In the absence of translation, RNase E can bypass 5' mRNA stabilizers in Escherichia coli

Journal of Molecular Biology

Volumn 282, Issue 2, 1998, Pages 241-254

  Joyce, Susan A ^a   Dreyfus, Marc ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

5' Stabilizer; lacZ gene; mRNA degradation; RNase E; Translation

Indexed keywords

MESSENGER RNA; RIBONUCLEASE; RIBOSOME RNA;

ARTICLE; BINDING SITE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; RIBOSOME SUBUNIT; RNA DEGRADATION; RNA TRANSLATION; SEQUENCE ANALYSIS; START CODON;

ESCHERICHIA COLI;

EID: 0032544304     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2027     Document Type: Article

References (67)

1. Adhya, S. & Gottesman, M. (1978). Control of transcription termination. Annu. Rev. Biochem. 47, 967-996.
2. Agaisse, H. & Lereclus, D. (1996). STAB-SD: a Shine-Dalgarno sequence in the 5′ untranslated region is a determinant of stability. Mol. Microbiol. 20, 633-643.
3. Arnold, T. E., Yu, J. & Belasco, J. G. (1998). mRNA stabilization by the ompA 5′ untranslated region: two protective elements hinder distinct pathways for mRNA degradation. RNA, 4, 319-330.
4. Baumeister, R., Flache, P., Melefors, O., von Gabain, A. & Hillen, W. (1991). Lack of a 5′ non-coding region in Tn1721 encoded TetR mRNA is associated with a low efficiency of translation and a short half-life in Escherichia coli. Nucl. Acids Res. 19, 4595-4600.
5. Bechhofer, D. (1993). 5′ mRNA stabilizers. In Control of Messenger RNA Stability (Belasco, J. G. & Brawerman, G., eds), pp. 31-52, Academic Press, San Diego and London.
6. Bechhofer, D. H. & Zen, K. H. (1989). Mechanism of erythromycin-induced ermC mRNA stability in Bacillus subtilis. J. Bacteriol. 171, 5803-5811.
7. Belasco, J. G. & Brawerman, G. (1993). Experimental approaches to the study of mRNA decay. In Control of Messenger RNA Stability (Belasco, J. G. & Brawerman, G., eds), pp. 475-493, Academic Press, San Diego and London.
8. Belasco, J. G., Nilsson, G., von Gabain, A. & Cohen, S. N (1986). The stability of E. coli gene transcripts is dependent on determinants localized to specific mRNA segments. Cell, 46, 245-251.
9. Blundell, M. & Kennel, D. (1974). Evidence for endonucleolytic attack in decay of lac messenger RNA in E. coli. J. Mol. Biol. 83, 143-161.
10. Bouvet, P. & Belasco, J. G. (1992). Control of RNase E-mediated RNA degradation by 5′-terminal base pairing in E. coli. Nature, 360, 488-491.
11. Carpousis, A. J., Van Houwe, G., Ehretsmann, C. & Krisch, H. M. (1994). Copurification of E. coli RNAase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation. Cell, 76, 889-900.
12. Chevrier-Miller, M., Jacques, N., Raibaud, O. & Dreyfus, M. (1990). Transcription of single-copy hybrid lacZ genes by T7 RNA polymerase in Escherichia coli: mRNA synthesis and degradation can be uncoupled from translation. Nucl. Acids Res. 18, 5787-5792.
13. Cho, K.-O. & Yanofsky, C. (1988). Sequence changes preceding a Shine-Dalgarno region influence trpE mRNA translation and decay. J. Mol. Biol. 204, 51-60.
14. Cole, J. R. & Nomura, M. (1986). Changes in the half-life of ribosomal protein messenger RNA caused by translational repression. J. Mol. Biol. 188, 383-392.
15. Comer, M. M., Dondon, J., Graffe, M., Yarchuk, O. & Springer, M. (1996). Growth rate-dependent control, feedback regulation and steady-state mRNA levels of the threonyl-tRNA synthetase gene of Escherichia coli. J. Mol. Biol. 261, 108-124.
16. Condon, C., Putzer, H., Luo, D. & Grunberg-Manago, M. (1997). Processing of the Bacillus subtilis thrS leader mRNA is RNase E-dependent in Escherichia coli. J. Mol. Biol. 268, 235-242.
17. Cremer, K., Silengo, L. & Schlessinger, D. (1974). Polypeptide formation and polyribosomes in E. coli treated with chloramphenicol. J. Bacteriol. 118, 582-589.
18. Donovan, W. P. & Kushner, S. R. (1986). Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K12. Proc. Natl Acad. Sci. USA, 83, 120-124.
19. Dreyfus, M. (1988). What constitues the signal for the initiation of protein synthesis on Escherichia coli mRNAs?. J. Mol. Biol. 204, 79-94.
20. Emory, S. A. & Belasco, J. G. (1990). The ompA 5′ untranslated RNA segment functions in Escherichia coli as a growth-rate-regulated mRNA stabilizer whose activity is unrelated to translational efficiency. J. Bacteriol. 172, 4472-4481.
21. Emory, S. A., Bouvet, P. & Belasco, J. G. (1992). A 5′-terminal stem-loop structure can stabilize mRNA in Escherichia coli. Genes Dev. 6, 135-148.
22. Frolova, L., Le, Goff X., Rasmussen, H. H., Cheperegin, S., Drugeon, G., Kress, M., Arman, I., Haenni, A. L., Celis, J. E. & Philippe, M., et al. (1994). A highly conserved eucaryotic protein family possessing properties of polypeptide chain release factor. Nature, 372, 701-703.
23. Guillerez, J., Gazeau, M. & Dreyfus, M. (1991). In the Escherichia coli lacZ gene the spacing between the translating ribosomes is insensitive to the efficiency of translation initiation. Nucl. Acids Res. 19, 6743-6750.
24. Hansen, M. J., Chen, L.-H., Fejzo, M. L. & Belasco, J. G. (1994). The ompA5′ untranlated region impedes a major pathway for mRNA degradation in Escherichia coli. Mol. Microbiol. 12, 707-716.
25. Hue, K. K., Cohen, S. D. & Bechhofer, D. H. (1995). A polypurine sequence that acts as a 5′ mRNA stabilizer in Bacillus subtilis. J. Bacteriol. 177, 3465-3471.
26. Iost, I. & Dreyfus, M. (1994). mRNAs can be stabilized by DEAD-box proteins. Nature, 372, 193-196.
27. Iost, I. & Dreyfus, M. (1995). The stability of the E. coli lacZ mRNA depends upon the simultaneity of its synthesis and translation. EMBO J. 14, 3252-3261.
28. Iost, I., Guillerez, J. & Dreyfus, M. (1992). Bacteriophage T7 RNA polymerase travels far ahead of ribosomes in vivo. J. Bacteriol. 174, 619-622.
29. Jacob, F. & Monod, J. (1961). Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol. 3, 318-356.
30. Jain, C. & Belasco, J. G. (1995). RNase E autoregulates its synthesis by controlling the degradation rate of its own mRNA in E. coli: unusual sensitivity of the rne transcript to RNase E activity. Genes Dev. 9, 84-96.
31. Jain, C. & Kleckner, N. (1993). IS10 mRNA stability and steady state levels in Escherichia coli: indirect effects of translation and role of rne function. Mol. Microbiol. 9, 233-247.
32. Kunst, F., Ogasawara, N., Moszer, I., et al. (1997). The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature, 390, 249-256.
33. Lewicki, B. T. U., Margus, T., Remme, J. & Nierhaus, K. H. (1993). Coupling of rRNA transcription and ribosomal assembly in vivo. J. Mol. Biol. 231, 581-593.
34. Lopez, P. J. & Dreyfus, M. (1996). The lacZ mRNA can be stabilized by the T7 late mRNA leader in E. coli. Biochimie, 78, 408-415.
35. Lopez, P. J., Iost, I. & Dreyfus, M. (1994). The use of a tRNA as an transcriptional reporter: the T7 late promoter is extremely efficient in Escherichia coli but its transcripts are poorly expressed. Nucl. Acids Res. 22, 1186-1193.
36. Lopez, P. J., Guillerez, J., Sousa, R. & Dreyfus, M. (1997). The low processivity of T7 RNA polymerase over the initially transcribed sequence can limit productive initiation in vivo. J. Mol. Biol. 269, 41-51.
37. Lopez, P. J., Marchand, I., Yarchuk, O. & Dreyfus, M. (1998). Translation inhibitors stabilize E. coli mRNAs independently of ribosome protection. Proc. Natl Acad. Sci. USA, 95, 6067-6072.
38. Mackie, G. A., Genereaux, J. L. & Masterman, S. K. (1997). Modulation of the activity of RNase E in vitro by RNA sequences and secondary structures 5′ to cleavage sites. J. Biol. Chem. 272, 609-616.
39. Makarova, O. V., Makarov, E. M., Sousa, R. & Dreyfus, M. (1995). Transcribing Escherichia coli genes with mutant T7 RNA polymerases: stability of lacZ mRNA inversely correlates with polymerase speed. Proc. Natl Acad. Sci. USA, 92, 12250-12254.
40. McCormick, J. R., Zengel, J. M. & Lindahl, L. (1994). Correlation of translation efficiency with the decay of lacZ mRNA in E. coli. J. Mol. Biol. 239, 608-622.
41. Miczak, A., Kaberdin, V. R., Wei, C. L. & Lin-Chao, S. (1996). Proteins associated with RNase E in a multi-component ribonucleolytic complex. Proc. Natl Acad. Sci. USA, 93, 3865-3869.
42. Morse, D. E. & Yanofsky, C. (1969). Polarity and the degradation of mRNA. Nature, 224, 329-331.
43. 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.
44. Murakawa, G. J., Kwan, C., Yamashita, J. & Nierlich, D. P. (1991). Transcription and decay of the lac messenger: role of an intergenic terminator. J. Bacteriol. 173, 28-36.
45. Nilsson, G., Belasco, J. G., Cohen, S. N. & von Gabain, A. (1987). Effect of premature termination of translation on mRNA stability depends on the site of ribosome release. Proc. Natl Acad. Sci. USA, 84, 4890-4894.
46. Ono, M. & Kuwano, M. (1979). A conditional lethal mutation in an E. coli strain with a longer chemical lifetime of messenger RNA. J. Mol. Biol. 129, 343-357.
47. Petersen, C. (1993). Translation and mRNA stability in bacteria: a complex relationship. In Control of Messenger RNA Stability (Belasco, J. G. & Brawerman, G., eds), pp. 117-145, Academic Press, San Diego and London.
48. Poot, R. A., Tsareva, N. V., Boni, I. V. & van Duin, J. (1997). RNA folding kinetics regulates translation of phage MS2 maturation gene. Proc. Natl Acad. Sci. USA, 94, 10110-10115.
49. Py, B., Higgins, C. F., Krish, H. M. & Carpousis, A. J. (1996). A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature, 381, 169-172.
50. Rapaport, L. R. & Mackie, G. A. (1994). Influence of translation efficiency on the stability of the mRNA for ribosomal protein S 20 in Escherichia coli. J. Bacteriol. 176, 992-998.
51. Rheinberger, H. J., Geigenmüller, U., Wedde, M. & Nierhaus, K. H. (1988). Parameters for the preparation of Escherichia coli ribosomes and ribosomal subunits active in tRNA binding. Methods Enzymol. 164, 658-670.
52. Russel, M., Gold, L., Morrisett, H. & O'Farrell, P. Z. (1976). Translational, autogenous regulation of gene 32 expression during bacteriophage T4 infection. J. Biol. Chem. 251, 7263-7270.
53. Ruteshouser, E. C. & Richardson, J. P. (1989). Identification and characterization of transcription termination sites in the Escherichia coli lacZ gene. J. Mol. Biol. 208, 23-43.
54. Sandler, P. & Weisblum, B. (1989). Erythromycin-induced ribosome stall in the ermA leader: a barricade to a 5′-to-3′ nucleolytic cleavage of the ermA transcript. J. Bacteriol. 171, 6680-6688.
55. Schneider, E., Blundell, M. & Kennell, D. (1978). Translation and mRNA decay. Mol. Gen. Genet. 160, 121-129.
56. Seraphin, B. & Rosbash, M. (1989). Identification of functional U1 snRNA-pre-mRNA complexes committed to spliceosome assembly and splicing. Cell, 59, 349-358.
57. Stanssens, P., Remaut, E. & Fiers, W. (1986). Inefficient translation initiation causes premature transcription termination in the lacZ gene. Cell, 44, 711-718.
58. Steitz, J. A. (1969). Polypeptide chain initiation: nucleotide sequences of the three ribosome binding sites in bacteriophage R17 RNA. Nature, 224, 957-964.
59. Stormo, G. D., Schneider, T. D. & Gold, L. M. (1982). Characterization of translational initiation sites in E. coli. Nucl. Acids Res. 10, 2971-2996.
60. Studier, F. W. & Moffatt, B. A. (1986). Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189, 113-130.
61. Uzan, M., Favre, R. & Brody, E. (1988). A nuclease that cuts specifically in the ribosome binding site of some T4 mRNAs. Proc. Natl Acad. Sci. USA, 85, 8895-8899.
62. von Gabain, A., Belasco, J. G., Schottel, J. L., Chang, A. C. & Cohen, S. N. (1983). Decay of mRNA in Escherichia coli: investigation of the fate of specific segments of transcripts. Proc. Natl Acad. Sci. USA, 80, 653-657.
63. Wagner, L. A., Gesteland, R. F., Dayhuff, T. J. & Weiss, R. B. (1994). An efficient Shine-Dalgarno sequence but not translation is necessary for lacZ mRNA stability in Escherichia coli. J. Bacteriol. 176, 1683-1688.
64. Xu, F. & Cohen, S. N. (1995). RNA degradation in Escherichia coli regulated by 3′ adenylation and 5′ phosphorylation. Nature, 374, 180-183.
65. Yarchuk, O., lost, I. & Dreyfus, M. (1991). The relation between translation and mRNA degradation in the lacZ gene. Biochimie, 73, 1533-1541.
66. Yarchuk, O., Jacques, N., Guillerez, J. & Dreyfus, M. (1992). Interdependence of translation, transcription and mRNA degradation in the lacZ gene. J. Mol. Biol. 226, 581-596.
67. Zuker, M. (1989). On finding all suboptimal foldings on an RNA molecule. Science, 244, 48-52.