Intracellular translation initiation factor levels in Saccharomyces cerevisiae and their role in cap-complex function

Molecular Microbiology

Volumn 46, Issue 2, 2002, Pages 531-544

  Von der Haar, Tobias ^a   McCarthy, John E G ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; HELICASE; INITIATION FACTOR; MESSENGER RNA; POLYCLONAL ANTIBODY; PROTEIN SUBUNIT; RECOMBINANT PROTEIN;

ARTICLE; BINDING AFFINITY; CELL LEVEL; CELL SIZE; COMPLEX FORMATION; CONTROLLED STUDY; FUNGAL CELL; FUNGAL STRAIN; FUNGUS GROWTH; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PROTEIN VARIANT; RABBIT; RIBOSOME; RIBOSOME SUBUNIT; SACCHAROMYCES CEREVISIAE; STOICHIOMETRY; TRANSLATION INITIATION; TRANSLATION REGULATION; YEAST CELL;

ANIMALS; EUKARYOTIC INITIATION FACTOR-4E; EUKARYOTIC INITIATION FACTORS; GENE EXPRESSION REGULATION, FUNGAL; NUCLEAR CAP-BINDING PROTEIN COMPLEX; PHOSPHOPROTEINS; PROTEIN BIOSYNTHESIS; RABBITS; RNA CAPS; RNA, VIRAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; FUNGI; ORYCTOLAGUS CUNICULUS; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0036428702     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2002.03172.x     Document Type: Article

References (70)

1. Altmann, M., Handschin, C., and Trachsel, H. (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., Krieger, M., and Trachsel, H. (1989) Nucleotide sequence of the gene encoding a 20 kDa protein associated with the cap binding protein eIF-4E from Saccharomyces cerevisiae. Nucleic Acids Res 17:7520.
3. Altmann, M., Schmitz, N., Berset, C., and Trachsel, H. (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. Asano, K., Phan, L., Anderson, J., and Hinnebusch, A.G. (1998) Complex formation by all five homologues of mammalian translation initiation factor 3 subunits from yeast Saccharomyces cerevisiae. J Biol Chem 273: 18573-18585.
5. Asano, K., Clayton, J., Shalev, A., and Hinnebusch, A.G. (2000) A multifactor complex of eukaryotic initiation factors, eIF1, eIF2, eIF3, eIF5, and initiator tRNA (Met) is an important translation initiation intermediate in vivo. Genes Dev 14:2534-2546.
6. Ashe, M.P., De Long, S.K., and Sachs, A.B. (2000) Glucose depletion rapidly inhibits translation initiation in yeast. Mol Biol Cell 11:833-848.
7. Belli, G., Gari, E., Aldea, M., and Herrero, E. (1998) Functional analysis of yeast essential genes using a promoter-substitution cassette and the tetracycline-regulatable dual expression system. Yeast 14:1127-1138.
8. Browning, K.S., Gallie, D.R., Hershey, J.W.B., Hinnebusch, A.G., Maitra, U., Merrick, W.C., and Norbury, C. (2001) Unified nomenclature for the subunits of eukaryotic initiation factor 3. Trends Biochem Sci 26:284.
9. Chaudhuri, J., Si, K., and Maitra, U. (1997) Function of eukaryotic translation initiation factor 1A (eIF1A) (formerly called eIF-4C) in initiation of protein synthesis. J Biol Chem 272:7883-7891.
10. Chaudhuri, J., Chowdhury, D., and Maitra, U. (1999) Distinct functions of eukaryotic translation initiation factors eIF1A and eIF3 in the formation of the 40 S ribosomal preinitiation complex. J Biol Chem 274:17975-17980.
11. Chu, S., DeRisi, J., Eisen, M., Mulholland, J., Botstein, D., Brown, P.O., and Herskowitz, I. (1998) The transcriptional program of sporulation in budding yeast. Science 282: 699-705.
12. Coppolecchia, R., Buser, P., Stotz, A., and Linder, P. (1993) A new yeast translation initiation factor suppresses a mutation in the eIF-4A RNA helicase. EMBO J 12:4005-4011.
13. de la Cruz, J., Iost, I., Kressler, D., and Linder, P. (1997) The p20 and Ded1 proteins have antagonistic roles in eIF4E-dependent translation in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 94:5201-5206.
14. de la Cruz, J., Kressler, D., and Linder, P. (1999) Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem Sci 24:192-198.
15. Danaie, P., Altmann, M., Hall, M.N., Trachsel, H., and Helliwell, S.B. (1999) CLN3 expression is sufficient to restore G1-to-S-phase progression in Saccharomyces cerevisiae mutants defective in translation initiation factor eIF4E. Biochem J 340:135-141.
16. Das, S., and Maitra, U. (2001) Functional significance and mechanism of eIF5-promoted GTP hydrolysis in eukaryotic translation initiation. Prog Nucleic Acid Res Mol Biol 70:207-231
17. Dombek, K.M., and Ingram, L.O. (1986) Determination of the intracellular concentration of ethanol in Saccharomyces cerevisiae during fermentation. Appl Environ Microbiol 51: 197-200.
18. Donahue, T.F., Cigan, A.M., Pabich, E.K., and Valavicius, B.C. (1988) Mutations at a Zn (II) finger motif in the yeast eIF-2 beta gene alter ribosomal start-site selection during the scanning process. Cell 54:621-632.
19. Dua, K., Williams, T.M., and Beretta, L. (2001) Translational control of the proteome: Relevance to cancer. Proteomics 1: 1191-1199.
20. Duncan, R., and Hershey, J.W.B. (1983) Identification and quantitation of levels of protein synthesis initiation factors in crude HeLa cell lysates by two-dimensional polyacrylamide gel electrophoresis. J Biol Chem 258: 7228-7235.
21. Duncan, R., Milburn, S.C., and Hershey, J.W.B. (1987) Regulated phosphorylation and low abundance of HeLa cell initiation factor eIF-4F suggest a role in translational control. Heat shock effects on eIF-4F. J Biol Chem 262:380-388.
22. Esteban, R., and Wickner, R.B. (1988) A deletion mutant of L-A double-stranded RNA replicates like M1 double-stranded RNA. J Virol 62:1278-1285.
23. Etchison, D., and Milburn, S. (1987) Separation of protein synthesis initiation factor eIF4A from a p220-associated cap binding complex activity. Mol Cell Biochem 76:15-25.
24. Etchison, D., Milburn, S.C., Edery, I., Sonenberg, N., and Hershey, J.W. (1982) Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the pro-teolysis of a 220,000-dalton polypeptide associated with eucaryotic initiation factor 3 and a cap binding protein complex. J Biol Chem 257:14806-14810.
25. Flynn, A., and Proud, C.G. (1995) Serine 209, not serine 53, is the major site of phosphorylation in initiation factor eIF4E in serum-treated Chinese hamster ovary cells. J Biol Chem 270:21684-21688.
26. Futcher, B., Latter, G.I., Monardo, P., McLaughlin, C.S., and Garrels, J.I. (1999) A sampling of the yeast proteome. Mol Cell Biol 19:7357-7368.
27. Goyer, C., Altmann, M., Lee, H.S., Blanc, A., Deshmukh, M., Woolford, J.L. Jr, Trachsel, H., and Sonenberg, N. (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.
28. von der Haar, T., Ball, P.D., and McCarthy, J.E.G. (2000) Stabilization of eukaryotic initiation factor 4E binding to the mRNA 5′-Cap by domains of eIF4G. J Biol Chem 275: 30551-30555.
29. von der Haar, T., Hughes, J.M.X., Karim, M.M., Ptushkina, M., and McCarthy, J.E.G. (2002) Translation initiation and surface plasmon resonance: New technology applied to old questions. Biochem Soc Trans 30:155-162.
30. Haghighat, A., Mader, S., Pause, A., and Sonenberg, N. (1995) Repression of cap-dependent translation by 4E-binding protein 1: Competition with p220 for binding to eukaryotic initiation factor-4E. EMBO J 14:5701-5709.
31. Hershey, J.W.B., and Merrick, W.C. (2000) The pathway and mechanism of eukaryotic protein synthesis. In Translational Control of Gene Expression Sonenberg, N., Hershey, J.W.B., and Mathews, M.B., (eds). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp. 33-88.
32. Hinnebusch, A.G. (1997) Translational regulation of yeast GCN4. A window on factors that control initiator-tRNA binding to the ribosome. J Biol Chem 272:21661-21664.
33. Holstege, F.C., Jennings, E.G., Wyrick, J.J., Lee, T.I., Hengartner, C.J., Green, M.R., Golub, T.R., Lander, E.S., and Young, R.A. (1998) Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95:717-728.
34. Kimball, S.R. (1999) Eukaryotic initiation factor eIF2. Int J Biochem Cell Biol 31:25-29.
35. Korneeva, N.L., Lamphear, B.J., Hennigan, F.L., and Rhoads, R.E. (2000) Mutually Cooperative Binding of eIF3 and eIF4A to Human eIF4G-1. J Biol Chem 275:41369-41376.
36. Kozak, M. (1978) How do eucaryotic ribosomes select initiation regions in messenger RNA? Cell 15:1109-1123.
37. Kozak, M. (1989) The scanning model for translation: An update. J Cell Biol 108:229-241.
38. Lang, V., Zanchin, N.I.T., Lunsdorf, H., Tuite, M., and McCarthy, J.E.G. (1994) Initiation factor eIF-4E of Saccharomyces cerevisiae. Distribution within the cell, binding to mRNA, and consequences of its overproduction. J Biol Chem 269:6117-6123.
39. Langlands, K., and Prochownik, E.V. (1997) A rapid method for the preparation of yeast lysates that facilitates the immunodetection of proteins generated by the yeast two-hybrid system. Anal Biochem 249:250-252.
40. Mathews, D.H., Sabina, J., Zuker, M., and Turner, D.H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288:911-940.
41. McCarthy, J.E.G. (1998) Posttranscriptional control of gene expression in yeast. Microbiol Mol Biol Rev 62:1492-1553.
42. Munro, H.N. (1990) Iron regulation of ferritin gene expression. J Cell Biochem 44:107-115.
43. Neff, C.L., and Sachs, A.B. (1999) Eukaryotic translation initiation factors 4G and 4A from Saccharomyces cerevisiae interact physically and functionally. Mol Cell Biol 19: 5557-5564.
44. Pause, A., Methot, N., Svitkin, Y., Merrick, W.C., and Sonenberg, N. (1994) Dominant negative mutants of mammalian translation initiation factor eIF-4A define a critical role for eIF-4F in cap-dependent and cap- independent initiation of translation. EMBO J 13:1205-1215.
45. Pavitt, G.D., Ramaiah, K.V., Kimball, S.R., and Hinnebusch, A.G. (1998) eIF2 independently binds two distinct eIF2B subcomplexes that catalyze and regulate guanine-nucleotide exchange. Genes Dev 12:514-526.
46. Pestova, T.V., and Hellen, C.U. (1999) Ribosome recruitment and scanning: What's new? Trends Biochem Sci 24:85-87.
47. Pestova, T.V., Lomakin, I.B., Lee, J.H., Choi, S.K., Dever, T.E., and Hellen, C.U. (2000) The joining of ribosomal subunits in eukaryotes requires eIF5B. Nature 403:332-335.
48. Pestova, T.V., Kolupaeva, V.G., Lomakin, I.B., Pilipenko, E.V., Shatsky, I.N., Agol, V.I., and Hellen, C.U. (2001) Molecular mechanisms of translation initiation in eukaryotes. Proc Natl Acad Sci USA 98:7029-7036.
49. Phan, L., Zhang, X., Asano, K., Anderson, J., Vornlocher, H.P., Greenberg, J.R., Qin, J., and Hinnebusch, A.G. (1998) Identification of a translation initiation factor 3 (eIF3) core complex, conserved in yeast and mammals, that interacts with eIF5. Mol Cell Biol 18:4935-4946.
50. Ptushkina, M., von der Haar, T., Vasilescu, S., Frank, R., Birkenhäger, R., and McCarthy, J.E.G. (1998) Cooperative modulation by eIF4G of eIF4E-binding to the mRNA 5′ cap in yeast involves a site partially shared by p20. EMBO J 17:4798-4808.
51. Rau, M., Ohlmann, T., Morley, S.J., and Pain, V.M. (1996) A reevaluation of the cap-binding protein, eIF4E, as a rate-limiting factor for initiation of translation in reticulocyte lysate. J Biol Chem 271:8983-8990.
52. Rozen, F., Edery, I., Meerovitch, K., Dever, T.E., Merrick, W.C., and Sonenberg, N. (1990) Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Mol Cell Biol 10:1134-1144.
53. Russo, G.L., van den Bos, C., Sutton, A., Coccetti, P., Baroni, M.D., Alberghina, L., and Marshak, D.R. (2000) Phosphorylation of Cdc28 and regulation of cell size by the protein kinase CKII in Saccharomyces cerevisiae. Biochem J 351:143-150.
54. Russo, G.L., van den Bos, C., and Marshak, D.R. (2001) Mutation at the CK2 phosphorylation site on Cdc28 affects kinase activity and cell size in Saccharomyces cerevisiae. Mol Cell Biochem 227:113-117.
55. Sachs, A.B., and Deardorff, J.A. (1992) Translation initiation requires the PAB-dependent poly (A) ribonuclease in yeast. Cell 70:961-973.
56. Sagliocco, F.A., Vega Laso, M.R., Zhu, D., Tuite, M.F., McCarthy, J.E., and Brown, A.J. (1993) The influence of 5′-secondary structures upon ribosome binding to mRNA during translation in yeast. J Biol Chem 268: 26522-26530.
57. Steinberg, T.H., Jones, L.J., Haugland, R.P., and Singer, V.L. (1996) SYPRO orange and SYPRO red protein gel stains: One-step fluorescent staining of denaturing gels for detection of nanogram levels of protein. Anal Biochem 239:223-237.
58. Strudwick, S., and Borden, K.L. (2002) The emerging roles of translation factor eIF4E in the nucleus. Differentiation 70:10-22.
59. Tarun, S.Z. Jr and Sachs, A.B. (1996) Association of the yeast poly (A) tail binding protein with translation initiation factor eIF-4G. EMBO J 15:7168-7177.
60. Tyson, C.B., Lord, P.G., and Wheals, A.E. (1979) Dependency of size of Saccharomyces cerevisiae cells on growth rate. J Bacteriol 138:92-98.
61. Vasilescu, S., Ptushkina, M., Linz, B., Muller, P.P., and McCarthy, J.E.G. (1996) Mutants of eukaryotic initiation factor eIF-4E with altered mRNA cap binding specificity reprogram mRNA selection by ribosomes inSaccharomy-ces cerevisiae. J Biol Chem 271:7030-7037.
62. Velasco, C.R., Vilela, C., Berthelot, K., and McCarthy, J.E.G. (2002) Modulation of eukaryotic mRNA stability via the cap-binding translation complex eIF4F. J Mol Biol 318: 951-962.
63. Vilela, C., Velasco, C., Ptushkina, M., and McCarthy, J.E.G. (2000) The eukaryotic mRNA decapping protein Dcp1 interacts physically and functionally with the eIF4F translation initiation complex. EMBO J 19:4372-4382.
64. Warner, J.R. (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24:437-440.
65. Watkins, S.J., and Norbury, C.J. (2002) Translation initiation and its deregulation during tumorigenesis. Br J Cancer 86: 1023-1027.
66. Webb, B.L., and Proud, C.G. (1997) Eukaryotic initiation factor 2B (eIF2B). Int J Biochem Cell Biol 29:1127-1131.
67. Yoder-Hill, J., Pause, A., Sonenberg, N., and Merrick, W.C. (1993) The p46 subunit of eukaryotic initiation factor (eIF) -4F exchanges with eIF-4A. J Biol Chem 268:5566-5573.
68. Yoon, H.J., and Donahue, T.F. (1992) The suil suppressor locus in Saccharomyces cerevisiae encodes a translation factor that functions during tRNA (iMet) recognition of the start codon. Mol Cell Biol 12:248-260.
69. Zanchin, N.I.T., and McCarthy, J.E.G. (1995) Characterization of the in vivo phosphorylation sites of the mRNA. Cap-binding complex proteins eukaryotic initiation factor-4E and p20 in Saccharomyces cerevisiae. J Biol Chem 270:26505-26510.
70. Zimmerman, S.B., and Trach, S.O. (1991) Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. J Mol Biol 222:599-620.