A quantitative model for mRNA translation in Saccharomyces cerevisiae

Yeast

Volumn 27, Issue 10, 2010, Pages 785-800

  You, Tao ^a   Coghill, George M ^a   Brown, Alistair J P ^b  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Eukaryotic translation initiation; Kinetic model; MRNA translation; Robustness

Indexed keywords

AMINO ACID; MESSENGER RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ELF 1; TRANSCRIPTION FACTOR ELF 3; TRANSCRIPTION FACTOR ELF 5; UNCLASSIFIED DRUG;

ARTICLE; CELL HETEROGENEITY; CELL POPULATION; GENE CONTROL; GENE EXPRESSION; KINETICS; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN MALNUTRITION; QUANTITATIVE ANALYSIS; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; TRANSLATION INITIATION;

GENE EXPRESSION REGULATION, FUNGAL; MODELS, BIOLOGICAL; PEPTIDE INITIATION FACTORS; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 78650347088     PISSN: 0749503X     EISSN: 10970061     Source Type: Journal    
DOI: 10.1002/yea.1770     Document Type: Article

References (56)

1. Acker MG, Shin BS, Dever TE, Lorsch JR. 2006. Interaction between eukaryotic initiation factors 1A and 5B is required for efficient ribosomal subunit joining. J Biol Chem 281(13): 8469-8475.
2. Algire MA, Maag D, Savio P, et al. 2002. Development and characterization of a reconstituted yeast translation initiation system. RNA 8(3): 382-397.
3. Arava Y, Boas FE, Brown PO, Herschlag D. 2005. Dissecting eukaryotic translation and its control by ribosome density mapping. Nucleic Acids Res 33(8): 2421-2432.
4. Arava Y, Wang Y, Storey JD, et al. 2003. Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 100(7): 3889-3894.
5. Asano K, Clayton J, Shalev A, Hinnebusch AG. 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(19): 2534-2546.
6. Asano K, Sachs MS. 2007. Translation factor control of ribosome conformation during start codon selection. Genes Dev 21: 1280-1287.
7. Bar-Even A, Paulsson J, Maheshri N, et al. 2006. Noise in protein expression scales with natural protein abundance. Nat Genet 38(6): 636-643.
8. Barkai N, Leibler S. 1997. Robustness in simple biochemical networks. Nature 387(6636): 913-917.
9. Bergmann JE, Lodish HF. 1979. A kinetic model of protein synthesis. J Biol Chem 254(23): 11927-11937.
10. Brockmann R, Beyer A, Heinisch JJ, Wilhelm T. 2007. Posttranscriptional expression regulation: what determines translation rates? PLoS Comp Biol 3(3): e57.
11. Campbell SG, Hoyle NP, Ashe MP. 2005. Dynamic cycling of eIF2 through a large eIF2B-containing cytoplasmic body: implications for translation control. J Cell Biol 170(6): 925-934.
12. Cherkasova VA, Hinnebusch AG. 2003. Translational control by TOR and TAP42 through dephosphorylation of eIF2α kinase GCN2. Genes Dev 17(7): 859-872.
13. Cheung Y-N, Maag D, Mitchell SF, et al. 2007. Dissociation of eIF1 from the 40S ribosomal subunit is a key step in start codon selection in vivo. Genes Dev 21: 1217-1230.
14. Colman-Lerner A, Gordon A, Serra E, et al. 2005. Regulated cell-to-cell variation in a cell-fate decision system. Nature 437(29): 699-706.
15. Delbecq P, Werner M, Feller A, et al. 1994. A segment of mRNA encoding the leader peptide of the CPA1 gene confers repression by arginine on a heterologous yeast gene transcript. Mol Cell Biol 14: 2378-2390.
16. Dholakia JN, Wahba AJ. 1989. Mechanism of the nucleotide exchange reaction in eukaryotic polypeptide chain initiation. Characterization of the guanine nucleotide exchange factor as a GTP-binding protein. J Biol Chem 264(1): 546-550.
17. Dimelow RJ, Wilkinson SJ. 2009. Control of translation initiation: a model-based analysis from limited experimental data. J R Soc Interface 6(30): 51-61.
18. Fell DA. 1997. Understanding the Control of Metabolism. Portland Press: London.
19. Ghaemmaghami S, Huh WK, Bower K, et al. 2003. Global analysis of protein expression in yeast. Nature 425(6959): 737-741.
20. Godefroy-Colburn T, Thach RE. 1981. The role of mRNA competition in regulating translation. IV. Kinetic model. J Biol Chem 256(22): 11762-11773.
21. Grant CM, Miller PF, Hinnebusch AG. 1994. Requirements for intercistronic distance and level of eukaryotic initiation factor 2 activity in reinitiation on GCN4 mRNA vary with the downstream cistron. Mol Cell Biol 14(4): 2616-2628.
22. Guth E, Connolly SH, Bovee M, Francklyn CSA. 2005. A substrate-assisted concerted mechanism for aminoacylation by a class II aminoacyl-tRNA synthetase. Biochemistry 44(10): 3785-3794.
23. Hans MA, Heinzle E, Wittmann C. 2003. Free intracellular amino acid pools during autonomous oscillations in Saccharomyces cerevisiae. Biotechnol Bioeng 82(2): 143-151.
24. Harley CB, Pollard JW, Stanners CP, Goldstein S. 1981. Model for messenger RNA translation during amino acid starvation applied to the calculation of protein synthetic error rates. J Biol Chem 256(21): 10786-10794.
25. Hinnebusch AG. 2005. Translational Regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol 59: 407-450.
26. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS. 2009. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324(5924): 218-223.
27. Jivotovskaya A, Valášek L, Hinnebusch AG, Nielsen KH. 2006. Eukaryotic translation initiation factor 3. eIF3. and eIF2 can promote mRNA binding to 40S subunits independently of eIF4G in yeast. Mol Cell Biol 26(4): 1355-1372.
28. Kacser H, Burns JA. 1973. The control of flux. Symp Soc Exper Biol 27: 65-104.
29. Kapp LD, Lorsch JR. 2004. The molecular mechanics of eukaryotic translation. Annu Rev Biochem 73: 657-704.
30. Kitano H. 2007. Towards a theory of biological robustness. Mol Syst Biol 3: 137.
31. Kuepfer L, Peter M, Sauer U, Stelling J. 2007. Ensemble modeling for analysis of cell signaling dynamics. Nat Biotechnol 25(9): 1001-1006.
32. Lu P, Vogel C, Wang R, et al. 2007. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat Biotechnol 25(1): 117-124.
33. MacKay VL, Li X, Flory MR, et al. 2004. Gene expression analyzed by high-resolution state array analysis and quantitative proteomics: response of yeast to mating pheromone. Mol Cell Proteom 3(5): 478-489.
34. Manchester KL. 2001. Catalysis of guanine nucleotide exchange on eIF2 by eIF2B: can it be both a substituted enzyme and a sequential mechanism? Biochem Biophys Res Commun 289(3): 643-646.
35. Marintchev A, Wagner G. 2004. Translation initiation: structures, mechanisms and evolution. Q Rev Biophys 37(3-4): 197-284.
36. Maag D, Lorsch JR. 2003. Communication between eukaryotic translation initiation factors 1 and 1A on the yeast small ribosomal subunit. J Mol Biol 330: 917-924.
37. Maag D, Fekete CA, Gryczynski Z, Lorsch JR. 2005. A conformational change in the eukaryotic translation preinitiation complex and release of eIF1 signal recognition of the start codon. Mol Cell 17(2): 265-275.
38. Newman JR, Ghaemmaghami S, Ihmels J, et al. 2006. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441(7095): 840-846.
39. Nika J, Yang W, Pavitt GD, et al. 2000. Purification and kinetic analysis of eIF2B from Saccharomyces cerevisiae. J Biol Chem 275(34): 26011-26017.
40. Passmore LA, Schmeing TM, Maag D, et al. 2007. The eukaryotic translation initiation factors eIF1 and eIF1A induce an open conformation of the 40S ribosome. Mol Cell 26: 41-50.
41. Paulsson J. 2005. Models of stochastic gene expression. Phys Life Rev 2: 157-175.
42. Reibarkh M, Yamamoto Y, Singh CR, et al. 2008. Eukaryotic initiation factor. eIF. 1 carries two distinct eIF5-binding faces important for multifactor assembly and AUG selection. J Biol Chem 283(2): 1094-1103.
43. Rosen AE, Brooks BS, Guth E, et al. 2006. Evolutionary conservation of a functionally important backbone phosphate group critical for aminoacylation of histidine tRNAs. RNA 12(7): 1315-1322.
44. Rowlands AG, Panniers R, Henshaw EC. 1988. The catalytic mechanism of guanine nucleotide exchange factor action and competitive inhibition by phosphorylated eukaryotic initiation factor 2. J Biol Chem 263(12): 5526-5533.
45. Runarsson TP, Yao X. 2005. Search biases in constrained evolutionary optimization. IEEE Transactions on Systems, Man, and Cybernetics 35(2): 233-243.
46. Sangthong P, Hughes J, McCarthy JEG. 2007. Distributed control for recruitment, scanning and subunit joining steps of translation initiation. Nucleic Acids Res 35(11): 3573-3580.
47. Singh CR, Lee B, Udagawa T, et al. 2006. An eIF5/eIF2 complex antagonizes guanine nucleotide exchange by eIF2B during translation initiation. EMBO J 25: 4537-4546.
48. Singh CR, Udagawa T, Lee B, et al. 2007. Change in nutritional status modulates the abundance of critical pre-initiation intermediate complexes during translation initiation in vivo. J Mol Biol 370: 315-330.
49. Singh CR, Yamamoto Y, Asano K. 2004. Physical association of eukaryotic initiation factor, eIF, 5-carboxyl-terminal domain with the lysine-rich eIF2β segment strongly enhances its binding to eIF3. J Biol Chem 279(48): 49644-49655.
50. Skjøndal-Bar N, Morris DR. 2007. Dynamic model of the process of translation in eukaryotic cells. Bull Math Biol 69: 361-393.
51. Valášek L, Nielsen KH, Zhang F, et al. 2004. Interactions of eukaryotic translation initiation factor 3, eIF3. Subunit NIP1/c with eIF1 and eIF5 promote preinitiation complex assembly and regulate start codon selection. Mol Cell Biol 24(21): 9437-9455.
52. Vilela C, Linz B, Rodrigues-Pousada C, McCarthy JEG. 1998. The yeast transcription factor genes YAP1 and YAP2 are subject to differential control at the levels of both translation and mRNA stability. Nucleic Acids Res 26: 1150-1159.
53. von der Haar T, Hughes JM, Manjarul Karim M, et al. 2002. Translation initiation and surface plasmon resonance: new technology applied to old questions. Biochem Soc Trans 30(2): 155-162.
54. von der Haar T, McCarthy JEG. 2002. Intracellular translation initiation factor levels in Saccharomyces cerevisiae and their role in cap-complex function. Mol Microbiol 2: 531-544.
55. Wullschleger S, Loewith R, Hall MN. 2006. TOR signaling in growth and metabolism. Cell 124(3): 471-484.
56. You T, Coghill GM, Brown AJP. 2007. A Quantitative model for the translational control of GCN4 in yeast. 2nd Foundations of Systems Biology in Engineering Conference Proceedings, Stuttgart; 121-126.