Mutations in translation initiation factors lead to increased rates of deadenylation and decapping of mRNAs in Saccharomyces cerevisiae

Molecular and Cellular Biology

Volumn 19, Issue 8, 1999, Pages 5247-5256

  Schwartz, David C ^a   Parker, Roy ^a,b  

^a The University of Arizona   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPPED RNA; CIS ACTING ELEMENT; INITIATION FACTOR; MESSENGER RNA;

ARTICLE; GENE MUTATION; HALF LIFE TIME; NONHUMAN; PRIORITY JOURNAL; RNA METABOLISM; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; TRANSLATION INITIATION; TRANSLATION REGULATION;

SACCHAROMYCES CEREVISIAE;

EID: 0032778953     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.8.5247     Document Type: Article

References (55)

1. Altmann, M., C. Handschin, and H. Trachsel. 1987. mRNA cap-binding protein: cloning of the gene encoding protein synthesis initiation factor eIF-4E from Saccharomyces cerevisiae. Mol. Cell. Biol. 7:998-1003.
2. Altmann, M., N. Sonenberg, and H. Trachsel. 1989. Translation in Saccharomyces cerevisiae. Initiation factor 4E-dependent cell-free system. Mol. Cell. Biol. 9:4467-4472.
3. Altmann, M., N. Schmitz, C. Berset, and H. Trachsel. 1997. A novel inhibitor of cap-dependent translation initiation in yeast: p20 competes with eIF4G for binding to eIF4E. EMBO J. 16:1114-1121.
4. Anderson, J. S. J., and R. Parker. 1998. The 3′ to 5′ degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SK12 DEVH box protein and 3′ to 5′ exonucleases of the exosome complex. EMBO J. 17:1497-1506.
5. Banerjee, A. K. 1980. 5′-terminal cap structure in eucaryotic messenger ribonucleic acids. Bacteriol. Rev. 44:175-205.
6. Barnes, C. A. 1998. Upf1 and Upf2 proteins mediate normal yeast mRNA degradation when translation initiation is limited. Nucleic Acids Res. 26: 2433-2441.
7. Bashkirov, V. I., H. Scherthan, J. A. Solinger, J. Buerstedde, and W. Heyer. 1997. A mouse cytoplasmic exoribonuclease (mXRN1p) with preference for G4 tetraplex substrates. J. Cell Biol. 136:761-773.
8. Beelman, C. A., and R. Parker. 1994. Differential effects of translational inhibition in cis and trans on the decay of the unstable yeast MFA2 mRNA. J. Biol. Chem. 269:9687-9692.
9. Beelman, C. A., and R. Parker. 1995. Degradation of mRNA in eukaryotes. Cell 81:179-183.
10. 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 the normal rates of mRNA turnover. Nature 382:642-646.
11. Bernstein, P., S. W. Peltz, and J. Ross. 1989. The poly(A)-poly(A)-binding protein complex is a major determinant of mRNA stability in vitro. Mol. Cell. Biol. 9:659-670.
12. Binder, R., J. A. Horowitz, J. P. Basilion, D. M. Koeller, R. D. Klausner, and J. B. Harford. 1994. Evidence that the pathway of transferrin receptor mRNA degradation involves an endonucleolytic cleavage within the 3′ UTR and does not involve poly(A) tail shortening. EMBO J. 13:1969-1980.
13. Caponigro, G., D. Muhlrad, and R Parker. 1993. A small segment of the MATα1 transcript promotes mRNA decay in Saccharomyces cerevisiae. A stimulatory role for rare codons. Mol. Cell. Biol. 13:5141-5148.
14. Caponigro, G., and R. Parker. 1995. Multiple functions for the poly(A)-binding protein in mRNA decapping and deadenylation in yeast. Genes Dev. 9:2421-2432.
15. Caponigro, G., and R. Parker. 1996. Mechanisms and control of mRNA turnover in Saccharomyces cerevisiae. Microbiol. Rev. 60:233-249.
16. Cereghino, G. P., D. P. Atencio, M. Saghbini, J. Beiner, and I. E. Scheffler. 1995. Glucose-dependent turnover of the mRNAs encoding succinate dehydrogenase peptides in Saccharomyces cerevisiae: sequence elements in the 5′ untranslated region of the Ip mRNA play a dominant role. Mol. Biol. Cell 6:1125-1143.
17. 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.
18. Decker, C. J., and R. Parker. 1993. A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev. 7:1632-1643.
19. Edery, I., M. Humbelin, A. Darveau, K. A. Lee, S. Milburn, J. W. Hershey, H. Trachsel, and N. Sonenberg. 1983. Involvement of eukaryotic initiation factor 4A in the cap recognition process. J. Biol. Chem. 258:11398-11403.
20. Evans, D. R. H., C. Rasmussen, P. J. Hanic-Joyce, G. C. Johnston, R. A. Singer, and C. A. Barnes. 1995. Mutational analysis of the PRT1 protein subunit of yeast translation initiation factor 3. Mol. Cell. Biol. 15:4525-4535.
21. Garcia-Barrio, M. T., T. Naranda, C. R. Vazquez de Aldana, R. Cuesta, A. G. Hinnebusch, J. W. B. Hershey, and M. Tamame. 1995. GCD10, a translational repressor of GCN4, is the RNA-binding subunit of eukaryotic translation initiation factor-3. Genes Dev. 9:1781-1796.
22. Goyer, C., M. Altmann, H. Trachsel, and N. Sonenberg. 1989. Identification and characterization of cap-binding proteins from yeast. J. Biol. Chem. 264:7603-7610.
23. Goyer, C., M. Altmann, H. S. Lee, A. Blanc, M. Deshmukh, J. L. Woolford, Jr., H. Trachsel, and N. Sonenberg. 1993. TIF4631 and TIF4632. Two yeast genes encoding the high-molecular-weight subunits of the cap-binding protein complex (eukaryotic initiation factor 4F) contain an RNA recognition motif-like sequence and carry out an essential function. Mol. Cell. Biol. 13:4860-4874.
24. Grifo, J. A., S. M. Tahara, M. A. Morgan, A. J. Shatkin, and W. C. Merrick. 1983. New initiation factor activity required for globin mRNA translation. J. Biol. Chem. 258:5804-5810.
25. Hannig. E. M. 1995. Protein synthesis in eukaryotic organisms: new insights into the function of translation initiation factor eIF-3. Bioessays 17:915-919.
26. Hatfield, L., C. A. Beelman, A. Stevens, and R. Parker. 1996. Mutations in trans-acting factors affecting mRNA decapping in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:5830-5838.
27. Herrick, D., R. Parker, and A. Jacobson. 1990. Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol. Cell. Biol. 10:2269-2284.
28. Hsu, C. L., and A. Stevens. 1993. Yeast cells lacking 5′→3′ exoribonuclease 1 contain mRNA species that are poly(A) deficient and partially lack the 5′ cap structure. Mol. Cell. Biol. 13:4826-4835.
29. Jacobson, A., and S. W. Peltz. 1996. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu. Rev. Biochem. 65:693-739.
30. 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.
31. LaGrandeur, T., and R. Parker. 1999. The context of the translation start codon, in combination with other mRNA features, contributes to mRNA decay rates in Saccharomyces cerevisiae. RNA 5:420-433.
32. Laird-Offringa, I. A., C. L. De Witt, P. Elfferich, and A. J. van der Eb. 1990. Poly(A) tail shortening is the translation-dependent step in c-myc mRNA degradation. Mol. Cell. Biol. 10:6132-6140.
33. Lamphear, B. J., R. Kirchweger, T. Skern, and R. E. Rhoads. 1995. Mapping of functional domains in eIF4G with picornaviral proteases. Implication for cap-dependent and cap-independent translational initiation. J. Biol. Chem. 270:21975-21983.
34. Lanker, S., P. P. Müller, M. Altmann, C. Goyer, N. Sonenberg, and H. Trachsel. 1992. Interactions of the eIF-4F subunits in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 267:21167-21171.
35. Le, H., R. L. Tanguay, M. L. Balasta, C. Wei, K. S. Browning, A. M. Metz, D. J. Goss, and D. R. Gallie. 1997. Translation initiation factors eIF-iso4G and eIF-4B interact with the poly(A)-binding protein and increase its RNA binding activity. J. Bio. Chem. 272:16247-16255.
36. Leeds, P., J. M. Wood, B.-S. Lee, and M. R. Culbertson. 1992. Gene products that promote mRNA turnover in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:2165-2177.
37. Linz, B., N. Koloteva, S. Vasilescu, and J. E. G. McCarthy. 1997. Disruption of ribosomal scanning on the 5′-untranslated region, and not restriction of translational initiation per se, modulates the stability of nonaberrant mRNAs in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 272:9131-9140.
38. Mader, S., H. Lee, A. Pause, and N. Sonenberg. 1995. The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4γ and the translational repressors, 4E-binding proteins. Mol. Cell. Biol. 15:4990-4997.
39. Muckenthaler, M., N. Gunkel, R. Stripecke, and M. W. Hentze. 1997. Regulated poly(A) tail shortening in somatic cells mediated by cap-proximal translational repressor proteins and ribosome association. RNA 3:983-995.
40. Muhlrad, D., and R. Parker. 1992. Mutations affecting stability and deadenylation of the yeast MFA2 transcript. Genes Dev. 6:2100-2111.
41. 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′ to 3′ digestion of the transcript. Genes Dev. 8:855-866.
42. Muhlrad, D., C. J. Decker, and R. Parker. 1995. Turnover mechanisms of the stable yeast PCK1 mRNA. Mol. Cell. Biol. 15:2145-2156.
43. Naranda, T., S. E. MacMillan, and J. W. B. Hershey. 1994. Purified yeast translation factor eIF3 is an RNA-binding protein complex that contains the PRT1 protein. J. Biol. Chem. 269:32286-32292.
44. Rhoads, R. E. 1988. Cap recognition and entry of mRNA into the protein synthesis initiation cycle. Trends Biochem. Sci. 13:52-56.
45. Ross, J. 1995. mRNA stability in mammalian cells. Microbiol. Rev. 59:423-450.
46. Sachs, A. B., and R. W. Davis. 1989. The poly(A) binding protein is required for poly(A) shortening and 60S ribosomal subunit-dependent translation initiation. Cell 58:857-867.
47. Schmid, S. R., and P. Linder. 1991. Translation initiation factor 4A from Saccharomyces cerevisiae. Analysis of residues conserved in the D-E-A-D family of RNA helicases. Mol. Cell. Biol. 11:3463-3471.
48. 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. 5:221-234.
49. Sonenberg, N., M. A. Morgan, W. C. Merrick, and A. J. Shatkin. 1978. A polypeptide in eukaryotic initiation factors that crosslinks specifically to the 5′-terminal cap in mRNA. Proc. Natl. Acad. Sci. USA 75:4843-4847.
50. Tarun, S., 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.
51. Tharun, S., and R. Parker. 1999. Analysis of mutations in the yeast mRNA decapping enzyme. Genetics 15:1273-1285.
52. Vreken, P., and H. A. Raue. 1992. The rate-limiting step in yeast PGK1 mRNA degradation is an endonucleolytic cleavage in the 3′-terminal part of the coding region. Mol. Cell. Biol. 12:2986-2996.
53. Wilson, T., and R. Triesman. 1988. Removal of poly(A) and consequent degradation of the c-fos mRNA facilitated by 3′ AU-rich sequences. Nature 336:396-399.
54. Wormington, M., A. M. Searfoss, and C. A. Hurney. 1996. Overexpression of poly(A) binding protein prevents maturation-specific deadenylation and translational inactivation in Xenopus oocytes. EMBO J. 15:900-909.
55. Zuk, D., and A. Jacobson. 1998. A single amino acid substitution in yeast eIF-5A results in mRNA stabilization. EMBO J. 17:2914-2925.