A primary role for release factor 3 in quality control during translation elongation in Escherichia coli

Cell

Volumn 147, Issue 2, 2011, Pages 396-408

  Zaher, Hani S ^a   Green, Rachel ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GUANOSINE TRIPHOSPHATASE; MESSENGER RNA; RELEASE FACTOR 2; RELEASE FACTOR 3; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE DELETION; GENE FUNCTION; GENETIC HETEROGENEITY; MASS SPECTROMETRY; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS REGULATION; REPORTER GENE; RIBOSOMAL FRAMESHIFTING; RNA STABILITY; SENSITIZATION; TRANSLATION ELONGATION; TRANSLATION REGULATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 80054693287     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.08.045     Document Type: Article

References (61)

1. F.M. Adamski, K.K. McCaughan, F. Jorgensen, C.G. Kurland, and W.P. Tate The concentration of polypeptide chain release factors 1 and 2 at different growth rates of Escherichia coli J. Mol. Biol. 238 1994 302 308 (Pubitemid 24154713)
2. D.I. Andersson, K. Bohman, L.A. Isaksson, and C.G. Kurland Translation rates and misreading characteristics of rpsD mutants in Escherichia coli Mol. Gen. Genet. 187 1982 467 472 (Pubitemid 13218797)
3. T. Baba, T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, M. Baba, K.A. Datsenko, M. Tomita, B.L. Wanner, and H. Mori Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection Mol. Syst. Biol. 2 2006 2006 0008
4. M.R. Capecchi Polypeptide chain termination in vitro: isolation of a release factor Proc. Natl. Acad. Sci. USA 58 1967 1144 1151
5. M.R. Capecchi, and H.A. Klein Characterization of three proteins involved in polypeptide chain termination Cold Spring Harb. Symp. Quant. Biol. 34 1969 469 477
6. T. Caskey, E. Scolnick, R. Tompkins, J. Goldstein, and G. Milman Peptide chain termination, codon, protein factor, and ribosomal requirements Cold Spring Harb. Symp. Quant. Biol. 34 1969 479 488
7. W.J. Craigen, and C.T. Caskey Expression of peptide chain release factor 2 requires high-efficiency frameshift Nature 322 1986 273 275 (Pubitemid 16059452)
8. K.A. Datsenko, and B.L. Wanner One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Proc. Natl. Acad. Sci. USA 97 2000 6640 6645 (Pubitemid 30412767)
9. D.E. Eyler, and R. Green Distinct response of yeast ribosomes to a miscoding event during translation RNA 17 2011 925 932
10. D.V. Freistroffer, M. Kwiatkowski, R.H. Buckingham, and M. Ehrenberg The accuracy of codon recognition by polypeptide release factors Proc. Natl. Acad. Sci. USA 97 2000 2046 2051 (Pubitemid 30134019)
11. D.V. Freistroffer, M.Y. Pavlov, J. MacDougall, R.H. Buckingham, and M. Ehrenberg Release factor RF3 in E.coli accelerates the dissociation of release factors RF1 and RF2 from the ribosome in a GTP-dependent manner EMBO J. 16 1997 4126 4133 (Pubitemid 27281027)
12. H. Gao, Z. Zhou, U. Rawat, C. Huang, L. Bouakaz, C. Wang, Z. Cheng, Y. Liu, A. Zavialov, and R. Gursky RF3 induces ribosomal conformational changes responsible for dissociation of class I release factors Cell 129 2007 929 941 (Pubitemid 46813153)
13. G. Grentzmann, D. Brechemier-Baey, V. Heurgue-Hamard, and R.H. Buckingham Function of polypeptide chain release factor RF-3 in Escherichia coli. RF-3 action in termination is predominantly at UGA-containing stop signals J. Biol. Chem. 270 1995 10595 10600
14. G. Grentzmann, D. Brechemier-Baey, V. Heurgue, L. Mora, and R.H. Buckingham Localization and characterization of the gene encoding release factor RF3 in Escherichia coli Proc. Natl. Acad. Sci. USA 91 1994 5848 5852 (Pubitemid 24188239)
15. V. Heurgue-Hamard, V. Dincbas, R.H. Buckingham, and M. Ehrenberg Origins of minigene-dependent growth inhibition in bacterial cells EMBO J. 19 2000 2701 2709 (Pubitemid 30323558)
16. V. Heurgue-Hamard, R. Karimi, L. Mora, J. MacDougall, C. Leboeuf, G. Grentzmann, M. Ehrenberg, and R.H. Buckingham Ribosome release factor RF4 and termination factor RF3 are involved in dissociation of peptidyl-tRNA from the ribosome EMBO J. 17 1998 808 816 (Pubitemid 28062059)
17. O. Isken, and L.E. Maquat Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function Genes Dev. 21 2007 1833 1856 (Pubitemid 47204924)
18. K. Ito, K. Ebihara, M. Uno, and Y. Nakamura Conserved motifs in prokaryotic and eukaryotic polypeptide release factors: tRNA-protein mimicry hypothesis Proc. Natl. Acad. Sci. USA 93 1996 5443 5448 (Pubitemid 26159469)
19. C.E. Jahn, A.O. Charkowski, and D.K. Willis Evaluation of isolation methods and RNA integrity for bacterial RNA quantitation J. Microbiol. Methods 75 2008 318 324
20. B.D. Janssen, and C.S. Hayes Kinetics of paused ribosome recycling in Escherichia coli J. Mol. Biol. 394 2009 251 267
21. F. Jorgensen, F.M. Adamski, W.P. Tate, and C.G. Kurland Release factor-dependent false stops are infrequent in Escherichia coli J. Mol. Biol. 230 1993 41 50 (Pubitemid 23093546)
22. R. Karimi, and M. Ehrenberg Dissociation rates of peptidyl-tRNA from the P-site of E.coli ribosomes EMBO J. 15 1996 1149 1154
23. T. Kigawa, T. Yabuki, N. Matsuda, T. Matsuda, R. Nakajima, A. Tanaka, and S. Yokoyama Preparation of Escherichia coli cell extract for highly productive cell-free protein expression J. Struct. Funct. Genomics 5 2004 63 68 (Pubitemid 39030621)
24. L. Kisselev, M. Ehrenberg, and L. Frolova Termination of translation: interplay of mRNA, rRNAs and release factors? EMBO J. 22 2003 175 182 (Pubitemid 36119423)
25. B.P. Klaholz, A.G. Myasnikov, and M. Van Heel Visualization of release factor 3 on the ribosome during termination of protein synthesis Nature 427 2004 862 865 (Pubitemid 38297750)
26. E.B. Kramer, H. Vallabhaneni, L.M. Mayer, and P.J. Farabaugh A comprehensive analysis of translational missense errors in the yeast Saccharomyces cerevisiae RNA 16 2010 1797 1808
27. T. Margus, M. Remm, and T. Tenson Phylogenetic distribution of translational GTPases in bacteria BMC Genomics 8 2007 15
28. M.B. Matthews, N. Sonenberg, and J.W.B. Hershey Origins and principles of translational control M.B. Matthews, N. Sonenberg, J.W.B. Hershey, Translational Control in Biology and Medicine 2007 Cold Spring Harbor Laboratory Press Cold spring harbor, NY 1 40
29. O. Mikuni, K. Ito, J. Moffat, K. Matsumura, K. McCaughan, T. Nobukuni, W. Tate, and Y. Nakamura Identification of the prfC gene, which encodes peptide-chain-release factor 3 of Escherichia coli Proc. Natl. Acad. Sci. USA 91 1994 5798 5802 (Pubitemid 24188229)
30. G. Milman, J. Goldstein, E. Scolnick, and T. Caskey Peptide chain termination. 3. Stimulation of in vitro termination Proc. Natl. Acad. Sci. USA 63 1969 183 190
31. L. Mora, A. Zavialov, M. Ehrenberg, and R.H. Buckingham Stop codon recognition and interactions with peptide release factor RF3 of truncated and chimeric RF1 and RF2 from Escherichia coli Mol. Microbiol. 50 2003 1467 1476 (Pubitemid 38010445)
32. Y. Nakamura, K. Ito, and L.A. Isaksson Emerging understanding of translation termination Cell 87 1996 147 150 (Pubitemid 26358994)
33. T. Nogueira, M. de Smit, M. Graffe, and M. Springer The relationship between translational control and mRNA degradation for the Escherichia coli threonyl-tRNA synthetase gene J. Mol. Biol. 310 2001 709 722 (Pubitemid 32695690)
34. V.P. Pisareva, A.V. Pisarev, C.U. Hellen, M.V. Rodnina, and T.V. Pestova Kinetic analysis of interaction of eukaryotic release factor 3 with guanine nucleotides J. Biol. Chem. 281 2006 40224 40235 (Pubitemid 46043300)
35. J. Precup, and J. Parker Missense misreading of asparagine codons as a function of codon identity and context J. Biol. Chem. 262 1987 11351 11355
36. E.Z. Ron, R.E. Kohler, and B.D. Davis Polysomes extracted from Escherichia coli by freeze-thaw-lysozyme lysis Science 153 1966 1119 1120
37. N. Sternberg, and R. Hoess The molecular genetics of bacteriophage P1 Annu. Rev. Genet. 17 1983 123 154
38. R.C. Thompson, and A.M. Karim The accuracy of protein biosynthesis is limited by its speed: high fidelity selection by ribosomes of aminoacyl-tRNA ternary complexes containing GTP Proc. Natl. Acad. Sci. USA 79 1982 4922 4926 (Pubitemid 12004141)
39. Y. Watanabe, Y. Nakamura, and K. Ito A novel class of bacterial translation factor RF3 mutations suggests specific structural domains for premature peptidyl-tRNA drop-off FEBS Lett. 584 2010 790 794
40. E.M. Youngman, S.L. He, L.J. Nikstad, and R. Green Stop codon recognition by release factors induces structural rearrangement of the ribosomal decoding center that is productive for peptide release Mol. Cell 28 2007 533 543 (Pubitemid 350137792)
41. H.S. Zaher, and R. Green Fidelity at the molecular level: lessons from protein synthesis Cell 136 2009 746 762
42. H.S. Zaher, and R. Green Quality control by the ribosome following peptide bond formation Nature 457 2009 161 166
43. H.S. Zaher, and R. Green Kinetic basis for global loss of fidelity arising from mismatches in the P-site codon:anticodon helix RNA 16 2010 1980 1989
44. H.S. Zaher, and P.J. Unrau T7 RNA polymerase mediates fast promoter-independent extension of unstable nucleic acid complexes Biochemistry 43 2004 7873 7880 (Pubitemid 38787696)
45. A.V. Zavialov, R.H. Buckingham, and M. Ehrenberg A posttermination ribosomal complex is the guanine nucleotide exchange factor for peptide release factor RF3 Cell 107 2001 115 124 (Pubitemid 32972042)
46. A.V. Zavialov, and M. Ehrenberg Peptidyl-tRNA regulates the GTPase activity of translation factors Cell 114 2003 113 122 (Pubitemid 36859845)
47. A.V. Zavialov, L. Mora, R.H. Buckingham, and M. Ehrenberg Release of peptide promoted by the GGQ motif of class 1 release factors regulates the GTPase activity of RF3 Mol. Cell 10 2002 789 798 (Pubitemid 35335634)
48. Andersson, D.I.; Bohman, K.; Isaksson, L.A.; and Kurland, C.G. (1982). Translation rates and misreading characteristics of rpsD mutants in Escherichia coli. Mol. Gen. Genet. 187, 467-472. (Pubitemid 13218797)
49. Apirion, D. (1978). Isolation, genetic mapping and some characterization of a mutation in Escherichia coli that affects the processing of ribonuleic acid. Genetics 90, 659-671. (Pubitemid 9065186)
50. Atherly, A.G.; and Menninger, J.R. (1972). Mutant E. coli strain with temperature sensitive peptidyl-transfer RNA hydrolase. Nat. New Biol. 240, 245-246.
51. Baba, T.; Ara, T.; Hasegawa, M.; Takai, Y.; Okumura, Y.; Baba, M.; Datsenko, K. A.; Tomita, M.; Wanner, B. L.; and Mori, H. (2006). Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2, 2006 0008.
52. Datsenko, K.A.; and Wanner, B.L. (2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97, 6640-6645. (Pubitemid 30412767)
53. Fill, N. (1969). A functional analysis of the rel gene in Escherichia coli. J. Mol. Biol. 45, 195-203.
54. Gong, F.; and Yanofsky, C. (2002). Analysis of tryptophanase operon expression in vitro: accumulation of TnaC-peptidyl-tRNA in a release factor 2-depleted S-30 extract prevents Rho factor action, simulating induction. J. Biol. Chem. 277, 17095-17100. (Pubitemid 34967740)
55. Jelenc, P.C.; and Kurland, C.G. (1979). Nucleoside triphosphate regeneration decreases the frequency of translation errors. Proc. Natl. Acad. Sci. USA 76, 3174-3178.
56. Nickenig, G.; and Murphy, T.J. (1994). Downregulation by growth factors of vascular smooth muscle angiotensin receptor gene expression. Mol. Pharmacol. 46, 653-659. (Pubitemid 24334755)
57. Precup, J.; and Parker, J. (1987). Missense misreading of asparagine codons as a function of codon identity and context. J. Biol. Chem. 262, 11351-11355.
58. 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. (Pubitemid 38692525)
59. Zaher, H.S.; and Green, R. (2009). Quality control by the ribosome following peptide bond formation. Nature 457, 161-166.
60. Zaher, H.S.; and Green, R. (2010). Hyperaccurate and error-prone ribosomes exploit distinct mechanisms during tRNA selection. Mol. Cell 39, 110-120.
61. Zaher, H.S.; and Unrau, P.J. (2005). Nucleic acid library construction using synthetic DNA constructs. Methods Mol. Biol. 288, 359-378.