Yeast initiator tRNA identity elements cooperate to influence multiple steps of translation initiation

RNA

Volumn 12, Issue 5, 2006, Pages 751-764

  Kapp, Lee D ^a   Kolitz, Sarah E ^a   Lorsch, Jon R ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Identity elements; Initiator tRNA; Mechanism; Protein synthesis; T loop; Translation

Indexed keywords

CYTOSINE; GUANINE; GUANOSINE TRIPHOSPHATE; INITIATION FACTOR 2; MESSENGER RNA; TRANSFER RNA;

ANTICODON; ARTICLE; BASE PAIRING; CONFORMATIONAL TRANSITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RIBOSOME; RIBOSOME SUBUNIT; RNA BINDING; START CODON; THERMODYNAMICS; TRANSLATION INITIATION; YEAST;

BASE SEQUENCE; CONSERVED SEQUENCE; EUKARYOTIC INITIATION FACTOR-1; EUKARYOTIC INITIATION FACTOR-2; EUKARYOTIC INITIATION FACTOR-5; EUKARYOTIC INITIATION FACTORS; GUANOSINE TRIPHOSPHATE; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PROTEIN BIOSYNTHESIS; PROTEIN STRUCTURE, TERTIARY; PUROMYCIN; RIBOSOMES; RNA, FUNGAL; RNA, TRANSFER, MET; SACCHAROMYCES CEREVISIAE;

EUKARYOTA;

EID: 33646168052     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.2263906     Document Type: Article

References (67)

1. Algire, M.A., Maag, D., Savio, P., Acker, M.G., Tarun, S.Z., Sachs, A.B., Asano, K., Nielsen, K.H., Olsen, D.S., Phan, L., et al. 2002. Development and characterization of a reconstituted yeast translation initiation system. RNA 8: 382-397.
2. Algire, M.A., Maag, D., and Lorsch, J.R. 2005. Pi release from eIF2, not GTP hydrolysis, is the step controlled by start-site selection during eukaryotic translation initiation. Mol. Cell 20: 251-262.
3. Met in vivo. J. Mol. Biol. 233: 43-58.
4. Astrom, S.U., Nordlund, M.E., Erickson, F.L., Hannig, E.M., and Bystrom, A.S. 1999. Genetic interactions between a null allele of the RIT1 gene encoding an initiator tRNA-specific modification enzyme and genes encoding translation factors in Saccharomyces cerevisiae. Mol. Gen. Genet. 261: 967-976.
5. Basavappa, R. and Sigler, P.B. 1991. The 3 Å crystal structure of yeast initiator tRNA: Functional implications in initiator/elongator discrimination. EMBO J. 10: 3105-3111.
6. Phe from E. coli bound to the ribosomal A-site. Nucleic Acids Res. 11: 575-589.
7. Carter, A.P., Clemons, W.M., Brodersen, D.E., Morgan-Warren, R.J., Wimberly, B.T., and Ramakrishnan, V. 2000. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407: 340-348.
8. Carter, A.P., Clemons Jr., W.M., Brodersen, D.E., Morgan-Warren, R.J., Hartsch, T., Wimberly, B.T., and Ramakrishnan, V.V. 2001. Crystal structure of an initiation factor bound to the 30S ribosomal subunit. Science 291: 498-501.
9. Chakrabarti, A. and Maitra, U. 1991. Function of eukaryotic initiation factor 5 in the formation of an 80S ribosomal polypeptide chain initiation complex. J. Biol. Chem. 21: 14039-14045.
10. Cochella, L. and Green, R. 2005. An active role for tRNA in decoding beyond codon:anticodon pairing. Science 308: 1178-1180.
11. Dabrowski, M., Spahn, C.M., and Nierhaus, K.H. 1995. Interaction of tRNAs with the ribosome at the A and P sites. EMBO J. 14: 4872-4882.
12. Dallas, A. and Noller, H.F. 2001. Interaction of translation initiation factor 3 with the 30S ribosomal subunit. Mol. Cell 8: 855-864.
13. Desgres, J., Keith, G., Kuo, K.C., and Gehrke, C.W. 1989. Presence of phosphorylated O-ribosyl-adenosine in T-psi-stem of yeast methionine initiator tRNA. Nucleic Acids Res. 17: 865-882.
14. Drabkin, H.J. and RajBhandary, U.L. 1998. Initiation of protein synthesis in mammalian cells with codons other than AUG and amino acids other than methionine. Mol. Cell. Biol. 18: 5140-5147.
15. Drabkin, H.J., Helk, B., and RajBhandary, U.L. 1993. The role of nucleotides conserved in eukaryotic initiator methionine tRNAs in initiation of protein synthesis. J. Biol. Chem. 268: 25221-25228.
16. Drabkin, H.J., Estrella, M., and RajBhandary, U.L. 1998. Initiator-elongator discrimination in vertebrate tRNAs for protein synthesis. Mol. Cell. Biol. 18: 1459-1466.
17. Phe by using slow tritium exchange. Proc. Natl. Acad. Sci. 77: 5135-5139.
18. Farruggio, D., Chaudhuri, J., Maitra, U., and RajBhandary, U.L. 1996. The A1 x U72 base pair conserved in eukaryotic initiator tRNAs is important specifically for binding to the eukaryotic translation initiation factor eIF2. Mol. Cell. Biol. 16: 4248-4256.
19. Forster, C., Chakraburtty, K., and Sprinzl, M. 1993. Discrimination between initiation and elongation of protein biosynthesis in yeast: Identity assured by a nucleotide modification in the initiator tRNA. Nucleic Acids Res. 21: 5679-5683.
20. Gaspar, N.J., Kinzy, T.G., Scherer, B.J., Humbelin, M., Hershey, J.W., and Merrick, W.C. 1994. Translation initiation factor eIF-2. Cloning and expression of the human cDNA encoding the gamma-subunit. J. Biol. Chem. 269: 3415-3422.
21. Guillon, J.M., Heiss, S., Soutourina, J., Mechulam, Y., Laalami, S., Grunberg-Manago, M., and Blanquet, S. 1996. Interplay of methionine tRNAs with translation elongation factor Tu and translation initiation factor 2 in Escherichia coli. J. Biol. Chem. 271: 22321-22325.
22. Hartz, D., Binkley, J., Hollingsworth, T., and Gold, L. 1990. Domains of initiator tRNA and initiation codon crucial for initiator tRNA selection by Escherichia coli IF3. Genes & Dev. 4: 1790-1800.
23. Hirsh, D. 1971. Tryptophan transfer RNA as the UGA suppressor. J. Mol. Biol. 58: 439-458.
24. Huang, H., Yoon, H., Hannig, E.M., and Donahue, T.F. 1997. GTP hydrolysis controls stringent selection of the AUG start codon during translation initiation in Saccharomyces cerevisiae. Genes & Dev. 11: 2396-2413.
25. Jivotovskaya, A.V., Valasek, L., Hinnebusch, A.G., and Nielsen, K.H. 2006. eIF3 and eIF2 can promote mRNA binding to 40S subunits independently of eIF4G in yeast. Mol. Cell. Biol. 26: 1355-1372.
26. Kapp, L.D. and Lorsch, J.R. 2004a. GTP-dependent recognition of the methionine moiety on initiator tRNA by translation factor eIF2. J. Mol. Biol. 335: 923-936.
27. _. 2004b. The molecular mechanics of eukaryotic translation. Annu. Rev. Biochem. 73: 657-704.
28. Met from yeast and wheat germ. Nucleic Acids Res. 18: 4677-4682.
29. Kyrpides, N.C. and Woese, C.R. 1998. Universally conserved translation initiation factors. Proc. Natl. Acad. Sci. 95: 224-228.
30. Lancaster, L. and Noller, H.F. 2005. Involvement of 16S rRNA nucleotides G1338 and A1339 in discrimination of initiator tRNA. Mol. Cell 20: 623-632.
31. Lomakin, I.B., Kolupaeva, V.G., Marintchev, A., Wagner, G., and Pestova, T.V. 2003. Position of eukaryotic initiation factor eIF1 on the 40S ribosomal subunit determined by directed hydroxyl radical probing. Genes & Dev. 17: 2786-2797.
32. Lomakin, I.B., Shirokikh, N.E., Yusupov, M.M., Hellen, C.U., and Pestova, T.V. 2006. The fidelity of translation initiation: Reciprocal activities of eIF1, IF3 and YciH. EMBO J. 25: 196-210.
33. Lorsch, J.R. and Herschlag, D. 1999. Kinetic dissection of fundamental processes of eukaryotic translation initiation in vitro. EMBO J. 18: 6705-6717.
34. Maag, D., Fekete, C.A., Gryczynski, Z., and Lorsch, J.R. 2005. A conformational change in the eukaryotic translation pre-initiation complex and release of eIF1 signal recognition of the start codon. Mol. Cell 17: 265-275.
35. Maag, D., Algire, M.A., and Lorsch, J.R. 2006. Communication between eukaryotic translation initiation factors 5 and 1A within the ribosomal pre-initiation complex plays a role in start site selection. J. Mol. Biol. 356: 724-737.
36. Mandal, N., Mangroo, D., Dalluge, J.J., McCloskey, J.A., and RajBhandary, U.L. 1996. Role of the three consecutive G:C base pairs conserved in the anticodon stem of initiator tRNAs in initiation of protein synthesis in Escherichia coli. RNA 2: 473-482.
37. Marck, C. and Grosjean, H. 2002. tRNomics. Analysis of tRNA genes from 50 genomes of Eukarya, Archaea, and Bacteria reveals anticodon-sparing strategies and domain-specific features. RNA 8: 1189-1232.
38. Mayer, C., Stortchevoi, A., Kohrer, C., Varshney, U., and RajBhandary, U.L. 2001. Initiator tRNA and its role in initiation of protein synthesis. Cold Spring Harb. Symp. Quant. Biol. 66: 195-206.
39. McCutcheon, J.P., Agrawal, R.K., Philips, S.M., Grassucci, R.A., Gerchman, S.E., Clemons Jr., W.M., and Frank, J. 1999. Location of translational initiation factor IF3 on the small ribosomal subunit. Proc. Natl. Acad. Sci. 96: 4301-4306.
40. Moras, D., Dock, A.C., Dumas, P., Westhof, E., Romby, P., Ebel, J.P., and Giege, R. 1986. Anticodon-anticodon interaction induces conformational changes in tRNA: Yeast tRNAAsp, a model for tRNA-mRNA recognition. Proc. Natl. Acad. Sci. 83: 932-936.
41. Palmiter, R.D. 1975. Quantitation of parameters that determine the rate of ovalbumin synthesis. Cell 4: 189-197.
42. Met in initiation of translation in vitro. RNA 7: 1496-1505.
43. Pestova, T.V. and Kolupaeva, V.G. 2002. The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes & Dev. 16: 2906-2922.
44. Pestova, T.V., Borukhov, S.I., and Hellen, C.U.T. 1998. Eukaryotic ribosomes require initiation factors 1 and 1A to locate initiation codons. Nature 394: 854-859.
45. 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.
46. RajBhandary, U.L. 1994. Initiator transfer RNAs. J. Bacteriol. 176: 547-552.
47. Rodnina, M.V., Fricke, R., and Wintermeyer, W. 1994. Transient conformational states of aminoacyl-tRNA during ribosome binding catalyzed by elongation factor Tu. Biochemistry 33: 12267-12275.
48. Schevitz, R.W., Podjarny, A.D., Krishnamachari, N., Hughes, J.J., Sigler, P.B., and Sussman, J.L. 1979. Crystal structure of a eukaryotic initiator tRNA. Nature 278: 188-190.
49. Schmitt, E., Blanquet, S., and Mechulam, Y. 2002. The large subunit of initiation factor aIF2 is a close structural homologue of elongation factors. EMBO J. 21: 1821-1832.
50. Schultz, D.W. and Yarus, M. 1994a. tRNA structure and ribosomal function. I. tRNA nucleotide 27-43 mutations enhance first position wobble. J. Mol. Biol. 235: 1381-1394.
51. _. 1994b. tRNA structure and ribosomal function. II. Interaction between anticodon helix and other tRNA mutations. J. Mol. Biol. 235: 1395-1405.
52. Schwarz, U., Menzel, H.M., and Gassen, H.G. 1976. Codon-dependent rearrangement of the three-dimensional structure of phenylalanine tRNA, exposing the T-Y-C-G sequence for binding to the 50S ribosomal subunit. Biochemistry 15: 2484-2490.
53. Seong, B.L. and RajBhandary, U.L. 1987a. Escherichia coli formylmethionine tRNA: Mutations in GGGCCC sequence conserved in anticodon stem of initiator tRNAs affect initiation of protein synthesis and conformation of anticodon loop. Proc. Natl. Acad. Sci. 84: 334-338.
54. _. 1987b. Mutants of Escherichia coli formylmethionine tRNA: A single base change enables initiator tRNA to act as an elongator in vitro. Proc. Natl. Acad. Sci. 84: 8859-8863.
55. Simsek, M. and RajBhandary, U.L. 1972. The primary structure of yeast initiator transfer ribonucleic acid. Biochem. Biophys. Res. Commun. 49: 508-515.
56. Smith, D. and Yarus, M. 1989a. Transfer RNA structure and coding specificity. I. Evidence that a D-arm mutation reduces tRNA dissociation from the ribosome. J. Mol. Biol. 206: 489-501.
57. _. 1989b. Transfer RNA structure and coding specificity. II. A D-arm tertiary interaction that restricts coding range. J. Mol. Biol. 206: 503-511.
58. Spahn, C.M., Beckmann, R., Eswar, N., Penczek, P.A., Sali, A., Blobel, G., and Frank, J. 2001. Structure of the 80S ribosome from Saccharomyces cerevisiae-tRNA-ribosome and subunit-subunit interactions. Cell 107: 373-386.
59. Sprinzl, M. and Vassilenko, K.S. 2005. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 33: D139-D140.
60. Valle, M., Sengupta, J., Swami, N.K., Grassucci, R.A., Burkhardt, N., Nierhaus, K.H., Agrawal, R.K., and Frank, J. 2002. Cryo-EM reveals an active role for aminoacyl-tRNA in the accommodation process. EMBO J. 21: 3557-3567.
61. Valle, M., Zavialov, A., Sengupta, J., Rawat, U., Ehrenberg, M., and Frank, J. 2003. Locking and unlocking of ribosomal motions. Cell 114: 123-134.
62. von Pawel-Rammingen, U., Astrom, S., and Bystrom, A.S. 1992. Mutational analysis of conserved positions potentially important for initiator tRNA function in Saccharomyces cerevisiae. Mol. Cell. Biol. 12: 1432-1442.
63. Met primarily as an elongator in eukaryotic protein synthesis. J. Biol. Chem. 264: 18506-18511.
64. Met. Nature 286: 346-351.
65. Wrede, P., Woo, N.H., and Rich, A. 1979. Initiator tRNAs have a unique anticodon loop conformation. Proc. Natl. Acad. Sci. 76: 3289-3293.
66. Youngman, E.M., Brunelle, J.L., Kochaniak, A.B., and Green, R. 2004. The active site of the ribosome is composed of two layers of conserved nucleotides with distinct roles in peptide bond formation and peptide release. Cell 117: 589-599.
67. Yusupov, M.M., Yusupova, G.Z., Baucom, A., Lieberman, K., Earnest, T.N., Cate, J.H., and Noller, H.F. 2001. Crystal structure of the ribosome at 5.5 Å resolution. Science 292: 883-896.