CspR, a cold shock RNA-binding protein involved in the long-term survival and the virulence of enterococcus faecalis

Journal of Bacteriology

Volumn 194, Issue 24, 2012, Pages 6900-6908

  Michaux, Charlotte ^a   Martini, Cecilia ^a,c   Shioya, Koki ^d   Lecheheb, Sandra Ahmed ^e   Budin verneuil, Aurélie ^a   Cosette, Pascal ^e   Sanguinetti, Maurizio ^c   Hartke, Axel ^a   Verneuil, Nicolas ^a   Giard, Jean christophe ^b  

^a UNIVERSITÉ DE CAEN   (France)

^b UNIVERSITÉ DE CAEN   (France)

^c CATHOLIC UNIVERSITY   (Italy)

^d NAGAOKA UNIVERSITY OF TECHNOLOGY   (Japan)

^e UNIVERSITÉ DE ROUEN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COLD SHOCK PROTEIN; COLD SHOCK PROTEIN RNA BINDING; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASSAY; BACTERIAL VIRULENCE; COLD SHOCK RESPONSE; CONTROLLED STUDY; DOWN REGULATION; ENTEROCOCCUS FAECALIS; FEMALE; GALLERIA MELLONELLA; LONG TERM SURVIVAL; MOUSE; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PERITONEUM MACROPHAGE; PHENOTYPE; PRECIPITATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN RNA BINDING; PROTEOMICS; STARVATION; SURVIVAL RATE; TRANSCRIPTOMICS; UPREGULATION; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; COLD SHOCK PROTEINS AND PEPTIDES; ENTEROCOCCUS FAECALIS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GRAM-POSITIVE BACTERIAL INFECTIONS; HOST FACTOR 1 PROTEIN; KIDNEY; MACROPHAGES, PERITONEAL; MICE; MICROBIAL VIABILITY; MOTHS; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT; STRESS, PHYSIOLOGICAL;

ENTEROCOCCUS FAECALIS; GALLERIA MELLONELLA; HEXAPODA; POSIBACTERIA;

EID: 84870664574     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01673-12     Document Type: Article

References (56)

1. Bae W, Xia B, Inouye M, Severinov K. 2000. Escherichia coli CspA-family RNA chaperones are transcription antiterminators. Proc. Natl. Acad. Sci. U. S. A. 97:7784-7789.
2. Beaufils S, et al. 2007. The cold shock response of Lactobacillus casei: relation between HPr phosphorylation and resistance to freeze/thaw cycles. J. Mol. Microbiol. Biotechnol. 13:65-75.
3. Brandi A, Pon CL, Gualerzi CO. 1994. Interaction of the main cold shock protein CS7.4 (CspA) of Escherichia coli with the promoter region of hns. Biochimie 76:1090-1098.
4. Brennan RG, Link TM. 2007. Hfq structure, function and ligand binding. Curr. Opin. Microbiol. 10:125-133.
5. Carbona et al. 2007. Comparative study of the physiological roles of three peroxidases (NADH peroxidase, alkyl hydroperoxide reductase and thiol peroxidase) in oxidative stress response, survival inside macrophages and virulence of Enterococcus faecalis. Mol. Microbiol. 66:1148-1163.
6. 2 induce the promoter of Staphylococcus aureus cspC gene more strongly than cold. J. Basic Microbiol. 49:205-211.
7. Chao Y, Vogel J. 2010. The role of Hfq in bacterial pathogens. Curr. Opin. Microbiol. 13:24-33.
8. Charollais J, Dreyfus M, Iost I. 2004. CsdA, a cold-shock RNA helicase from Escherichia coli, is involved in the biogenesis of 50S ribosomal subunit. Nucleic Acids Res. 32:2751-2759.
9. Christiansen JK, Larsen MH, Ingmer H, Soøgaard-Andersen L, Kallipolitis BH. 2004. The RNA-binding protein Hfq of Listeria monocytogenes: role in stress tolerance and virulence. J. Bacteriol. 186:3355-3362.
10. Duval BD, Mathew A, Satola SW, Shafer WM. 2010. Altered growth, pigmentation, and antimicrobial susceptibility properties of Staphylococcus aureus due to loss of the major cold shock gene cspB. Antimicrob. Agents Chemother. 54:2283-2290.
11. Ermolenko DN, Makhatadze GI. 2002. Bacterial cold-shock proteins. Cell. Mol. Life Sci. 59:1902-1913.
12. Erova TE, et al. 2008. Cold shock exoribonuclease R (VacB) is involved in Aeromonas hydrophila pathogenesis. J. Bacteriol. 190:3467-3474.
13. Fox KA, et al. 2009. Multiple posttranscriptional regulatory mechanisms partner to control ethanolamine utilization in Enterococcus faecalis. Proc. Natl. Acad. Sci. U. S. A. 106:4435-4440.
14. Franze de Fernandez MT, Hayward WS, August JT. 1972. Bacterial proteins required for replication of phage Q. ribonucleic acid. Purification and properties of host factor I, a ribonucleic acid-binding protein. J. Biol. Chem. 247:824-831.
15. Gentry-Weeks C, Estay M, Loui C, Baker D. 2003. Intravenous mouse infection model for studying the pathology of Enterococcus faecalis infections. Infect. Immun. 71:1434-1441.
16. Gentry-Weeks CR, Karkhoff-Schweizer R, Pikis A, Estay M, Keith JM. 1999. Survival of Enterococcus faecalis in mouse peritoneal macrophages. Infect. Immun. 67:2160-2165.
17. Graumann PL, Marahiel MA. 1998. A superfamily of proteins that contain the cold-shock domain. Trends Biochem. Sci. 23:286-290.
18. Graumann PL, Marahiel MA. 1999. Cold shock proteins CspB and CspC are major stationary-phase-induced proteins in Bacillus subtilis. Arch. Microbiol. 171:135-138.
19. Graumann P, Marahiel MA. 1996. Some like it cold: response of microorganisms to cold shock. Arch. Microbiol. 166:293-300.
20. Graumann P, Schröder K, Schmid R, Marahiel MA. 1996. Cold shock stress-induced proteins in Bacillus subtilis. J. Bacteriol. 178:4611-4619.
21. Graumann P, Wendrich TM, Weber MH, Schröder K, Marahiel MA.1997. A family of cold shock proteins in Bacillus subtilis is essential for cellular growth and for efficient protein synthesis at optimal and low temperatures. Mol. Microbiol. 25:741-756.
22. Gualerzi CO, Giuliodori AM, Pon CL. 2003. Transcriptional and posttranscriptional control of cold-shock genes. J. Mol. Biol. 331:527-539.
23. Hancock LE, Gilmore MS. 2002. The capsular polysaccharide of Enterococcus faecalis and its relationship to other polysaccharides in the cell wall. Proc. Natl. Acad. Sci. U. S. A. 99:1574-1579.
24. Hankins JS, Zappavigna C, Prud'homme-Généreux A, Mackie GA. 2007. Role of RNA structure and susceptibility to RNase E in regulation of a cold shock mRNA, cspA mRNA. J. Bacteriol. 189:4353-4358.
25. Horn G, Hofweber R, Kremer W, Kalbitzer HR. 2007. Structure and function of bacterial cold shock proteins. Cell. Mol. Life Sci. 64:1457-1470.
26. Jiang W, Hou Y, Inouye M. 1997. CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J. Biol. Chem. 272:196-202.
27. Jones PG, Mitta M, Kim Y, Jiang W, Inouye M. 1996. Cold shock induces a major ribosomal-associated protein that unwinds doublestranded RNA in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 93:76-80.
28. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
29. La Teana A, et al. 1991. Identification of a cold shock transcriptional enhancer of the Escherichia coli gene encoding nucleoid protein H-NS. Proc. Natl. Acad. Sci. U. S. A. 88:10907-10911.
30. Lebreton F, et al. 2009. ace, which encodes an adhesin in Enterococcus faecalis, is regulated by Ers and is involved in virulence. Infect. Immun. 77:2832-2839.
31. Limsuwun K, Jones PG. 2000. Spermidine acetyltransferase is required to prevent spermidine toxicity at low temperatures in Escherichia coli. J. Bacteriol. 182:5373-5380.
32. Lopez MM, Yutani K, Makhatadze GI. 2001. Interactions of the cold shock protein CspB from Bacillus subtilis with single-stranded DNA. Importance of the T base content and position within the template. J. Biol. Chem. 276:15511-15518.
33. Meijerink J, et al. 2001. A novel method to compensate for different amplification efficiencies between patient DNA samples in quantitative real-time PCR. J. Mol. Diagn. 3:55-61.
34. Michaux C, et al. 2011. SlyA is a transcriptional regulator involved in the virulence of Enterococcus faecalis. Infect. Immun. 79:2638-2645.
35. Muller C, et al. 2006. The response regulator CroR modulates expression of the secreted stress-induced SalB protein in Enterococcus faecalis. J. Bacteriol. 188:2636-2645.
36. Nogueira T, Springer M. 2000. Post-transcriptional control by global regulators of gene expression in bacteria. Curr. Opin. Microbiol. 3:154-158.
37. Ogier J-C, Serror P. 2008. Safety assessment of dairy microorganisms: the Enterococcus genus. Int. J. Food Microbiol. 126:291-301.
38. Perl D, et al. 1998. Conservation of rapid two-state folding in mesophilic, thermophilic and hyperthermophilic cold shock proteins. Nat. Struct. Biol. 5:229-235.
39. Phadtare S, Inouye M. 1999. Sequence-selective interactions with RNA by CspB, CspC and CspE, members of the CspA family of Escherichia coli. Mol. Microbiol. 33:1004-1014.
40. Piette F, et al. 2010. Proteomics of life at low temperatures: trigger factor is the primary chaperone in the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Mol. Microbiol. 76:120-132.
41. Qin X, Singh KV, Weinstock GM, Murray BE. 2001. Characterization of fsr, a regulator controlling expression of gelatinase and serine protease in Enterococcus faecalis OG1RF. J. Bacteriol. 183:3372-3382.
42. Riboulet-Bisson E, et al. 2008. Characterization of the Ers regulon of Enterococcus faecalis. Infect. Immun. 76:3064-3074.
43. Rigottier-Gois L, et al. 2011. Large-scale screening of a targeted Enterococcus faecalis mutant library identifies envelope fitness factors. PLoS One 6:e29023. doi:10.1371/journal.pone.0029023.
44. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
45. Schmid B, et al. 2009. Role of cold shock proteins in growth of Listeria monocytogenes under cold and osmotic stress conditions. Appl. Environ. Microbiol. 75:1621-1627.
46. Schröder K, Graumann P, Schnuchel A, Holak TA, Marahiel MA. 1995. Mutational analysis of the putative nucleic acid-binding surface of the cold-shock domain, CspB, revealed an essential role of aromatic and basic residues in binding of single-stranded DNA containing the Y-box motif. Mol. Microbiol. 16:699-708.
47. Shankar N, et al. 2001. Role of Enterococcus faecalis surface protein Esp in the pathogenesis of ascending urinary tract infection. Infect. Immun. 69:4366-4372.
48. Shioya K, et al. 2011. Genome-wide identification of small RNAs in the opportunistic pathogen Enterococcus faecalis V583. PLoS One 6:e23948.doi:10.1371/journal.pone.0023948.
49. Sun X, Zhulin I, Wartell RM. 2002. Predicted structure and phyletic distribution of the RNA-binding protein Hfq. Nucleic Acids Res. 30:3662-3671.
50. Thurlow LR, Thomas VC, Hancock LE. 2009. Capsular polysaccharide production in Enterococcus faecalis and contribution of CpsF to capsule serospecificity. J. Bacteriol. 191:6203-6210.
51. Toledo-Arana A, et al. 2009. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459:950-956.
52. Valentin-Hansen P, Eriksen M, Udesen C. 2004. The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol. Microbiol. 51:1525-1533.
53. Vogel J, Luisi BF. 2011. Hfq and its constellation of RNA. Nat. Rev. Microbiol. 9:578-589.
54. Wisplinghoff H, et al. 2004. Nosocomial bloodstream infections in U.S. hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin. Infect. Dis. 39:309-317.
55. Yamanaka K, Fang L, Inouye M. 1998. The CspA family in Escherichia coli: multiple gene duplication for stress adaptation. Mol. Microbiol. 27: 247-255.
56. Yamanaka K, Inouye M. 1997. Growth-phase-dependent expression of cspD, encoding a member of the CspA family in Escherichia coli. J. Bacteriol. 179:5126-5130.