The CshA DEAD-box RNA helicase is important for quorum sensing control in Staphylococcus aureus

RNA Biology

Volumn 10, Issue 1, 2013, Pages 157-165

  Oun, Stella ^a   Redder, Peter ^a   Didier, Jean Philippe ^a   François, Patrice ^b   Corvaglia, Anna Rita ^a   Buttazzoni, Elena ^a   Giraud, Caroline ^a   Girard, Myriam ^b   Schrenzel, Jacques ^b   Linder, Patrick ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

Degradosome; Quorum sensing; RNA helicase; Staphylococcus aureus

Indexed keywords

BACTERIAL RNA; CSHA PROTEIN; DEAD BOX PROTEIN; HEMOLYSIN; MESSENGER RNA; PROTEINASE; UNCLASSIFIED DRUG;

AGR GENE; ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIUM ADHERENCE; BACTERIUM MUTANT; BIOFILM; CATHETER; COLD SENSITIVITY; CONTROLLED STUDY; GENE INACTIVATION; HEMOLYSIS; NONHUMAN; PROSTHESIS; PROTEIN EXPRESSION; PROTEIN SECRETION; QUORUM SENSING; RNA STABILITY; STAPHYLOCOCCUS AUREUS;

EID: 84875208274     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.22899     Document Type: Article

References (62)

1. Linder P, Jankowsky E. From unwinding to clamping-the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 2011; 12:505-16; PMID:21779027; http://dx.doi.org/10.1038/nrm3154.
2. Liu F, Putnam A, Jankowsky E. ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding. Proc Natl Acad Sci USA 2008; 105:20209-14; PMID:19088201; http://dx.doi. org/10.1073/pnas.0811115106.
3. Jankowsky E, Bowers H. Remodeling of ribonucleo-protein complexes with DExH/D RNA helicases. Nucleic Acids Res 2006; 34:4181-8; PMID:16935886; http://dx.doi.org/10.1093/nar/gkl410. (Pubitemid 44542197)
4. Nishi K, Morel-Deville F, Hershey JWB, Leighton T, Schnier J. An eIF-4A-like protein is a suppressor of an Escherichia coli mutant defective in 50S ribo-somal subunit assembly. Nature 1988; 336:496-8; PMID:2461520; http://dx.doi.org/10.1038/336496a0.
5. Toone WM, Rudd KE, Friesen JD. deaD, a new Escherichia coli gene encoding a presumed ATP-dependent RNA helicase, can suppress a mutation in rpsB, the gene encoding ribosomal protein S2. J Bacteriol 1991; 173:3291-302; PMID:2045359.
6. Sharpe Elles LM, Sykes M T, Williamson JR, Uhlenbeck OC. A dominant negative mutant of the E. coli RNA helicase DbpA blocks assembly of the 50S ribosomal subunit. Nucleic Acids Res 2009; 37:6503-14; PMID:19734347; http://dx.doi.org/10.1093/nar/gkp711.
7. Fuller-Pace FV, Nicol SM, Reid AD, Lane D P. DbpA: a DEAD box protein specifically activated by 23s rRNA. EMBO J 1993; 12:3619-26; PMID:8253085. (Pubitemid 23256448)
8. Tsu CA, Uhlenbeck OC. Kinetic analysis of the RNA-dependent adenosinetriphosphatase activity of DbpA, an Escherichia coli DEAD protein specific for 23S ribosomal RNA. Biochemistry 1998; 37:16989-96; PMID:9836593; http://dx.doi.org/10.1021/bi981837y. (Pubitemid 28566777)
9. Kossen K, Uhlenbeck OC. Cloning and biochemical characterization of Bacillus subtilis YxiN, a DEAD protein specifically activated by 23S rRNA: delineation of a novel sub-family of bacterial DEAD proteins. Nucleic Acids Res 1999; 27:3811-20; PMID:10481020; http://dx.doi.org/10.1093/nar/27.19.3811. (Pubitemid 29454429)
10. Wang S, Hu Y, Overgaard MT, Karginov FV, Uhlenbeck OC, McKay DB. The domain of the Bacillus subtilis DEAD-box helicase YxiN that is responsible for specific binding of 23S rRNA has an RNA recognition motif fold. RNA 2006; 12:959-67; PMID:16611943; http://dx.doi.org/10.1261/rna.5906. (Pubitemid 43788114)
11. Moll I, Grill S, Gründling A, Bläsi U. Effects of ribosomal proteins S1, S2 and the DeaD/CsdA DEAD-box helicase on translation of leaderless and canonical mRNAs in Escherichia coli. Mol Microbiol 2002; 44:1387-96; PMID:12068815; http://dx.doi. org/10.1046/j.1365-2958.2002.02971.x. (Pubitemid 34595768)
12. Jain C. The E. coli RhlE RNA helicase regulates the function of related RNA helicases during ribosome assembly. RNA 2008; 14:381-9; PMID:18083833; http://dx.doi.org/10.1261/rna.800308. (Pubitemid 351171597)
13. Py B, Higgins CF, Krisch HM, Carpousis AJ. A DEAD-box RNA helicase in the Escherichia coli RNA degra-dosome. Nature 1996; 381:169-72; PMID:8610017; http://dx.doi.org/10.1038/381169a0. (Pubitemid 26137967)
14. Vanzo NF, Li YS, Py B, Blum E, Higgins CF, Raynal LC, et al. Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev 1998; 12:2770-81; PMID:9732274; http://dx.doi.org/10.1101/gad.12.17. 2770. (Pubitemid 28420656)
15. Coburn GA, Miao X, Briant DJ, Mackie GA. Reconstitution of a minimal RNA degradosome demonstrates functional coordination between a 3' exo-nuclease and a DEAD-box RNA helicase. Genes Dev 1999; 13:2594-603; PMID:10521403; http://dx.doi. org/10.1101/gad.13.19.2594. (Pubitemid 29489650)
16. Prud'homme-Généreux A, Beran RK, Iost I, Ramey CS, Mackie GA, Simons RW. Physical and functional interactions among RNase E, polynucleotide phosphorylase and the cold-shock protein, CsdA: evidence for a 'cold shock degradosome'. Mol Microbiol 2004; 54:1409-21; PMID:15554978; http://dx.doi. org/10.1111/j.1365-2958.2004.04360.x. (Pubitemid 39578281)
17. Gury J, Barthelmebs L, Cavin J F. Random transposon mutagenesis of Lactobacillus plantarum by using the pGh9:IS S1 vector to clone genes involved in the regulation of phenolic acid metabolism. Arch Microbiol 2004; 182:337-45; PMID:15375644; http://dx.doi. org/10.1007/s00203-004-0705-1. (Pubitemid 39506384)
18. Pandiani F, Chamot S, Brillard J, Carlin F, Nguyen-the C, Broussolle V. Role of the five RNA helicases in the adaptive response of Bacillus cereus ATCC 14579 cells to temperature, pH, and oxidative stresses. Appl Environ Microbiol 2011; 77:5604-9; PMID:21705526; http://dx.doi.org/10.1128/AEM.02974-10.
19. Roos S, Lindgren S, Jonsson H. Autoaggregation of Lactobacillus reuteri is mediated by a putative DEAD-box helicase. Mol Microbiol 1999; 32:427-36; PMID:10231497; http://dx.doi.org/10.1046/j.1365-2958.1999.01363.x. (Pubitemid 29178707)
20. Briolat V, Reysset G. Identification of the Clostridium perfringens genes involved in the adaptive response to oxidative stress. J Bacteriol 2002; 184:2333-43; PMID:11948145; http://dx.doi.org/10.1128/JB.184.9.2333-2343.2002. (Pubitemid 34311124)
21. Markkula A, Mattila M, Lindström M, Korkeala H. Genes encoding putative DEAD-box RNA heli-cases in Listeria monocytogenes EGD-e are needed for growth and motility at 3°C. Environ Microbiol 2012; 14:2223-32; PMID:22564273; http://dx.doi. org/10.1111/j.1462-2920.2012.02761.x.
22. Pearce BJ, Yin YB, Masure HR. Genetic identification of exported proteins in Streptococcus pneumoniae. Mol Microbiol 1993; 9:1037-50; PMID:7934910; http://dx.doi.org/10.1111/j.1365-2958.1993.tb01233.x. (Pubitemid 23271781)
23. Tu Quoc PH, Genevaux P, Pajunen M, Savilahti H, Georgopoulos C, Schrenzel J, et al. Isolation and characterization of biofilm formation-defective mutants of Staphylococcus aureus. Infect Immun 2007; 75:1079-88; PMID:17158901; http://dx.doi.org/10.1128/IAI.01143-06. (Pubitemid 46385799)
24. Lehnik-Habrink M, Pförtner H, Rempeters L, Pietack N, Herzberg C, Stülke J. The RNA degradosome in Bacillus subtilis: identification of CshA as the major RNA helicase in the multiprotein complex. Mol Microbiol 2010; 77:958-71; PMID:20572937.
25. Roux CM, DeMuth J P, Dunman PM. Characterization of components of the Staphylococcus aureus mRNA degradosome holoenzyme-like complex. J Bacteriol 2011; 193:5520-6; PMID:21764917; http://dx.doi. org/10.1128/JB.05485-11.
26. Lowy FD. Staphylococcus aureus infections. N Engl J Med 1998; 339:520-32; PMID:9709046; http://dx.doi.org/10.1056/NEJM199808203390806.
27. Novick R P. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 2003; 48:1429-49; PMID:12791129; http://dx.doi.org/10.1046/j.1365-2958.2003.03526.x. (Pubitemid 36751052)
28. Garzoni C, Kelley WL. Staphylococcus aureus: new evidence for intracellular persistence. Trends Microbiol 2009; 17:59-65; PMID:19208480; http://dx.doi. org/10.1016/j.tim.2008.11.005.
29. von Eiff C. Staphylococcus aureus small colony variants: a challenge to microbiologists and clinicians. Int J Antimicrob Agents 2008; 31:507-10; PMID:18180148; http://dx.doi.org/10.1016/j.ijan-timicag.2007.10.026.
30. Goerke C, Wolz C. Adaptation of Staphylococcus aureus to the cystic fibrosis lung. Int J Med Microbiol 2010; 300:520-5; PMID:20843740; http://dx.doi. org/10.1016/j.ijmm.2010.08.003.
31. Götz F. Staphylococcus and biofilms. Mol Microbiol 2002; 43:1367-78; PMID:11952892; http://dx.doi. org/10.1046/j.1365-2958.2002.02827.x. (Pubitemid 34595531)
32. Otto M. Staphylococcal biofilms. Curr Top Microbiol Immunol 2008; 322:207-28; PMID:18453278; http://dx.doi.org/10.1007/978-3-540-75418-3-10.
33. Boisset S, Geissmann T, Huntzinger E, Fechter P, Bendridi N, Possedko M, et al. Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 2007; 21:1353-66; PMID:17545468; http://dx.doi.org/10.1101/gad. 423507. (Pubitemid 46871039)
34. Vuong C, Götz F, Otto M. Construction and characterization of an agr deletion mutant of Staphylococcus epidermidis. Infect Immun 2000; 68:1048-53; PMID:10678906; http://dx.doi.org/10.1128/IAI.68.3.1048-1053.2000. (Pubitemid 30108490)
35. O'Neill E, Pozzi C, Houston P, Smyth D, Humphreys H, Robinson DA, et al. Association between methicillin susceptibility and biofilm regulation in Staphylococcus aureus isolates from device-related infections. J Clin Microbiol 2007; 45:1379-88; PMID:17329452; http://dx.doi.org/10.1128/JCM.02280-06. (Pubitemid 46762387)
36. Ando Y, Nakamura K. Bacillus subtilis DEAD protein YdbR possesses ATPase, RNA binding, and RNA unwinding activities. Biosci Biotechnol Biochem 2006; 70:1606-15; PMID:16861794; http://dx.doi. org/10.1271/bbb.50678. (Pubitemid 44124918)
37. Tanner NK, Cordin O, Banroques J, Doère M, Linder P. The Q motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis. Mol Cell 2003; 11:127-38; PMID:12535527; http://dx.doi.org/10.1016/ S1097-2765(03)00006-6. (Pubitemid 36126596)
38. Rozen F, Pelletier J, Trachsel H, Sonenberg N. A lysine substitution in the ATP-binding site of eucaryotic initiation factor 4A abrogates nucleotide-binding activity. Mol Cell Biol 1989; 9:4061-3; PMID:2506440. (Pubitemid 19216300)
39. Sengoku T, Nureki O, Nakamura A, Kobayashi S, Yokoyama S. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 2006; 125:287-300; PMID:16630817; http://dx.doi. org/10.1016/j.cell.2006.01.054.
40. Novick R P, Ross H F, Projan SJ, Kornblum J, Kreiswirth B, Moghazeh S. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 1993; 12:3967-75; PMID:7691599. (Pubitemid 23282772)
41. Janzon L, Arvidson S. The role of the delta-lysin gene (hld) in the regulation of virulence genes by the accessory gene regulator (agr) in Staphylococcus aureus. EMBO J 1990; 9:1391-9; PMID:2328718.
42. Yao J, Zhong J, Fang Y, Geisinger E, Novick R P, Lambowitz AM. Use of targetrons to disrupt essential and nonessential genes in Staphylococcus aureus reveals temperature sensitivity of Ll.LtrB group II intron splicing. RNA 2006; 12:1271-81; PMID:16741231; http://dx.doi.org/10.1261/rna.68706. (Pubitemid 43990552)
43. Somerville GA, Beres SB, Fitzgerald JR, DeLeo FR, Cole RL, Hoff JS, et al. In vitro serial passage of Staphylococcus aureus: changes in physiology, virulence factor production, and agr nucleotide sequence. J Bacteriol 2002; 184:1430-7; PMID:11844774; http://dx.doi.org/10.1128/JB.184.5.1430-1437.2002. (Pubitemid 34157567)
44. Redder P, Linder P. New range of vectors with a stringent 5-fluoroorotic acid-based counterselection system for generating mutants by allelic replacement in Staphylococcus aureus. Appl Environ Microbiol 2012; 78:3846-54; PMID:22447609; http://dx.doi. org/10.1128/AEM.00202-12.
45. Broussolle V, Pandiani F, Haddad N, Michaud C, Carlin F, Nguyen-the C, et al. Insertional mutagenesis reveals genes involved in Bacillus cereus ATCC 14579 growth at low temperature. FEMS Microbiol Lett 2010; 306:177-83; PMID:20370835; http://dx.doi. org/10.1111/j.1574-6968.2010.01953.x.
46. Pandiani F, Brillard J, Bornard I, Michaud C, Chamot S, Nguyen-the C, et al. Differential involvement of the five RNA helicases in adaptation of Bacillus cereus ATCC 14579 to low growth temperatures. Appl Environ Microbiol 2010; 76:6692-7; PMID:20709848; http://dx.doi.org/10.1128/AEM.00782-10.
47. Hunger K, Beckering CL, Wiegeshoff F, Graumann PL, Marahiel MA. Cold-induced putative DEAD box RNA helicases CshA and CshB are essential for cold adaptation and interact with cold shock protein B in Bacillus subtilis. J Bacteriol 2006; 188:240-8; PMID:16352840; http://dx.doi.org/10.1128/JB.188.1. 240-248.2006.
48. Kong KF, Vuong C, Otto M. Staphylococcus quorum sensing in biofilm formation and infection. Int J Med Microbiol 2006; 296:133-9; PMID:16487744; http://dx.doi.org/10.1016/j.ijmm.2006.01.042. (Pubitemid 43375996)
49. Cafiso V, Bertuccio T, Santagati M, Demelio V, Spina D, Nicoletti G, et al. agr-Genotyping and transcription-al analysis of biofilm-producing Staphylococcus aureus. FEMS Immunol Med Microbiol 2007; 51:220-7; PMID:17854479; http://dx.doi.org/10.1111/j.1574-695X.2007.00298.x. (Pubitemid 47387498)
50. Boles BR, Horswill AR. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 2008; 4:e1000052; PMID:18437240; http://dx.doi. org/10.1371/journal.ppat.1000052.
51. Goerke C, Campana S, Bayer MG, Döring G, Botzenhart K, Wolz C. Direct quantitative transcript analysis of the agr regulon of Staphylococcus aureus during human infection in comparison to the expression profile in vitro. Infect Immun 2000; 68:1304-11; PMID:10678942; http://dx.doi.org/10.1128/IAI.68. 3.1304-1311.2000. (Pubitemid 30108526)
52. Sakoulas G, Eliopoulos GM, Moellering RC Jr., Wennersten C, Venkataraman L, Novick R P, et al. Accessory gene regulator (agr) locus in geographically diverse Staphylococcus aureus isolates with reduced susceptibility to vancomycin. Antimicrob Agents Chemother 2002; 46:1492-502; PMID:11959587; http://dx.doi.org/10.1128/AAC.46.5.1492-1502.2002. (Pubitemid 34415333)
53. Fowler VG Jr., Sakoulas G, McIntyre LM, Meka VG, Arbeit RD, Cabell CH, et al. Persistent bactere-mia due to methicillin-resistant Staphylococcus aureus infection is associated with agr dysfunction and low-level in vitro resistance to thrombin-induced platelet microbicidal protein. J Infect Dis 2004; 190:1140-9; PMID:15319865; http://dx.doi.org/10.1086/423145. (Pubitemid 39186802)
54. Vuong C, Dürr M, Carmody AB, Peschel A, Klebanoff SJ, Otto M. Regulated expression of pathogen-associated molecular pattern molecules in Staphylococcus epi-dermidis: quorum-sensing determines pro-inflammatory capacity and production of phenol-soluble modu-lins. Cell Microbiol 2004; 6:753-9; PMID:15236642; http://dx.doi.org/10.1111/j.1462-5822.2004.00401.x. (Pubitemid 39077381)
55. Yarwood JM, Paquette KM, Tikh IB, Volper EM, Greenberg E P. Generation of virulence factor variants in Staphylococcus aureus biofilms. J Bacteriol 2007; 189:7961-7; PMID:17675387; http://dx.doi. org/10.1128/JB.00789-07. (Pubitemid 350178905)
56. Cordin O, Banroques J, Tanner NK, Linder P. The DEAD-box protein family of RNA helicases. Gene 2006; 367:17-37; PMID:16337753; http://dx.doi. org/10.1016/j.gene.2005.10.019. (Pubitemid 43286737)
57. Steimer L, Klostermeier D. RNA helicases in infection and disease. RNA Biol 2012; 9:751-71; PMID:22699555; http://dx.doi.org/10.4161/rna.20090.
58. Sambrook J, Russell DR. Molecular cloning: a laboratory manual. Cold Spring Harbor, N. Y.: Cold Spring Harbor Laboratory Press, 2001.
59. Sullivan MA, Yasbin RE, Young FE. New shuttle vectors for Bacillus subtilis and Escherichia coli which allow rapid detection of inserted fragments. Gene 1984; 29:21-6; PMID:6092222; http://dx.doi. org/10.1016/0378-1119(84) 90161-6. (Pubitemid 14030928)
60. Chien Y, Manna AC, Projan SJ, Cheung AL. SarA, a global regulator of virulence determinants in Staphylococcus aureus, binds to a conserved motif essential for sar-dependent gene regulation. J Biol Chem 1999; 274:37169-76; PMID:10601279; http://dx.doi.org/10.1074/jbc.274.52.37169.
61. Redder P, Linder P. New range of vectors with a stringent 5-fluoroorotic acid-based counterselection system for generating mutants by allelic replacement in Staphylococcus aureus. Appl Environ Microbiol 2012; 78:3846-54; PMID:22447609; http://dx.doi. org/10.1128/AEM.00202-12.
62. Charpentier E, Anton AI, Barry P, Alfonso B, Fang Y, Novick R P. Novel cassette-based shuttle vector system for gram-positive bacteria. Appl Environ Microbiol 2004; 70:6076-85; PMID:15466553; http://dx.doi. org/10.1128/AEM.70.10. 6076-6085.2004. (Pubitemid 39471856)