Characterization of the role of ribonucleases in Salmonella small RNA decay

Nucleic Acids Research

Volumn 35, Issue 22, 2007, Pages 7651-7664

  Viegas, Sandra C ^a   Pfeiffer, Verena ^b   Sittka, Alexandra ^b   Silva, Inȩs J ^a   Vogel, Jörg ^b   Arraiano, Cecília M ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL RNA; CHAPERONE; NUCLEASE; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; POLYNUCLEOTIDE ADENYLYLTRANSFERASE 1; PROTEIN CSRB; PROTEIN CSRC; PROTEIN HFQ; PROTEIN MICA; PROTEIN SRAL; RIBONUCLEASE; RIBONUCLEASE E; RIBONUCLEASE G; RIBONUCLEASE III; SMALL RNA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; ENZYME ACTIVITY; GENE EXPRESSION; GENE EXPRESSION PROFILING; MUTAGENESIS; NONHUMAN; POLYADENYLATION; PRIORITY JOURNAL; RNA DEGRADATION; RNA STABILITY; SALMONELLA TYPHIMURIUM;

ENDORIBONUCLEASES; EXORIBONUCLEASES; MUTATION; POLYADENYLATION; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; RIBONUCLEASE III; RIBONUCLEASES; RNA STABILITY; RNA, BACTERIAL; RNA, UNTRANSLATED; SALMONELLA TYPHIMURIUM;

ENTEROBACTERIACEAE; SALMONELLA; SALMONELLA TYPHIMURIUM;

EID: 38049028411     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm916     Document Type: Article

References (87)

1. Majdalani,N., Vanderpool,C.K. and Gottesman,S. (2005) Bacterial small RNA regulators. Crit. Rev. Biochem. Mol. Biol., 40, 93-113.
2. Storz,G., Altuvia,S. and Wassarman,K.M. (2005) An abundance of RNA regulators. Annu. Rev. Biochem., 74, 199-217.
3. Vogel,J. and Sharma,C.M. (2005) How to find small non-coding RNAs in bacteria. Biol. Chem., 386, 1219-1238.
4. Hershherg,R., Altuvia,S. and Margalit,H. (2003) A survey of small RNA-encoding genes in Escherichia coli. Nucleic Acids Res., 31 1813-1820.
5. Storz,G., Opdyke,J.A. and Zhang,A. (2004) Controlling mRNA stability and translation with small, noncoding RNAs. Curr. Opin. Microbiol., 7, 140-144.
6. Massé,E., Escorcia,F.E. and Gottesman,S. (2003) Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev., 17, 2374-2383.
7. Rasmussen,A.A., Eriksen,M., Gilany,K., Udesen,C., Franch,T., Petersen,C. and Valentin-Hansen,P. (2005) Regulation of ompA mRNA stability: The role of a small regulatory RNA in growth phase-dependent control. Mol. Microbiol., 58, 1421-1429.
8. Valentin-Hansen,P., Eriksen,M. and Udesen,C. (2004) The bacterial Sm-like protein Hfq: A key player in RNA transactions. Mol. Microbiol., 51, 1525-1533.
9. Aiba,H. (2007) Mechanism of RNA silencing by Hfq-binding small RNAs. Curr. Opin. Microbiol., 10, 134-139.
10. Urban,J.H. and Vogel,J. (2007) Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res., 35, 1018-1037.
11. Vogel,J., Bartels,V., Tang,T.H., Churakov,G., Slagter-Jager,J.G., Huttenbofer,A. and Wagner,E.G. (2003) RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res., 31, 6435-6443.
12. Régnier,P. and Arraiano,C.M. (2000) Degradation of mRNA in bacteria: emergence of ubiquitous features. Bioessays, 22, 235-244.
13. Arraiano,C.M. and Maquat,L.E. (2003) Post-transcriptional control of gene expression: Effectors of mRNA decay. Mol. Microbiol., 49 267-276.
14. Carpousis,A.J., Van Houwe,G., Ehretsmann,C. and 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.
15. Carpousis,A.J., Vanzo,N.F. and Raynal,L.C. (1999) mRNA degradation. A tale of poly(A) and multiprotein machines. Trends Genet., 15 24-28.
16. Lee,K., Bernstein,J.A. and Cohen,S.N. (2002) RNase G complementation of rne null mutation identifies functional interrelationships with RNase E in Escherichia coli. Mol. Microbiol., 43, 1445-1456.
17. 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.
18. Ow,M.C., Perwez,T. and Kushner,S.R. (2003) RNase G of Escherichia coli exhibits only limited functional overlap with its essential homologue, RNase E. Mol. Microbiol., 49, 607-622.
19. Nicholson,A.W. (1999) Function, mechanism and regulation of bacterial ribonucleases. FEMS Microbiol. Rev., 23, 371-390.
20. Santos,J.M., Drider,D., Marujo,P.E., Lopez,P. and Arraiano,C.M. (1997) Determinant role of E. coli RNase III in the decay of both specific and heterologous mRNAs. FEMS Microbiol. Lett., 157, 31-38.
21. Régnier,P. and Grunberg-Manago,M. (1990) RNase III cleavages in non-coding leaders of Escherichia coli transcripts control mRNA stability and genetic expression. Biochimie, 72, 825-834.
22. Frazão,C., McVey,C.E., Amblar,M., Barbas,A., Vonrhein,C., Arraiano,C.M. and Carrondo,M.A. (2006) Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature, 443, 110-114.
23. Amblar,M., Barbas,A., Gomez-Puertas,P. and Arraiano,C.M. (2007) The role of the S1 domain in exoribonucleolytic activity: Substrate specificity and multimerization. RNA, 13, 317-327.
24. Mohanty,B.K. and Kushner,S.R. (2000) Polynucleotide phosphorylase functions both as a 3′ right-arrow 5′ exonuclease and a poly(A) polymerase in Escherichia coli. Proc. Natl Acad. Sci. USA, 97 11966-11971.
25. Cairrão,F., Cruz,A., Mori,H. and Arraiano,C.M. (2003) Cold shock induction of RNase R and its role in the maturation of the quality control mediator SsrA/tmRNA. Mol. Microbiol., 50, 1349-1360.
26. Sarkar,N. (1997) Polyadenylation of mRNA in prokaryotes. Annu. Rev. Biochem., 66, 173-197.
27. Hajnsdorf,E., Braun,F., Haugel-Nielsen,J. and Regnier,P. (1995) Polyadenylylation destabilizes the rpsO mRNA of Escherichia coli. Proc. Natl Acad. Sci. USA, 92, 3973-3977.
28. Xu,F. and Cohen,S.N. (1995) RNA degradation in Escherichia coli regulated by 3′ adenylation and 5′ phosphorylation. Nature, 374, 180-183.
29. O'Hara,E.B., Chekanova,J.A., Ingle,C.A., Kushner,Z.R., Peters,E. and Kushner,S.R. (1995) Polyadenylylation helps regulate mRNA decay in Escherichia coli. Proc. Natl Acad Sci. USA, 92, 1807-1811.
30. Marujo,P.E., Hajnsdorf,E., Le Derout,J., Andrade,R., Arraiano,C.M. and Régnier,P. (2000) RNase II removes the oligo(A) tails that destabilize the rpsO mRNA of Escherichia coli. RNA, 6, 1185-1193.
31. Santos,J.M., Freire,P., Mesquita,F.S., Mika,F., Hengge,R. and Arraiano,C.M. (2006) Poly(A)-polymerase 1 links transcription with mRNA degradation via sigmaS proteolysis. Mol. Microbiol., 60, 177-188.
32. Altier,C., Suyemoto,M., Ruiz,A.I., Burnham,K.D. and Maurer,R. (2000) Characterization of two novel regulatory genes affecting Salmonella invasion gene expression. Mol. Microbiol., 35, 635-646.
33. Fortune,D.R., Suyemoto,M. and Altier,C. (2006) Identification of CsrC and characterization of its role in epithelial cell invasion in Salmonella enterica serovar Typhimurium. Infect. Immun., 74 331-339.
34. Liu,M.Y., Gui,G., Wei,B., Preston,J.F.III, Oakford,L., Yuksel,U., Giedroc,D.P. and Romeo,T. (1997) The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J. Biol. Chem., 272, 17502-17510.
35. Udekwu,K.I., Darfeuille,F., Vogel,J., Reimegard,J., Holmqvist,E. and Wagner,E.G. (2005) Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes Dev., 19 2355-2366.
36. Bossi,L. and Figueroa-Bossi,N. (2007) A small RNA downregulates LamB maltoporin in Salmonella. Mol. Microbiol., 65, 799-810.
37. Andrade,J.M., Cairrã6,17. and Arraiano,C.M. (2006) RNase R affects gene expression in stationary phase: Regulation of ompA. Mol. Microbiol., 60, 219-228.
38. Argaman,L., Hershberg,R., Vogel,J., Bejerano,C., Wagner,E.G., Margalit,H. and Altuvia,S. (2001) Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr. Biol., 11, 941-950.
39. Zhang,A., Wassarman,K.M., Rosenow,C., Tjaden,B.C., Storz,G. and Gottesman,S. (2003) Global analysis of small RNA and mRNA targets of Hfq. Mol. Microbiol., 50, 1111-1124.
40. 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.
41. Schmieger,H. (1971) The fate of the bacterial chromosome in P22-infected cells of Salmonella typhimurium. Mol. Gen. Genet., 110, 238-244.
42. Sittka,A., Pfeiffer,V., Tedin,K. and Vogel,J. (2007) The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol. Microbiol., 63, 193-217.
43. Lober,S., Jackel,D., Kaiser,N. and Hensel,M. (2006) Regulation of Salmonella pathogenicity island 2 genes by independent environmental signals. Int. J. Med Microbiol., 296, 435-447.
44. McClelland,M., Sanderson,K.E., Spieth,J., Clifton,S.W., Latreille,P., Courtney,L., Porwollik,S., Ali,J., Dante,M. et al. (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium, LT2. Nature, 413, 852-856.
45. Arraiano,C.M., Yancey,S.D. and Kushner,S.R. (1988) Stabilization of discrete mRNA breakdown products in ams pnp rnb multiple mutants of Escherichia coli K-12. J. Bacteriol., 170, 4625-4633.
46. Viegas,S.C., Schmidt,D., Kasche,V., Arraiano,C.M. and Ignatova,Z. (2005) Effect of the increased stability of the penicillin amidase mRNA on the protein expression levels. FEBS Lett., 579, 5069-5073.
47. Cairrão,F. and Arraiano,C.M. (2006) The role of endoribonucleases in the regulation of RNase R. Biochem. Biophys. Res. Commun., 343 731-737.
48. Vanzo,N.F., Li,Y.S., Py,B., Blum,E., Higgins,C.F., Raynal,L.C., Krisch,H.M. and Carpousis,A.J. (1998) Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev., 12, 2770-2781.
49. Lopez,P.J., Marchand.I., Joyce,S.A. and 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.
50. Ow,M.C., Liu,Q. and 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.
51. Amblar,M., Viegas,S.C., López,P. and Arraiano,C.M. (2004) Homologous and heterologous expression of RNase III from Lactococcus lactis. Biochem. Biophys. Res. Commun., 323, 884-890.
52. Burgin,A.B., Parodos,K., Lane,D.J. and Pace,N.R. (1990) The excision of intervening sequences from Salmonella 23S ribosomal RNA. Cell 60, 405-414.
53. Altuvia,S., Weinstein-Fischer,D., Zhang,A., Postow,L. and Storz,G. (1997) A small, stable RNA induced by oxidative stress: Role as a pleiotropic regulator and antimutator. Cell, 90, 43-53.
54. Vogel,J., Argaman,L., Wagner,E.G. and Altuvia,S. (2004) The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr. Biol. 14, 2271-2276.
55. Sledjeski,D.D., Gupta,A. and Gottesman,S. (1996) The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coll. EMBO J., 15, 3993-4000.
56. Masse, E. and Gottesman,S. (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc. Natl Acad. Sci. USA, 99, 4620-4625.
57. Delihas,N. and Forst,S. (2001) MicF: An antisense RNA gene involved in response of Escherichia coli to global stress factors. J. Mol. Biol., 313, 1-12.
58. Wassarman,K.M., Repoila,F., Rosenow,C., Storz,G. and Gottesman,S. (2001) Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev., 15, 1637-1651.
59. Song,M., Kim,H.J., Kim,E.Y., Shin,M., Lee,H.C., Hong,Y., Rhee.,J.H., Yoon,H., Ryu,S. et al. (2004) ppGpp-dependent stationary phase induction of genes on Salmonella pathogenicity island 1. J. Biol. Chem., 279, 34183-34190.
60. Lee,C.A. and Falkow,S. (1990) The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. Proc. Natl Acad. Sci. USA, 87, 4304-4308.
61. Figueroa-Bossi,N., Lemire,S., Maloriol,D., Balbontin,R., Casadesus,J. and Bossi,L. (2006) Loss of Hfq activates the sigmaE-dependent envelope stress response in Salmonella enterica. Mol. Microbiol., 62, 838-852.
62. Papenfort,K., Pfeiffer,V., Mika,F., Lucchini,S., Hinton,J.C. and Vogel,J. (2006) SigmaE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol. Microbiol., 62, 1674-1688.
63. Altier,C., Suyemoto,M. and Lawhon,S.D. (2000) Regulation of Salmonella enterica serovar typhimurium invasion genes by csrA. Infect. Immun., 68, 6790-6797.
64. Jones,A.M., Goodwill,A. and Elliott,T. (2006) Limited role for the DsrA and RprA regulatory RNAs in rpoS regulation in Salmonella enterica: J. Bacteriol., 188, 5077-5088.
65. Romeo,T., Gong,M., Liu,M.Y. and Brun-Zinkernagel,A.M. (1993) Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J. Bacteriol., 175, 4744-4755.
66. Liu,M.Y., Yang,H. and Romeo,T. (1995) The product of the pleiotropic Escherichia coli gene csrA modulates glycogen bio-synthesis via effects on mRNA stability. J. Bacteriol., 177, 2663-2672.
67. Lawhon,S.D., Frye,J.G., Suyemoto,M., Porwollik,S., McClelland,M. and Altier,C. (2003) Global regulation by CsrA in Salmonella typhimurium. Mol. Microbiol., 48, 1633-1645.
68. Eriksson,S., Lucchini,S., Thompson,A., Rhen,M. and Hinton,J.C. (2003) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol., 47, 103-118.
69. Johansen,J., Rasmussen,A.A., Overgaard,M. and Valentin-Hansen, P. (2006) Conserved small non-coding RNAs that belong to the sigmaE regulon: Role in down-regulation of outer membrane proteins. J. Mol. Biol., 364, 1-8.
70. Udekwu,K.I. and Wagner,E.G. (2007) Sigma E controls biogenesis of the antisense RNA MicA. Nucleic Acids Res., 35, 1279-1288.
71. Davis,B.M. and Waldor,M.K. (2007) RNase E-dependent processing stabilizes MicX, a Vibrio cholerae sRNA. Mol. Microbiol., 65, 373-385.
72. Suzuki,K., Babitzke,P., Kushner,S.R. and Romeo,T. (2006) Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev., 20 2605-2617.
73. Cheng,Z.F. and Deutscher,M.P. (2005) An important role for RNase R in mRNA decay. Mol. Cell, 17, 313-318.
74. Mackie,G.A. (1998) Ribonuclease E is a 5'-end-dependent endonuclease. Nature, 395, 720-723.
75. Vincent,H.A. a:nD Deutscher,M.P. (2006) Substrate recognition and catalysis by the exoribonuclease RNase R. J. Biol. Chem., 281 29769-29775.
76. Coburn,G.A. and Mackie,G.A. (1998) Reconstitution of the degradation of the mRNA for ribosomal protein S20 with purified enzymes. J. Mol. Biol., 279, 1061-1074.
77. Cohen,S.N. (1995) Surprises at the 3' end of prokaryotic RNA. Cell 80, 829-832.
78. Dam Mikkelsen,N. and Gerdes,K. (1997) Sok antisense RNA from plasmid R1 is functionally inactivated by RNase E and poly-adenylated by poly(A) polymerase I. Mol. Microbiol., 26, 311-320.
79. Soderbom,F., Binnie,U., Masters,M. and Wagner,E.G. (1997) Regulation of plasmid R1 replication: PcnB and R Nase E expedite the decay of the antisense RNA,CopA. Mol. Microbiol., 26, 493-504.
80. Melefors,O. and von Gabain,A. (1988) Site-specific endonucleolytic cleavages and the regulation of stability of E. coli ompA mRNA. Cell, 52, 893-901.
81. Udekwu,K.I. (2007) Ph.D. thesis, Uppsala University, Uppsala.
82. Carmell,M.A. and Hannon,G.J. (2004) RNase III enzymes and the initiation of gene silencing. Nat. Struct. Mol. Biol., 11, 214-218.
83. Darfeuille,F., Unoson,C., Vogel,J. and Wagner,E.G. (2007) An antisense RNA inhibits translation by competing with standby ribosomes. Mol. Cell, 26, 381-392.
84. Afonyushkin, T., Vecerek,B., Moll,I., Blasi,U. and Kaberdin,V.R. (2005) Both RNase E and RNase III control the stability of sodB mRNA upon translational inhibition by the small regulatory RNA RyhB. Nucleic Acids Res., 33, 1678-1689.
85. Huntzinger,E., Boisset,S., Saveanu,C., Benito,Y., Geissmann,T., Namane,A., Lina,G., Etienne,J., Ehresmann,B. et al. (2005) Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. EMBO J., 24 824-835.
86. Boisset,S., Geissmann,T., Huntzinger,E., Fechter,P., Bendridi,N., Possedko,M., Chevalier,C., Helfer,A.C., Benito,Y. et al. (2007) Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev., 21, 1353-1366.
87. Hoiseth,S.K. and Stocker,B.A. (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature, 291, 238-239.