The modulation of Staphylococcus aureus mRNA turnover

Future Microbiology

Volumn 6, Issue 10, 2011, Pages 1141-1150

  Morrison, John M ^a   Dunman, Paul M ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

drug discovery; mRNA turnover; pathogenesis; ribonuclease; Staphylococcus aureus; virulence

Indexed keywords

ALPHA HEMOLYSIN; BACTERIAL PROTEIN; BACTERIAL RNA; CSRA PROTEIN; EXORIBONUCLEASE; MAZF PROTEIN; MESSENGER RNA; RIBONUCLEASE; RIBONUCLEASE E; RIBONUCLEASE H; RIBONUCLEASE III; RIBONUCLEASE J1; RIBONUCLEASE J2; RIBONUCLEASE P; RIBONUCLEASE R; RNA BINDING PROTEIN; SMAD ANCHOR FOR RECEPTOR ACTIVATION; TRANSFER RNA; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; ENZYME ACTIVITY; GENE EXPRESSION; NONHUMAN; PHYSIOLOGICAL STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RIBOSWITCH; RNA STABILITY; RNA TRANSCRIPTION; STAPHYLOCOCCUS AUREUS;

GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RIBONUCLEASES; RNA, BACTERIAL; RNA, MESSENGER; RNA-BINDING PROTEINS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE; VIRULENCE FACTORS;

POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

EID: 80054796832     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.11.102     Document Type: Article

References (74)

1. Klevens RM, Morrison MA, Nadle J, et al. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298(15), 1763-1771 (2007 (Pubitemid 47598444)
2. Novick RP. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 48(6), 1429-1449 (2003 (Pubitemid 36751052)
3. Bronner S, Monteil H, Prevost G. Regulation of virulence determinants in Staphylococcus aureus: complexity and applications. FEMS Microbiol. Rev. 28(2), 183-200 (2004 (Pubitemid 38510501)
4. Kolar SL, Nagarajan V, Oszmiana A, et al. NsaRS is a cell-envelope- stress-sensing two-component system of Staphylococcus aureus. Microbiology 157(Pt 8), 2206-2219 (2011
5. Ross J. mRNA stability in mammalian cells. Microbiol. Rev. 59(3), 423-450 (1995
6. Roberts C, Anderson KL, Murphy E, et al. Characterizing the effect of the Staphylococcus aureus virulence factor regulator, SarA, on log-phase mRNA half-lives. J. Bacteriol. 188(7), 2593-2603 (2006
7. Anderson KL, Roberts C, Disz T, et al. Characterization of the Staphylococcus aureus heat shock, cold shock, stringent, and SOS responses and their effects on log-phase mRNA turnover. J. Bacteriol. 188(19), 6739-6756 (2006 (Pubitemid 44497886)
8. Anderson KL, Roux CM, Olson MW, et al. Characterizing the effects of inorganic acid and alkaline shock on the Staphylococcus aureus transcriptome and messenger RNA turnover. FEMS Immunol. Med. Microbiol. 60(3), 208-250 (2010
9. Blickwede M, Goethe R, Wolz C, Valentin-Weigand P, Schwarz S. Molecular basis of florfenicol-induced increase in adherence of Staphylococcus aureus strain Newman. J. Antimicrob. Chemother. 56(2), 315-323 (2005 (Pubitemid 41158519)
10. Blickwede M, Wolz C, Valentin-Weigand P, Schwarz S. Influence of clindamycin on the stability of coa and fnbB transcripts and adherence properties of Staphylococcus aureus Newman. FEMS Microbiol. Lett. 252(1), 73-78 (2005 (Pubitemid 41446395)
11. Huntzinger E, Boisset S, Saveanu C, et al. Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. EMBO J. 24(4), 824-835 (2005 (Pubitemid 40396111)
12. Anderson KL, Dunman PM. Messenger RNA turnover processes in Escherichia coli, Bacillus subtilis, and emerging studies in Staphylococcus aureus. Int. J. Microbiol. 2009, 525491 (2009
13. Carpousis AJ, Van Houwe G, Ehretsmann C, Krisch HM. Copurification of E. coli RNAase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation. Cell 76(5), 889-900 (1994 (Pubitemid 24085326)
14. Miczak A, Kaberdin VR, Wei CL, Lin-Chao S. Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc. Natl Acad. Sci. USA 93(9), 3865-3869 (1996 (Pubitemid 26144213)
15. Py B, Causton H, Mudd EA, Higgins CF. A protein complex mediating mRNA degradation in Escherichia coli. Mol. Microbiol. 14(4), 717-729 (1994 (Pubitemid 24364589)
16. Belasco JG, Higgins CF. Mechanisms of mRNA decay in bacteria: a perspective. Gene 72(1-2), 15-23 (1988 (Pubitemid 19032223)
17. Vanzo NF, Li YS, Py B, et al. Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev. 12(17), 2770-2781 (1998 (Pubitemid 28420656)
18. Coburn GA, Miao X, Briant DJ, Mackie GA. Reconstitution of a minimal RNA degradosome demonstrates functional coordination between a 3′ exonuclease and a DEAD-box RNA helicase. Genes Dev. 13(19), 2594-2603 (1999 (Pubitemid 29489650)
19. Liou GG, Chang HY, Lin CS, Lin-Chao S. DEAD box RhlB RNA helicase physically associates with exoribonuclease PNPase to degrade double-stranded RNA independent of the degradosome-assembling region of RNase E. J. Biol. Chem. 277(43), 41157-41162 (2002 (Pubitemid 35215707)
20. Even S, Pellegrini O, Zig L, et al. Ribonucleases J1 and J2: two novel endoribonucleases in B. subtilis with functional homology to E. coli RNase E. Nucleic Acids Res. 33(7), 2141-2152 (2005 (Pubitemid 41439882)
21. Roux CM, Demuth JP, Dunman PM. Characterization of components of the Staphylococcus aureus messenger RNA degradosome holoenzyme-like complex. J. Bacteriol. 193(19), 5520-5526 (2011
22. Commichau FM, Rothe FM, Herzberg C, et al. Novel activities of glycolytic enzymes in Bacillus subtilis: interactions with essential proteins involved in mRNA processing. Mol. Cell Proteomics 8(6), 1350-1360 (2009)
23. Lehnik-Habrink M, Pfortner H, Rempeters L, Pietack N, Herzberg C, Stulke J. The RNA degradosome in Bacillus subtilis: identification of CshA as the major RNA helicase in the multi-protein complex. 77(4), 958-971 Mol. Microbiol. (2010
24. Boisset S, Geissmann T, Huntzinger E, et al. Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev. 21(11), 1353-1366 (2007 (Pubitemid 46871039)
25. Chevalier C, Boisset S, Romilly C, et al. Staphylococcus aureus RNAIII binds to two distant regions of coa mRNA to arrest translation and promote mRNA degradation. PLoS Pathog. 6(3), e1000809 (2010
26. Chevalier C, Huntzinger E, Fechter P, et al. Staphylococcus aureus endoribonuclease III purification and properties. Methods Enzymol. 447, 309-327 (2008
27. Evans D, Marquez SM, Pace NR. RNase P: interface of the RNA and protein worlds. Trends Biochem. Sci. 31(6), 333-341 (2006 (Pubitemid 43903240)
28. Olson PD, Kuechenmeister LJ, Anderson KL, et al. Small molecule inhibitors of Staphylococcus aureus RnpA alter cellular mRNA turnover, exhibit antimicrobial activity, and attenuate pathogenesis. PLoS Pathog. 7(2), e1001287 (2011
29. Mathy N, Benard L, Pellegrini O, Daou R, Wen T, Condon C. 5′-to-3′ exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5 stability of mRNA. Cell 129(4), 681-692 (2007 (Pubitemid 46802375)
30. Hunt A, Rawlins JP, Thomaides HB, Errington J. Functional analysis of 11 putative essential genes in Bacillus subtilis. Microbiology 152(Pt 10), 2895-2907 (2006 (Pubitemid 44542371)
31. Nagata M, Kaito C, Sekimizu K. Phosphodiesterase activity of CvfA is required for virulence in Staphylococcus aureus. J. Biol. Chem. 283(4), 2176-2184 (2008
32. Zuo Y, Deutscher MP. Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res. 29(5), 1017-1026 (2001 (Pubitemid 32186186)
33. Cheng ZF, Deutscher MP. Purification and characterization of the Escherichia coli exoribonuclease RNase R. Comparison with RNase II. J. Biol. Chem. 277(24), 21624-21629 (2002 (Pubitemid 34952311)
34. Cheng ZF, Deutscher MP. An important role for RNase R in mRNA decay. Mol. Cell 17(2), 313-318 (2005 (Pubitemid 40138624)
35. Oussenko IA, Sanchez R, Bechhofer DH. Bacillus subtilis YhaM, a member of a new family of 3′-to-5′ exonucleases in Gram-positive bacteria. J. Bacteriol. 184(22), 6250-6259 (2002 (Pubitemid 35265906)
36. Van Melderen L. Toxin-antitoxin systems: why so many, what for? Curr. Opin. Microbiol. 13(6), 781-785 (2010
37. Zhu L, Zhang Y, Teh JS, et al. Characterization of mRNA interferases from Mycobacterium tuberculosis. J. Biol. Chem. 281(27), 18638-18643 (2006 (Pubitemid 44035523)
38. Pellegrini O, Mathy N, Gogos A, Shapiro L, Condon C. The Bacillus subtilis ydcDE operon encodes an endoribonuclease of the MazF/PemK family and its inhibitor. Mol. Microbiol. 56(5), 1139-1148 (2005 (Pubitemid 40755999)
39. Fu Z, Donegan NP, Memmi G, Cheung AL. Characterization of MazFSa, an endoribonuclease from Staphylococcus aureus. J. Bacteriol. 189(24), 8871-8879 (2007
40. Fu Z, Tamber S, Memmi G, Donegan NP, Cheung AL. Overexpression of MazFsa in Staphylococcus aureus induces bacteriostasis by selectively targeting mRNAs for cleavage. J. Bacteriol. 191(7), 2051-2059 (2009
41. Folichon M, Arluison V, Pellegrini O, Huntzinger E, Regnier P, Hajnsdorf E. The poly(A) binding protein Hfq protects RNA from RNase E and exoribonucleolytic degradation. Nucleic Acids Res. 31(24), 7302-7310 (2003 (Pubitemid 38008458)
42. Masse E, Escorcia FE, Gottesman S. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev. 17(19), 2374-2383 (2003 (Pubitemid 37214786)
43. Liu MY, Romeo T. The global regulator CsrA of Escherichia coli is a specific mRNA-binding protein. J. Bacteriol. 179(14), 4639-4642 (1997 (Pubitemid 27299086)
44. Vytvytska O, Jakobsen JS, Balcunaite G, Andersen JS, Baccarini M, Von Gabain A. Host factor I, Hfq, binds to Escherichia coli ompA mRNA in a growth rate-dependent fashion and regulates its stability. Proc. Natl Acad. Sci. USA 95(24), 14118-14123 (1998 (Pubitemid 28549330)
45. Wang X, Dubey AK, Suzuki K, Baker CS, Babitzke P, Romeo T. CsrA post-transcriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Mol. Microbiol. 56(6), 1648-1663 (2005 (Pubitemid 40780658)
46. Wei BL, Brun-Zinkernagel AM, Simecka JW, Pruss BM, Babitzke P, Romeo T. Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol. Microbiol. 40(1), 245-256 (2001 (Pubitemid 32322877)
47. Bohn C, Rigoulay C, Bouloc P. No detectable effect of RNA-binding protein Hfq absence in Staphylococcus aureus. BMC Microbiol. 7, 10 (2007
48. Pichon C, Felden B. Small RNA genes expressed from Staphylococcus aureus genomic and pathogenicity islands with specific expression among pathogenic strains. Proc. Natl Acad. Sci. USA 102(40), 14249-14254 (2005 (Pubitemid 41429684)
49. Liu Y, Wu N, Dong J, et al. Hfq is a global regulator that controls the pathogenicity of Staphylococcus aureus. PLoS One 5(9), e13069 (2010
50. Schumacher MA, Hurlburt BK, Brennan RG. Crystal structures of SarA, a pleiotropic regulator of virulence genes in S. aureus. Nature 409(6817), 215-219 (2001 (Pubitemid 32144289)
51. Balandina A, Claret L, Hengge-Aronis R, Rouviere-Yaniv J. The Escherichia coli histone-like protein HU regulates rpoS translation. Mol. Microbiol. 39(4), 1069-1079 (2001 (Pubitemid 32176349)
52. Brescia CC, Kaw MK, Sledjeski DD. The DNA binding protein H-NS binds to and alters the stability of RNA in vitro and in vivo. J. Mol. Biol. 339(3), 505-514 (2004 (Pubitemid 38625903)
53. Repoila F, Darfeuille F. Small regulatory non-coding RNAs in bacteria: physiology and mechanistic aspects. Biol. Cell. 101(2), 117-131 (2009
54. Gerdes K, Wagner EG. RNA antitoxins. Curr. Opin. Microbiol. 10(2), 117-124 (2007 (Pubitemid 46590043)
55. Gottesman S. The small RNA regulators of Escherichia coli: roles and mechanisms. Annu. Rev. Microbiol. 58, 303-328 (2004 (Pubitemid 39551989)
56. Abu-Qatouseh LF, Chinni SV, Seggewiss J, et al. Identification of differentially expressed small non-protein-coding RNAs in Staphylococcus aureus displaying both the normal and the small-colony variant phenotype. J. Mol. Med. 88(6), 565-575 (2010
57. Bohn C, Rigoulay C, Chabelskaya S, et al. Experimental discovery of small RNAs in Staphylococcus aureus reveals a riboregulator of central metabolism. Nucleic Acids Res. (19), 6620-6636 (2010
58. Geissmann T, Chevalier C, Cros MJ, et al. A search for small noncoding RNAs in Staphylococcus aureus reveals a conserved sequence motif for regulation. Nucleic Acids Res. 37(21), 7239-7257 (2009
59. Marchais A, Naville M, Bohn C, Bouloc P, Gautheret D. Single-pass classification of all noncoding sequences in a bacterial genome using phylogenetic profiles. Genome Res. 19(6), 1084-1092 (2009
60. Novick RP, Ross HF, Projan SJ, Kornblum J, Kreiswirth B, Moghazeh S. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J. 12(10), 3967-3975 (1993 (Pubitemid 23282772)
61. Recsei P, Kreiswirth B, OReilly M, Schlievert P, Gruss A, Novick RP. Regulation of exoprotein gene expression in Staphylococcus aureus by agar. Mol. Gen. Genet. 202(1), 58-61 (1986 (Pubitemid 16150393)
62. Ji G, Beavis RC, Novick RP. Cell density control of staphylococcal virulence mediated by an octapeptide pheromone. Proc. Natl Acad. Sci. USA 92(26), 12055-12059 (1995 (Pubitemid 26014010)
63. Geisinger E, Adhikari RP, Jin R, Ross HF, Novick RP. Inhibition of rot translation by RNAIII, a key feature of agr function. Mol. Microbiol. 61(4), 1038-1048 (2006 (Pubitemid 44134179)
64. Morfeldt E, Taylor D, Von Gabain A, Arvidson S. Activation of a-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J. 14(18), 4569-4577 (1995
65. Felden B, Vandenesch F, Bouloc P, Romby P. The Staphylococcus aureus RNome and its commitment to virulence. PLoS Pathog. 7(3), e1002006 (2011
66. Chabelskaya S, Gaillot O, Felden B. A Staphylococcus aureus small RNA is required for bacterial virulence and regulates the expression of an immune-evasion molecule. PLoS Pathog. 6(6), e1000927 (2010
67. Winkler WC, Breaker RR. Regulation of bacterial gene expression by riboswitches. Annu. Rev. Microbiol. 59, 487-517 (2005 (Pubitemid 41507440)
68. Barrick JE, Corbino KA, Winkler WC, et al. New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. Proc. Natl Acad. Sci. USA 101(17), 6421-6426 (2004 (Pubitemid 38585989)
69. Winkler WC, Nahvi A, Roth A, Collins JA, Breaker RR. Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428(6980), 281-286 (2004 (Pubitemid 38418792)
70. Collins JA, Irnov I, Baker S, Winkler WC. Mechanism of mRNA destabilization by the glmS ribozyme. Genes Dev. 21(24), 3356-3368 (2007 (Pubitemid 350277761)
71. Komatsuzawa H, Fujiwara T, Nishi H, et al. The gate controlling cell wall synthesis in Staphylococcus aureus. Mol. Microbiol. 53(4), 1221-1231 (2004 (Pubitemid 39120441)
72. Wilson DN. The A-Z of bacterial translation inhibitors. Crit. Rev. Biochem. Mol. Biol. 44(6), 393-433 (2009
73. Klein E, Smith DL, Laxminarayan R. Hospitalizations and deaths caused by methicillin-resistant Staphylococcus aureus, United States, 1999-2005. Emerg. Infect. Dis. 13(12), 1840-1846 (2007 (Pubitemid 350248484)
74. Klevens RM, Edwards JR, Gaynes RP. The impact of antimicrobial-resistant, health care-associated infections on mortality in the United States. Clin. Infect. Dis. 47(7), 927-930 (2008