Mycobacterium smegmatis RNase J is a 5'-3' exo-/endoribonuclease and both RNase J and RNase E are involved in ribosomal RNA maturation

Molecular Microbiology

Volumn 82, Issue 5, 2011, Pages 1260-1276

  Taverniti, Valerio ^a,b   Forti, Francesca ^a   Ghisotti, Daniela ^a   Putzer, Harald ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEASE; RIBONUCLEASE E; RIBONUCLEASE J; RIBOSOME RNA; RNA 16S; RNA 23S; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PRIORITY JOURNAL; RNA CLEAVAGE; RNA DEGRADATION; RNA METABOLISM; RNA PROCESSING;

BACILLUS SUBTILIS; ESCHERICHIA COLI; MODELS, BIOLOGICAL; MODELS, CHEMICAL; MODELS, MOLECULAR; MYCOBACTERIUM SMEGMATIS; RIBONUCLEASES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, BACTERIAL; RNA, RIBOSOMAL;

BACILLUS SUBTILIS; ESCHERICHIA COLI; MYCOBACTERIUM SMEGMATIS;

EID: 82155166270     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07888.x     Document Type: Article

References (51)

1. Agaisse, H., and Lereclus, D. (1996) STAB-SD: a Shine-Dalgarno sequence in the 5' untranslated region is a determinant of mRNA stability. Mol Microbiol 20: 633-643.
2. Arraiano, C.M., Andrade, J.M., Domingues, S., Guinote, I.B., Malecki, M., Matos, R.G., etal. (2010) The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol Rev 34: 883-923.
3. Baker, K.E., and Mackie, G.A. (2003) Ectopic RNase E sites promote bypass of 5'-end-dependent mRNA decay in Escherichia coli. Mol Microbiol 47: 75-88.
4. Bardarov, S., Bardarov, S., Jr, Pavelka, M.S., Jr, Sambandamurthy, V., Larsen, M., Tufariello, J., etal.(2002) Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M.bovis BCG and M.smegmatis. Microbiology 148: 3007-3017.
5. Bechhofer, D.H., and Dubnau, D. (1987) Induced mRNA stability in Bacillus subtilis. Proc Natl Acad Sci USA 84: 498-502.
6. Bradford, M.M. (1976) A rapid and sensitive method for the quantitiation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
7. Britton, R.A., Wen, T., Schaefer, L., Pellegrini, O., Uicker, W.C., Mathy, N., etal. (2007) Maturation of the 5' end of Bacillus subtilis 16S rRNA by the essential ribonuclease YkqC/RNase J1. Mol Microbiol 63: 127-138.
8. Callebaut, I., Moshous, D., Mornon, J.P., and de Villartay, J.P. (2002) Metallo-beta-lactamase fold within nucleic acids processing enzymes: the beta-CASP family. Nucleic Acids Res 30: 3592-3601.
9. Carpousis, A.J., Luisi, B.F., and McDowall, K.J. (2009) Endonucleolytic initiation of mRNA decay in Escherichia coli. Prog Mol Biol Transl Sci 85: 91-135.
10. Clouet-d'Orval, B., Rinaldi, D., Quentin, Y., and Carpousis, A.J. (2010) Euryarchaeal beta-CASP proteins with homology to bacterial RNase J Have 5'- to 3'-exoribonuclease activity. J Biol Chem 285: 17574-17583.
11. Condon, C., and Putzer, H. (2002) The phylogenetic distribution of bacterial ribonucleases. Nucleic Acids Res 30: 5339-5346.
12. Daou-Chabo, R., and Condon, C. (2009) RNase J1 endonuclease activity as a probe of RNA secondary structure. RNA 15: 1417-1425.
13. Deana, A., Celesnik, H., and Belasco, J.G. (2008) The bacterial enzyme RppH triggers messenger RNA degradation by 5' pyrophosphate removal. Nature 451: 355-358.
14. Deutscher, M.P. (2009) Maturation and degradation of ribosomal RNA in bacteria. Prog Mol Biol Transl Sci 85: 369-391.
15. Dorléans, A., Li de la Sierra Gallay, I., Piton, J., Zig, L., Winieski, L., Putzer, H., and Condon, C. (2011) Molecular basis for the recognition and cleavage of RNA by the bifunctional 5'-3' exo/endoribonuclease RNase J. Structure 19: 1252-1261.
16. Ehretsmann, C., Carpousis, A.J., and Krisch, H.M. (1992) Specificity of Escherichia coli endoribonuclease RNAse E: in vivo and in vitro analysis of mutants in a bacteriophage T4 mRNA processing site. Genes Dev 6: 149-159.
17. Even, S., Pellegrini, O., Zig, L., Labas, V., Vinh, J., Brechemmier-Baey, D., and Putzer, H. (2005) Ribonucleases J1 and J2: two novel endoribonucleases in B.subtilis with functional homology to E. coli RNase E. Nucleic Acids Res 33: 2141-2152.
18. Forti, F., Crosta, A., and Ghisotti, D. (2009) Pristinamycin-inducible gene regulation in mycobacteria. J Biotechnol 140: 270-277.
19. Gonzalez-y-Merchand, J.A., Colston, M.J., and Cox, R.A. (1996) The rRNA operons of Mycobacterium smegmatis and Mycobacterium tuberculosis: comparison of promoter elements and of neighbouring upstream genes. Microbiology 142: 667-674.
20. Grant, S.G., Jessee, J., Bloom, F.R., and Hanahan, D. (1990) Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci USA 87: 4645-4649.
21. Hambraeus, G., Karhumaa, K., and Rutberg, B. (2002) A 5' stem-loop and ribosome binding site but not translation are important for the stability of Bacillus subtilis aprE leader mRNA. Microbiology 148: 1795-1803.
22. Hasenohrl, D., Konrat, R., and Blasi, U. (2011) Identification of an RNase J ortholog in Sulfolobus solfataricus: implications for 5'-to-3' directional decay and 5'-end protection of mRNA in Crenarchaeota. RNA 17: 99-107.
23. Herskowitz, M.A., and Bechhofer, D.H. (2000) Endoribonuclease RNase III is essential in Bacillus subtilis. Mol Microbiol 38: 1027-1033.
24. Ji, Y.E., Colston, M.J., and Cox, R.A. (1994a) The ribosomal RNA (rrn) operons of fast-growing mycobacteria: primary and secondary structures and their relation to rrn operons of pathogenic slow-growers. Microbiology 140: 2829-2840.
25. Ji, Y.E., Kempsell, K.E., Colston, M.J., and Cox, R.A. (1994b) Nucleotide sequences of the spacer-1, spacer-2 and trailer regions of the rrn operons and secondary structures of precursor 23S rRNAs and precursor 5S rRNAs of slow-growing mycobacteria. Microbiology 140: 1763-1773.
26. Laalami, S., and Putzer, H. (2011) mRNA degradation and maturation in prokaryotes: the global players. Biomol Concepts. DOI 10.1515/BMC.2011.042.
27. Lehnik-Habrink, M., Schaffer, M., Mader, U., Diethmaier, C., Herzberg, C., and Stulke, J. (2011) RNA processing in Bacillus subtilis: identification of targets of the essential RNase Y. Mol Microbiol 81: 1459-1473.
28. Li, Z., Pandit, S., and Deutscher, M.P. (1999) RNase G (CafA protein) and RNase E are both required for the 5' maturation of 16S ribosomal RNA. EMBO J 18: 2878-2885.
29. Li de la Sierra-Gallay, I., Zig, L., Jamalli, A., and Putzer, H. (2008) Structural insights into the dual activity of RNase J. Nat Struct Mol Biol 15: 206-212.
30. Loughney, K., Lund, E., and Dahlberg, J.E. (1983) Ribosomal RNA precursors of Bacillus subtilis. Nucleic Acids Res 11: 6709-6721.
31. Luo, D., Condon, C., Grunberg-Manago, M., and Putzer, H. (1998) In vitro and in vivo secondary structure probing of the thrS leader in Bacillus subtilis. Nucleic Acids Res 26: 5379-5387.
32. McDowall, K.J., Lin-Chao, S., and Cohen, S.N. (1994) A+U content rather than a particular nucleotide order determines the specificity of RNase E cleavage. J Biol Chem 269: 10790-10796.
33. Mackie, G.A. (1992) Secondary structure of the mRNA for ribosomal protein S20. Implications for cleavage by ribonuclease E. J Biol Chem 267: 1054-1061.
34. Mackie, G.A. (1998) Ribonuclease E is a 5'-end-dependent endonuclease. Nature 395: 720-723.
35. Mäder, U., Zig, L., Kretschmer, J., Homuth, G., and Putzer, H. (2008) mRNA processing by RNases J1 and J2 affects Bacillus subtilis gene expression on a global scale. Mol Microbiol 70: 183-196.
36. Madhugiri, R., and Evguenieva-Hackenberg, E. (2009) RNase J is involved in the 5'-end maturation of 16S rRNA and 23S rRNA in Sinorhizobium meliloti. FEBS Lett 583: 2339-2342.
37. Mathy, N., Benard, L., Pellegrini, O., Daou, R., Wen, T., and 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.
38. Mathy, N., Hebert, A., Mervelet, P., Benard, L., Dorleans, A., Li de la Sierra-Gallay, I., etal. (2010) Bacillus subtilis ribonucleases J1 and J2 form a complex with altered enzyme behaviour. Mol Microbiol 75: 489-498.
39. Milano, A., Forti, F., Sala, C., Riccardi, G., and Ghisotti, D. (2001) Transcriptional regulation of furA and katG upon oxidative stress in Mycobacterium smegmatis. J Bacteriol 183: 6801-6806.
40. Newman, J.A., Hewitt, L., Rodrigues, C., Solovyova, A., Harwood, C.R., and Lewis, R.J. (2011) Unusual, dual endo- and exo-nuclease activity in the degradosome explained by crystal structure analysis of RNase J1. Structure 19: 1241-1251.
41. Redko, Y., Bechhofer, D.H., and Condon, C. (2008) Mini-III, an unusual member of the RNase III family of enzymes, catalyses 23S ribosomal RNA maturation in B.subtilis. Mol Microbiol 68: 1096-1106.
42. Richards, J., Liu, Q., Pellegrini, O., Celesnik, H., Yao, S., Bechhofer, D.H., etal. (2011) An RNA pyrophosphohydrolase triggers 5'-exonucleolytic degradation of mRNA in Bacillus subtilis. Mol Cell 43: 940-949. DOI 10.1016/j.molcel.2011.07.023.
43. Sabbatini, R., Federico, M., Baldini, L., Barbieri, F., Maiolo, M.T., and Silingardi, V. (1995) A randomized, double-blind, cross-over study comparing a levosulpiride-based and a metoclopramide-based combination in the prevention of ProMECE-CytaBOM-induced emesis. Haematologica 80: 416-420.
44. Sala, C., Forti, F., Di Florio, E., Canneva, F., Milano, A., Riccardi, G., and Ghisotti, D. (2003) Mycobacterium tuberculosis FurA autoregulates its own expression. J Bacteriol 185: 5357-5362.
45. Sala, C., Forti, F., Magnoni, F., and Ghisotti, D. (2008) The katG mRNA of Mycobacterium tuberculosis and Mycobacterium smegmatis is processed at its 5' end and is stabilized by both a polypurine sequence and translation initiation. BMC Mol Biol 9: 33.
46. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
47. Shahbabian, K., Jamalli, A., Zig, L., and Putzer, H. (2009) RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis. EMBO J 28: 3523-3533.
48. Snapper, S.B., Melton, R.E., Mustafa, S., Kieser, T., and Jacobs, W.R., Jr (1990) Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol Microbiol 4: 1911-1919.
49. Stover, C.K., de la Cruz, V.F., Fuerst, T.R., Burlein, J.E., Benson, L.A., Bennett, L.T., etal. (1991) New use of BCG for recombinant vaccines. Nature 351: 456-460.
50. Young, R.A., and Steitz, J.A. (1978) Complementary sequences 1700 nucleotides apart form a ribonuclease III cleavage site in Escherichia coli ribosomal precursor RNA. Proc Natl Acad Sci USA 75: 3593-3597.
51. Zeller, M.E., Csanadi, A., Miczak, A., Rose, T., Bizebard, T., and Kaberdin, V.R. (2007) Quaternary structure and biochemical properties of mycobacterial RNase E/G. Biochem J 403: 207-215.