson, S. Schandorff, J. Shewnarane, M. Vo, J. Taggart, M. Goudreault, B. Muskat, C. Alfarano. D. Dewar, Z. Lin, K. Michalickova, A. R. Willems, H. Sassi, P. A. Nielsen, K. J. Rasmussen, J. R. Andersen, L. E. Johansen, L. H. Hansen, H. Jespersen, A. Podtelejnikov, E. Nielsen, J. Crawford, V. Poulsen, B. D. Sorensen, J. Matthiesen, R. C. Hendrickson, F. Gleeson, T. Pawson, M. F. Moran, D. Durocher, M. Mann, C. W. Hogue, D. Figeys, and M. Tyers. 2002. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415:180-183.
18. Iizuka, N., and P. Sarnow. 1997. Translation-competent extracts from Saccharomyces cerevisiae: effects of L-A RNA, 5′ cap, and 3′ poly(A) tail on translational efficiency of mRNAs. Methods 11:353-360.
19. Jarzembowski, J. A., and J. S. Malter. 1997. Cytoplasmic fate of eukaryotic mRNA: identification and characterization of AU-binding proteins. Prog. Mol. Subcell. Biol. 18:141-172.
20. Johnson, G. L., and R. Lapadat. 2002. Mitogen-activated protein kinase pathways mediated by ERK, JNK and p38 protein kinases. Science 298:1911-1912.
21. Kedersha, N., and P. Anderson. 2001. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30:963-969.
22. Kedersha, N., M. R. Cho, W. Li, P. W. Yacono, S. Chen, N. Gilks, D. E. Golan, and P. Anderson. 2000. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151:1257-1268.
23. Kessler, S. H., and A. B. Sachs. 1998. RNA recognition motif 2 of yeast Pab1p is required for its functional interaction with eukaryotic translation initiation factor 4G. Mol. Cell. Biol. 18:51-57.
24. Koeffler, H. P., J. Gasson, and A. Tobler. 1988. Transcriptional and posttranscriptional modulation of myeloid colony-stimulating factor expression by tumor necrosis factor and other agents. Mol. Cell. Biol. 8:3432-3438.
25. Kontoyiannis, D., A. Kotlyarov, E. Carballo, L. Alexopoulou, P. J. Blackshear, M. Gaestel, R. Davis, R. Flaveli, and G. Kollias. 2001. Interleukin-10 targets p38 MAPK to modulate ARE-dependent TNF mRNA translation and limit intestinal pathology. EMBO J. 20:3760-3770.
26. Kozlov, G., J. F. Trempe, K. Khaleghpour, A. Kahvejian, I. Ekiel, and K. Gehring. 2001. Structure and function of the C-terminal PABC domain of human poly(A)-binding protein. Proc. Natl. Acad. Sci. USA 98:4409-4413.
27. Kruys, V., O. Marinx, G. Shaw, J. Deschamps, and G. Huez. 1989. Translational blockade imposed by cytokine-derived UA-rich sequences. Science 245:852-855.
28. Kuyumcu-Martinez, N. M., M. E. Van Eden, P. Younan, and R. E. Lloyd. 2004. Cleavage of poly(A)-binding protein by poliovirus 3C protease inhibits host cell translation: a novel mechanism for host translation shutoff. Mol. Cell. Biol. 24:1779-1790.
29. Mangus, D. A., N. Amrani, and A. Jacobson. 1998. Pbp1p, a factor interacting with Saccharomyces cerevisiae poly(A)-binding protein, regulates polyadenylation. Mol. Cell. Biol. 18:7383-7396.
30. Mangus, D. A., M. C. Evans, and A. Jacobson. 2003. Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol. 4:223.
31. McCarthy, J. E. G. 1998. Posttranscriptional control of gene expression in yeast. Microbiol. Mol. Biol. Rev. 62:1492-1553.
32. Melo, E. O., R. Dhalia, C. Martins de Sa, N. Standart, and O. P. de Melo Neto. 2003. Identification of a C-terminal poly(A)-binding protein (PABP)-PABP interaction domain: role in cooperative binding to poly(A) and efficient cap distal translational repression. J. Biol. Chem. 278:46357-46368.
33. Mijatovic, T., V. Kruys, D. Caput, P. Defrance, and G. Huez. 1997. Interleukin-4 and -13 inhibit tumor necrosis factor-alpha mRNA translational activation in lipopolysaccharide-induced mouse macrophages. J. Biol. Chem. 272:14394-14398.
34. Muhlrad, D., C. J. Decker, and R. Parker. 1994. Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5′→3′ digestion of the transcript. Genes Dev. 8:855-866.
35. Muhlrad, D., and R. Parker. 1992. Mutations affecting stability and deadenylation of the yeast MFA2 transcript. Genes Dev. 6:2100-2111.
36. Munro, D., and A. Jacobson. 1990. Tales of poly(A): a review. Gene 91:151-158.
37. Myer, V. E., X. C. Fan, and J. A. Steitz. 1997. Identification of HuR as a protein implicated in AUUUA-mediated mRNA decay. EMBO J. 16:2130-2139.
38. 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.
39. Peltz, S. W., and A. Jacobson. 1993. mRNA turnover in Saccharomyces cerevisiae. Control of messenger RNA stability, p. 291-328. In J. Belasco and G. Brawerman (ed.), Control of messenger RNA stability. Academic Press, Inc., San Diego, Calif.
40. Philippsen, P., A. Stotz, and C. Scherf. 1991. DNA of Saccharomyces cerevisiae. Methods Enzymol. 194:169-182.
41. Piecyk, M., S. Wax, A. R. P. Beck, N. Kedersha, M. Gupta, B. Maritim, S. Chen, C. Gueydan, V. Kruys, M. Streuli, and P. Andersen. 2000. TIA-1 is a translational silencer that selectively regulates the expression of TNF-α. EMBO J. 19:4154-4163.
42. Ruiz-Echevarria, M. J., R. Munshi, J. Tomback, T. G. Kinzy, and S. W. Peltz. 2001. Characterization of a general stabilizer element that blocks deadenylation-dependent mRNA decay. J. Biol. Chem. 276:30995-31003.
43. Sachs, A. B., M. W. Bond, and R. D. Kornberg. 1986. A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: domain structure and expression. Cell 45:827-835.
44. Schuler, G. D., and M. D. Cole. 1988. GM-CSF and oncogene mRNA stabilities are independently regulated in trans in a mouse monocytic tumor. Cell 55:1115-1122.
45. Shei, G.-J., and J. R. Broach. 1995. Yeast silencers can act as orientation-dependent gene inactivation centers that respond to environmental signals. Mol. Cell. Biol. 15:3496-3506.
46. Sladic, R. T., C. A. Lagnado, C. J. Bagley, and G. Goodall. 2004. Human PABP binds AU-rich RNA via RNA-binding domains 3 and 4. Eur. J. Biochem. 271:450-457.
47. Tarun, S. Z. J., and A. B. Sachs. 1996. Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J. 15: 7168-7177.
48. Uchida, N., S. Hoshino, H. Imataka, N. Sonenberg, and T. Katada. 2002. A novel role of the mammalian GSPT/eRF3 associating with poly(A)-binding protein in Cap/poly(A)-dependent translation. J. Biol. Chem. 277:50286-50292.
49. Vasudevan, S., and S. W. Peltz. 2001. Regulated ARE-mediated mRNA decay in Saccharomyces cerevislae. Mol. Cell 7:1191-1200.
50. Voeltz, G. K., J. Ongkasuwan, N. Standart, and J. A. Steitz. 2001. A novel embryonic poly(A) binding protein, ePAB, regulates mRNA deadenylation in Xenopus egg extracts. Genes Dev. 15:774-788.
51. Wells, S. E., P. E. Hillner, R. D. Vale, and A. B. Sachs. 1998. Circularization of mRNA by eukaryotic translation initiation factors. Mol. Cell 2:135-140.
52. Wiklund, L., M. Sokolowski, A. Carlsson, M. Rush, and S. Schwartz. 2002. Inhibition of translation by UAUUUAU and UAUUUUUAU motifs of the AU-rich RNA instability element in the HPV-1 late 3′ untranslated region. J. Biol. Chem. 277:40462-40471.
53. 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.
54. Wilusz, C. J., M. Gao, C. L. Jones, J. Wilusz, and S. W. Peltz. 2001. Poly(A)-binding proteins regulate both mRNA deadenylation and decapping in yeast cytoplasmic extracts. RNA 7:1416-1424.
55. Winzeler, E. A., D. D. Shoemaker, A. Astromoff, H. Liang, K. Anderson, B. Andre, R. Bangham, R. Benito, J. D. Boeke, H. Bussey, A. M. Chu, C. Connelly, K. Davis, F. Dietrich, S. W. Dow, M. El Bakkoury, F. Foury, S. H. Friend, E. Gentalen, G. Giaever, J. H. Hegemann, T. Jones, M. Laub, H. Liao, N. Liebundguth, D. J. Lockhart, A. Lucau-Danila, M. Lussier, N. M'Rabet, P. Menard, M. Mittmann, C. Pai, C. Rebischung, J. L. Revuelta, L. Riles, C. J. Roberts, P. Ross-MacDonald, B. Scherens, M. Snyder, S. Sookhai-Mahadeo, R. K. Storms, S. Veronneau, M. Voet, G. Volckaert, T. R. Ward, R. Wysocki, G. S. Yen, K. Yu, K. Zimmermann, P. Philippsen, M. Johnston, and R. W. Davis. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285:901-906.
56. 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.
57. Zhang, T., V. Kruys, G. Huez, and C. Gueydan. 2001. AU-rich element-mediated translational control: complexity and multiple activities of trans-activating factors. Biochem. Soc. Trans. 30:952-958.