Mutants of the RNA-processing enzyme RNase e reverse the extreme slow-growth phenotype caused by a mutant translation factor EF-Tu

Molecular Microbiology

Volumn 70, Issue 5, 2008, Pages 1194-1209

  Hammarlöf, Disa L ^a   Hughes, Diarmaid ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RIBONUCLEASE E; RNA POLYMERASE;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; GENE MUTATION; GENE SEQUENCE; GENETIC CODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA PROCESSING; SALMONELLA ENTERICA;

BACTERIAL PROTEINS; ENDORIBONUCLEASES; GENE EXPRESSION REGULATION, BACTERIAL; PEPTIDE ELONGATION FACTOR TU; PHENOTYPE; PROTEIN BIOSYNTHESIS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, BACTERIAL; RNA, MESSENGER; SALMONELLA TYPHIMURIUM; SUPPRESSION, GENETIC;

SALMONELLA ENTERICA;

EID: 55349119169     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06472.x     Document Type: Article

References (58)

1. Abdulkarim, F. Hughes, D. (1996) Homologous recombination between the tuf genes of Salmonella typhimurium. J Mol Biol 260 : 506 522.
2. Abdulkarim, F., Tuohy, T.M., Buckingham, R.H. Hughes, D. (1991) Missense substitutions lethal to essential functions of EF-Tu. Biochimie 73 : 1457 1464.
3. Abdulkarim, F., Liljas, L. Hughes, D. (1994) Mutations to kirromycin resistance occur in the interface of domains I and III of EF-Tu GTP. FEBS Lett 352 : 118 122.
4. Abdulkarim, F., Ehrenberg, M. Hughes, D. (1996) Mutants of EF-Tu defective in binding aminoacyl-tRNA. FEBS Lett 382 : 297 303.
5. Apirion, D. Lassar, A.B. (1978) A conditional lethal mutant of Escherichia coli which affects the processing of ribosomal RNA. J Biol Chem 253 : 1738 1742.
6. Arwidsson, O. Hughes, D. (2004) Evidence against reciprocal recombination as the basis for tuf gene conversion in Salmonella enterica serovar Typhimurium. J Mol Biol 338 : 463 467.
7. Babitzke, P. Kushner, S.R. (1991) The Ams (altered mRNA stability) protein and ribonuclease E are encoded by the same structural gene of Escherichia coli. Proc Natl Acad Sci USA 88 : 1 5.
8. Baker, K.E. Mackie, G.A. (2003) Ectopic RNase E sites promote bypass of 5′-end-dependent mRNA decay in Escherichia coli. Mol Microbiol 47 : 75 88.
9. Bjorkman, J., Samuelsson, P., Andersson, D.I. Hughes, D. (1999) Novel ribosomal mutations affecting translational accuracy, antibiotic resistance and virulence of Salmonella typhimurium. Mol Microbiol 31 : 53 58.
10. Blomberg, P., Wagner, E.G. Nordstrom, K. (1990) Control of replication of plasmid R1: the duplex between the antisense RNA, CopA, and its target, CopT, is processed specifically in vivo and in vitro by RNase III. EMBO J 9 : 2331 2340.
11. Bremer, H., Dennis (1996) Modulation of chemical composition and other parameters of the cell by growth rate. In Escherichia Coli and Salmonella: Cellular and Molecular Biology. Neidhart, F.C., et al. (eds). Washington, DC : American Society for Microbiology Press, pp. 1553 1569.
12. Callaghan, A.J., Grossmann, J.G., Redko, Y.U., Ilag, L.L., Moncrieffe, M.C., Symmons, M.F., et al. (2003) Quaternary structure and catalytic activity of the Escherichia coli ribonuclease E amino-terminal catalytic domain. Biochemistry 42 : 13848 13855.
13. Callaghan, A.J., Marcaida, M.J., Stead, J.A., McDowall, K.J., Scott, W.G. Luisi, B.F. (2005a) Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover. Nature 437 : 1187 1191.
14. Callaghan, A.J., Redko, Y., Murphy, L.M., Grossmann, J.G., Yates, D., Garman, E., et al. (2005b) 'Zn-link': a metal-sharing interface that organizes the quaternary structure and catalytic site of the endoribonuclease, RNase E. Biochemistry 44 : 4667 4675.
15. Carpousis, A.J. (2007) The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu Rev Microbiol 61 : 71 87.
16. Caruthers, J.M., Feng, Y., McKay, D.B. Cohen, S.N. (2006) Retention of core catalytic functions by a conserved minimal ribonuclease E peptide that lacks the domain required for tetramer formation. J Biol Chem 281 : 27046 27051.
17. Casaregola, S., Jacq, A., Laoudj, D., McGurk, G., Margarson, S., Tempete, M., et al. (1992) Cloning and analysis of the entire Escherichia coli ams gene. ams is identical to hmp1 and encodes a 114 kDa protein that migrates as a 180 kDa protein. J Mol Biol 228 : 30 40.
18. Cherepanov, P.P. Wackernagel, W. (1995) Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalysed excision of the antibiotic-resistance determinant. Gene 158 : 9 14.
19. Datsenko, K.A. 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.
20. Diwa, A., Bricker, A.L., Jain, C. Belasco, J.G. (2000) An evolutionarily conserved RNA stem-loop functions as a sensor that directs feedback regulation of RNase E gene expression. Genes Dev 14 : 1249 1260.
21. Ehrenberg, M. Kurland, C.G. (1984) Costs of accuracy determined by a maximal growth rate constraint. Q Rev Biophys 17 : 45 82.
22. Epshtein, V. Nudler, E. (2003) Cooperation between RNA polymerase molecules in transcription elongation. Science 300 : 801 805.
23. Ghora, B.K. Apirion, D. (1978) Structural analysis and in vitro processing to p5 rRNA of a 9S RNA molecule isolated from an rne mutant of E. coli. Cell 15 : 1055 1066.
24. Hughes, D. (1986) The isolation and mapping of EF-Tu mutations in Salmonella typhimurium. Mol Gen Genet 202 : 108 111.
25. Hughes, D. (1990) Both genes for EF-Tu in Salmonella typhimurium are individually dispensable for growth. J Mol Biol 215 : 41 51.
26. Iost, I. Dreyfus, M. (1995) The stability of Escherichia coli lacZ mRNA depends upon the simultaneity of its synthesis and translation. EMBO J 14 : 3252 3261.
27. Jain, C. Belasco, J.G. (1995) RNase E autoregulates its synthesis by controlling the degradation rate of its own mRNA in Escherichia coli: unusual sensitivity of the rne transcript to RNase E activity. Genes Dev 9 : 84 96.
28. Jain, C., Deana, A. Belasco, J.G. (2002) Consequences of RNase E scarcity in Escherichia coli. Mol Microbiol 43 : 1053 1064.
29. Jelenc, P.C. Kurland, C.G. (1979) Nucleoside triphosphate regeneration decreases the frequency of translation errors. Proc Natl Acad Sci USA 76 : 3174 3178.
30. Johanson, U. Hughes, D. (1994) Fusidic acid-resistant mutants define three regions in elongation factor G of Salmonella typhimurium. Gene 143 : 55 59.
31. Johanson, U., Aevarsson, A., Liljas, A. Hughes, D. (1996) The dynamic structure of EF-G studied by fusidic acid resistance and internal revertants. J Mol Biol 258 : 420 432.
32. Kjeldgaard, M., Nissen, P., Thirup, S. Nyborg, J. (1993) The crystal structure of elongation factor EF-Tu from Thermus aquaticus in the GTP conformation. Structure 1 : 35 50.
33. Kuwano, M., Ono, M., Endo, H., Hori, K., Nakamura, K., Hirota, Y. Ohnishi, Y. (1977) Gene affecting longevity of messenger RNA: a mutant of Escherichia coli with altered mRNA stability. Mol Gen Genet 154 : 279 285.
34. Leroy, A., Vanzo, N.F., Sousa, S., Dreyfus, M. Carpousis, A.J. (2002) Function in Escherichia coli of the non-catalytic part of RNase E: role in the degradation of ribosome-free mRNA. Mol Microbiol 45 : 1231 1243.
35. Lopez, P.J., Marchand, I., Joyce, S.A. Dreyfus, M. (1999) The C-terminal half of RNase E, which organizes the Escherichia coli degradosome, participates in mRNA degradation but not rRNA processing in vivo. Mol Microbiol 33 : 188 199.
36. Lovett, S.T. (2004) Encoded errors: mutations and rearrangements mediated by misalignment at repetitive DNA sequences. Mol Microbiol 52 : 1243 1253.
37. McClelland, M.K.E., Sanderson, J., Spieth, S.W., Clifton, P., Latreille, L., Courtney, S., et al. (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413 : 852 856.
38. McDowall, K.J. Cohen, S.N. (1996) The N-terminal domain of the rne gene product has RNase E activity and is non-overlapping with the arginine-rich RNA-binding site. J Mol Biol 255 : 349 355.
39. McDowall, K.J., Hernandez, R.G., Lin-Chao, S. Cohen, S.N. (1993) The ams-1 and rne-3071 temperature-sensitive mutations in the ams gene are in close proximity to each other and cause substitutions within a domain that resembles a product of the Escherichia coli mre locus. J Bacteriol 175 : 4245 4249.
40. Mackie, G.A. (1998) Ribonuclease E is a 5′-end-dependent endonuclease. Nature 395 : 720 723.
41. Miczak, A., Kaberdin, V.R., Wei, C.L. Lin-Chao, S. (1996) Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc Natl Acad Sci USA 93 : 3865 3869.
42. Misra, T.K. Apirion, D. (1979) RNase E, an RNA processing enzyme from Escherichia coli. J Biol Chem 254 : 11154 11159.
43. Mudd, E.A. Higgins, C.F. (1993) Escherichia coli endoribonuclease RNase E: autoregulation of expression and site-specific cleavage of mRNA. Mol Microbiol 9 : 557 568.
44. Mudd, E.A., Krisch, H.M. Higgins, C.F. (1990) RNase E, an endoribonuclease, has a general role in the chemical decay of Escherichia coli mRNA: evidence that rne and ams are the same genetic locus. Mol Microbiol 4 : 2127 2135.
45. Nissen, P., Kjeldgaard, M., Thirup, S., Polekhina, G., Reshetnikova, L., Clark, B.F. Nyborg, J. (1995) Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analogue. Science 270 : 1464 1472.
46. Nissen, P., Kjeldgaard, M., Thirup, S., Clark, B.F. Nyborg, J. (1996) The ternary complex of aminoacylated tRNA and EF-Tu-GTP. Recognition of a bond and a fold. Biochimie 78 : 921 933.
47. Ow, M.C., Liu, Q. Kushner, S.R. (2000) Analysis of mRNA decay and rRNA processing in Escherichia coli in the absence of RNase E-based degradosome assembly. Mol Microbiol 38 : 854 866.
48. Schmieger, H. Backhaus, H. (1973) The origin of DNA in transducing particles in P22-mutants with increased transduction-frequencies (HT-mutants). Mol Gen Genet 120 : 181 190.
49. Schubert, M., Edge, R.E., Lario, P., Cook, M.A., Strynadka, N.C., Mackie, G.A. McIntosh, L.P. (2004) Structural characterization of the RNase E S1 domain and identification of its oligonucleotide-binding and dimerization interfaces. J Mol Biol 341 : 37 54.
50. Sousa, S., Marchand, I. Dreyfus, M. (2001) Autoregulation allows Escherichia coli RNase E to adjust continuously its synthesis to that of its substrates. Mol Microbiol 42 : 867 878.
51. Taraseviciene, L., Bjork, G.R. Uhlin, B.E. (1995) Evidence for an RNA binding region in the Escherichia coli processing endoribonuclease RNase E. J Biol Chem 270 : 26391 26398.
52. Tubulekas, I. Hughes, D. (1993a) Growth and translation elongation rate are sensitive to the concentration of EF-Tu. Mol Microbiol 8 : 761 770.
53. Tubulekas, I. Hughes, D. (1993b) Suppression of rpsL phenotypes by tuf mutations reveals a unique relationship between translation elongation and growth rate. Mol Microbiol 7 : 275 284.
54. Tubulekas, I., Buckingham, R.H. Hughes, D. (1991) Mutant ribosomes can generate dominant kirromycin resistance. J Bacteriol 173 : 3635 3643.
55. Van Delft, J.H., Schmidt, D.S. Bosch, L. (1987) The tRNA-tufB operon transcription termination and processing upstream from tufB. J Mol Biol 197 : 647 657.
56. Wolf, H., Chinali, G. Parmeggiani, A. (1974) Kirromycin, an inhibitor of protein biosynthesis that acts on elongation factor Tu. Proc Natl Acad Sci USA 71 : 4910 4914.
57. Young, R. Bremer, H. (1976) Polypeptide-chain-elongation rate in Escherichia coli B/r as a function of growth rate. Biochem J 160 : 185 194.
58. Yu, D., Ellis, H.M., Lee, E.C., Jenkins, N.A., Copeland, N.G. Court, D.L. (2000) An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci USA 97 : 5978 5983.