Gene expression control by selective RNA processing and stabilization in bacteria

FEMS Microbiology Letters

Volumn 344, Issue 2, 2013, Pages 104-113

  Rochat, Tatiana ^a   Bouloc, Philippe ^b   Repoila, Francis ^c  

^a INRA Institut National de la Recherche Agronomique   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UMR1319 MICALIS   (France)

Author keywords

Post transcriptional regulation; RNA degradation; RNA maturation; RNA stability; RNase; Translation

Indexed keywords

MESSENGER RNA; RIBOSOME RNA; RNA; TRANSFER RNA;

BACILLUS SUBTILIS; ESCHERICHIA COLI; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; NONHUMAN; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; REVIEW; RNA CLEAVAGE; RNA DEGRADATION; RNA PROCESSING; RNA SEQUENCE; STAPHYLOCOCCUS AUREUS;

BACTERIA; GENE EXPRESSION REGULATION, BACTERIAL; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, BACTERIAL;

EID: 84879501375     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/1574-6968.12162     Document Type: Review

References (73)

1. Amitai S, Kolodkin-Gal I, Hananya-Meltabashi M, Sacher A & Engelberg-Kulka H (2009) Escherichia coli MazF leads to the simultaneous selective synthesis of both "death proteins" and "survival proteins". PLoS Genet 5: e1000390.
2. Arraiano CM, Andrade JM, Domingues S et al. (2010) The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol Rev 34: 883-923.
3. Bandyra KJ, Said N, Pfeiffer V, Gorna MW, Vogel J & Luisi BF (2012) The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E. Mol Cell 47: 943-953.
4. Belasco JG (2010) All things must pass: contrasts and commonalities in eukaryotic and bacterial mRNA decay. Nat Rev Mol Cell Biol 11: 467-478.
5. Britton RA, Wen T, Schaefer L et al. (2007) Maturation of the 5' end of Bacillus subtilis 16S rRNA by the essential ribonuclease YkqC/RNase J1. Mol Microbiol 63: 127-138.
6. Brock JE, Pourshahian S, Giliberti J, Limbach PA & Janssen GR (2008) Ribosomes bind leaderless mRNA in Escherichia coli through recognition of their 5'-terminal AUG. RNA 14: 2159-2169.
7. Burton ZF, Gross CA, Watanabe KK & Burgess RR (1983) The operon that encodes the sigma subunit of RNA polymerase also encodes ribosomal protein S21 and DNA primase in E. coli K12. Cell 32: 335-349.
8. Caron MP, Lafontaine DA & Masse E (2010) Small RNA-mediated regulation at the level of transcript stability. RNA Biol 7: 140-144.
9. Caron MP, Bastet L, Lussier A, Simoneau-Roy M, Masse E & Lafontaine DA (2012) Dual-acting riboswitch control of translation initiation and mRNA decay. P Natl Acad Sci USA 109: E3444-E3453.
10. Carpousis AJ (2007) The RNA Degradosome of Escherichia coli: an mRNA-Degrading Machine Assembled on RNase E. Annu Rev Microbiol 61: 71-87.
11. Celesnik H, Deana A & Belasco JG (2007) Initiation of RNA decay in Escherichia coli by 5' pyrophosphate removal. Mol Cell 27: 79-90.
12. Commichau FM, Rothe FM, Herzberg C et al. (2009) Novel activities of glycolytic enzymes in Bacillus subtilis: interactions with essential proteins involved in mRNA processing. Mol Cell Proteomics 8: 1350-1360.
13. Condon C (2003) RNA processing and degradation in Bacillus subtilis. Microbiol Mol Biol Rev 67: 157-174.
14. Condon C (2007) Maturation and degradation of RNA in bacteria. Curr Opin Microbiol 10: 271-278.
15. Condon C (2010) What is the role of RNase J in mRNA turnover? RNA Biol 7: 316-321.
16. Condon C & Bechhofer DH (2011) Regulated RNA stability in the Gram positives. Curr Opin Microbiol 14: 148-154.
17. Deutscher MP (2009) Maturation and degradation of ribosomal RNA in bacteria. Prog Mol Biol Transl Sci 85: 369-391.
18. Fouquier d'Herouel A, Wessner F, Halpern D et al. (2011) A simple and efficient method to search for selected primary transcripts: non-coding and antisense RNAs in the human pathogen Enterococcus faecalis. Nucleic Acids Res 39: e46.
19. Frohlich KS & Vogel J (2009) Activation of gene expression by small RNA. Curr Opin Microbiol 12: 674-682.
20. Gorna MW, Carpousis AJ & Luisi BF (2012) From conformational chaos to robust regulation: the structure and function of the multi-enzyme RNA degradosome. Q Rev Biophys 45: 105-145.
21. Gorski K, Roch JM, Prentki P & Krisch HM (1985) The stability of bacteriophage T4 gene 32 mRNA: a 5' leader sequence that can stabilize mRNA transcripts. Cell 43: 461-469.
22. Ikeda Y, Yagi M, Morita T & Aiba H (2011) Hfq binding at RhlB-recognition region of RNase E is crucial for the rapid degradation of target mRNAs mediated by sRNAs in Escherichia coli. Mol Microbiol 79: 419-432.
23. Kalamorz F, Reichenbach B, Marz W, Rak B & Gorke B (2007) Feedback control of glucosamine-6-phosphate synthase GlmS expression depends on the small RNA GlmZ and involves the novel protein YhbJ in Escherichia coli. Mol Microbiol 65: 1518-1533.
24. Khemici V, Poljak L, Luisi BF & Carpousis AJ (2008) The RNase E of Escherichia coli is a membrane-binding protein. Mol Microbiol 70: 799-813.
25. Kreikemeyer B, Boyle MD, Buttaro BA, Heinemann M & Podbielski A (2001) Group A streptococcal growth phase-associated virulence factor regulation by a novel operon (Fas) with homologies to two-component-type regulators requires a small RNA molecule. Mol Microbiol 39: 392-406.
26. Lasa I, Toledo-Arana A, Dobin A et al. (2011) Genome-wide antisense transcription drives mRNA processing in bacteria. P Natl Acad Sci USA 108: 20172-20177.
27. Laursen BS, Sorensen HP, Mortensen KK & Sperling-Petersen HU (2005) Initiation of protein synthesis in bacteria. Microbiol Mol Biol Rev 69: 101-123.
28. Lehnik-Habrink M, Schaffer M, Mader U, Diethmaier C, Herzberg C & Stulke J (2011a) RNA processing in Bacillus subtilis: identification of targets of the essential RNase Y. Mol Microbiol 81: 1459-1473.
29. Lehnik-Habrink M, Newman J, Rothe FM et al. (2011b) RNase Y in Bacillus subtilis: a Natively disordered protein that is the functional equivalent of RNase E from Escherichia coli. J Bacteriol 193: 5431-5441.
30. Lehnik-Habrink M, Lewis RJ, Mader U & Stulke J (2012) RNA degradation in Bacillus subtilis: an interplay of essential endo- and exoribonucleases. Mol Microbiol 84: 1005-1017.
31. Li de la Sierra-Gallay I, Zig L, Jamalli A & Putzer H (2008) Structural insights into the dual activity of RNase J. Nat Struct Mol Biol 15: 206-212.
32. Ludwig H, Homuth G, Schmalisch M, Dyka FM, Hecker M & Stulke J (2001) Transcription of glycolytic genes and operons in Bacillus subtilis: evidence for the presence of multiple levels of control of the gapA operon. Mol Microbiol 41: 409-422.
33. Mackie GA (1998) Ribonuclease E is a 5'-end-dependent endonuclease. Nature 395: 720-723.
34. Mackie GA (2013) RNase E: at the interface of bacterial RNA processing and decay. Nat Rev Microbiol 11: 45-57.
35. MacRae IJ & Doudna JA (2007) Ribonuclease revisited: structural insights into ribonuclease III family enzymes. Curr Opin Struct Biol 17: 138-145.
36. Malys N & McCarthy JE (2011) Translation initiation: variations in the mechanism can be anticipated. Cell Mol Life Sci 68: 991-1003.
37. Marujo PE, Braun F, Haugel-Nielsen J, Le Derout J, Arraiano CM & Regnier P (2003) Inactivation of the decay pathway initiated at an internal site by RNase E promotes poly(A)-dependent degradation of the rpsO mRNA in Escherichia coli. Mol Microbiol 50: 1283-1294.
38. Mathy N, Benard L, Pellegrini O, Daou R, Wen T & Condon C (2007) 5'-to-3' exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5' stability of mRNA. Cell 129: 681-692.
39. McCullen CA, Benhammou JN, Majdalani N & Gottesman S (2010) Mechanism of positive regulation by DsrA and RprA small noncoding RNAs: pairing increases translation and protects rpoS mRNA from degradation. J Bacteriol 192: 5559-5571.
40. Moll I, Grill S, Gualerzi CO & Blasi U (2002) Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control. Mol Microbiol 43: 239-246.
41. Morita T, Maki K & Aiba H (2005) RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev 19: 2176-2186.
42. Mudd EA, Prentki P, Belin D & Krisch HM (1988) Processing of unstable bacteriophage T4 gene 32 mRNAs into a stable species requires Escherichia coli ribonuclease E. EMBO J 7: 3601-3607.
43. Newbury SF, Smith NH & Higgins CF (1987a) Differential mRNA stability controls relative gene expression within a polycistronic operon. Cell 51: 1131-1143.
44. Newbury SF, Smith NH, Robinson EC, Hiles ID & Higgins CF (1987b) Stabilization of translationally active mRNA by prokaryotic REP sequences. Cell 48: 297-310.
45. Obana N, Shirahama Y, Abe K & Nakamura K (2010) Stabilization of Clostridium perfringens collagenase mRNA by VR-RNA-dependent cleavage in 5' leader sequence. Mol Microbiol 77: 1416-1428.
46. Olson PD, Kuechenmeister LJ, Anderson KL et al. (2011) Small molecule inhibitors of Staphylococcus aureus RnpA alter cellular mRNA turnover, exhibit antimicrobial activity, and attenuate pathogenesis. PLoS Pathog 7: e1001287.
47. Prevost K, Desnoyers G, Jacques JF, Lavoie F & Masse E (2011) Small RNA-induced mRNA degradation achieved through both translation block and activated cleavage. Genes Dev 25: 385-396.
48. Ramirez-Pena E, Trevino J, Liu Z, Perez N & Sumby P (2010) The group A Streptococcus small regulatory RNA FasX enhances streptokinase activity by increasing the stability of the ska mRNA transcript. Mol Microbiol 78: 1332-1347.
49. Repoila F & Darfeuille F (2009) Small regulatory non-coding RNAs in bacteria: physiology and mechanistic aspects. Biol Cell 101: 117-131.
50. Resch A, Afonyushkin T, Lombo TB, McDowall KJ, Blasi U & Kaberdin VR (2008) Translational activation by the noncoding RNA DsrA involves alternative RNase III processing in the rpoS 5'-leader. RNA 14: 454-459.
51. Richards J, Liu Q, Pellegrini O et al. (2011) An RNA pyrophosphohydrolase triggers 5'-exonucleolytic degradation of mRNA in Bacillus subtilis. Mol Cell 43: 940-949.
52. Roux CM, DeMuth JP & Dunman PM (2011) Characterization of components of the Staphylococcus aureus mRNA degradosome holoenzyme-like complex. J Bacteriol 193: 5520-5526.
53. Sanson B & Uzan M (1995) Post-transcriptional controls in bacteriophage T4: roles of the sequence-specific endoribonuclease RegB. FEMS Microbiol Rev 17: 141-150.
54. Schmidtke C, Findeiss S, Sharma CM et al. (2012) Genome-wide transcriptome analysis of the plant pathogen Xanthomonas identifies sRNAs with putative virulence functions. Nucleic Acids Res 40: 2020-2031.
55. Shahbabian K, Jamalli A, Zig L & Putzer H (2009) RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis. EMBO J 28: 3523-3533.
56. Sharma CM, Hoffmann S, Darfeuille F et al. (2010) The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464: 250-255.
57. Silva IJ, Saramago M, Dressaire C, Domingues S, Viegas SC & Arraiano CM (2011) Importance and key events of prokaryotic RNA decay: the ultimate fate of an RNA molecule. Wiley Interdiscip Rev RNA 2: 818-836.
58. Sobrero P & Valverde C (2012) The bacterial protein Hfq: much more than a mere RNA-binding factor. Crit Rev Microbiol 38: 276-299.
59. Stazic D, Lindell D & Steglich C (2011) Antisense RNA protects mRNA from RNase E degradation by RNA-RNA duplex formation during phage infection. Nucleic Acids Res 39: 4890-4899.
60. Taverniti V, Forti F, Ghisotti D & Putzer H (2011) Mycobacterium smegmatis RNase J is a 5'-3' exo-/endoribonuclease and both RNase J and RNase E are involved in ribosomal RNA maturation. Mol Microbiol 82: 1260-1276.
61. Tsai YC, Du D, Dominguez-Malfavon L et al. (2012) Recognition of the 70S ribosome and polysome by the RNA degradosome in Escherichia coli. Nucleic Acids Res 40: 10417-10431.
62. Udagawa T, Shimizu Y & Ueda T (2004) Evidence for the translation initiation of leaderless mRNAs by the intact 70 S ribosome without its dissociation into subunits in eubacteria. J Biol Chem 279: 8539-8546.
63. Urban JH & Vogel J (2008) Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation. PLoS Biol 6: e64.
64. Vecerek B, Beich-Frandsen M, Resch A & Blasi U (2010) Translational activation of rpoS mRNA by the non-coding RNA DsrA and Hfq does not require ribosome binding. Nucleic Acids Res 38: 1284-1293.
65. Vesper O, Amitai S, Belitsky M, Byrgazov K, Kaberdina AC, Engelberg-Kulka H & Moll I (2011) Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell 147: 147-157.
66. Vogel J & Luisi BF (2011) Hfq and its constellation of RNA. Nat Rev Microbiol 9: 578-589.
67. Wagner EG (2009) Kill the messenger: bacterial antisense RNA promotes mRNA decay. Nat Struct Mol Biol 16: 804-806.
68. Waters LS & Storz G (2009) Regulatory RNAs in bacteria. Cell 136: 615-628.
69. Winkler WC, Nahvi A, Roth A, Collins JA & Breaker RR (2004) Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428: 281-286.
70. Yajnik V & Godson GN (1993) Selective decay of Escherichia coli dnaG messenger RNA is initiated by RNase E. J Biol Chem 268: 13253-13260.
71. Yamaguchi Y & Inouye M (2009) mRNA interferases, sequence-specific endoribonucleases from the toxin-antitoxin systems. Prog Mol Biol Transl Sci 85: 467-500.
72. Zhang Y, Zhang J, Hoeflich KP, Ikura M, Qing G & Inouye M (2003) MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Mol Cell 12: 913-923.
73. Zheng X, Hu GQ, She ZS & Zhu H (2011) Leaderless genes in bacteria: clue to the evolution of translation initiation mechanisms in prokaryotes. BMC Genomics 12: 361.