Rot and SaeRS cooperate to activate expression of the staphylococcal superantigen-like exoproteins

Journal of Bacteriology

Volumn 194, Issue 16, 2012, Pages 4355-4365

  Benson, Meredith A ^a   Lilo, Sarit ^a   Nygaard, Tyler ^b   Voyich, Jovanka M ^b   Torres, Victor J ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; STAPHYLOCOCCAL SUPERANTIGEN LIKE PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ROT; TRANSCRIPTION FACTOR SAER; UNCLASSIFIED DRUG;

ARTICLE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; PROTEIN KINASES; REPRESSOR PROTEINS; STAPHYLOCOCCUS AUREUS; SUPERANTIGENS;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

EID: 84866330681     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00706-12     Document Type: Article

References (58)

1. Adhikari RP, Novick RP. 2008. Regulatory organization of the staphylococcal sae locus. Microbiology 154:949-959.
2. Anonymous. 1999. Four pediatric deaths from community-acquired methicillin-resistant Staphylococcus aureus-Minnesota and North Dakota, 1997-1999. MMWR Morb. Mortal. Wkly. Rep. 48:707-710.
3. Attia AS, Benson MA, Stauff DL, Torres VJ, Skaar EP. 2010. Membrane damage elicits an immunomodulatory program in Staphylococcus aureus. PLoS Pathog. 6:e1000802. doi:10.1371/journal.ppat.1000802.
4. Baba T, Bae T, Schneewind O, Takeuchi F, Hiramatsu K. 2008. Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes: polymorphism and evolution of two major pathogenicity islands. J. Bacteriol. 190:300-310.
5. Bae T, Schneewind O. 2006. Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55:58-63.
6. Benito Y, et al. 2000. Probing the structure of RNAIII, the Staphylococcus aureus agr regulatory RNA, and identification of the RNA domain involved in repression of protein A expression. RNA 6:668-679.
7. Benson MA, et al. 2011. Staphylococcus aureus regulates the expression and production of the staphylococcal superantigen-like secreted proteins in a Rot-dependent manner. Mol. Microbiol. 81:659-675.
8. Boisset S, 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.
9. Boles BR, Thoendel M, Roth AJ, Horswill AR. 2010. Identification of genes involved in polysaccharide-independent Staphylococcus aureus biofilm formation. PLoS One 5:e10146. doi:10.1371/journal.pone.0010146.
10. Bubeck Wardenburg J, Williams WA, Missiakas D. 2006. Host defenses against Staphylococcus aureus infection require recognition of bacterial lipoproteins. Proc. Natl. Acad. Sci. U. S. A. 103:13831-13836.
11. Cheung AL, Bayer AS, Zhang G, Gresham H, Xiong YQ. 2004. Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus. FEMS Immunol. Med. Microbiol. 40:1-9.
12. Cho H, Jeong DW, Li C, Bae T. 2012. Organizational requirements of the SaeR binding sites for functional P1 promoter of the sae operon in Staphylococcus aureus. J. Bacteriol. 194:2865-2876.
13. Diep BA, et al. 2006. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367:731-739.
14. Duthie ES, Lorenz LL. 1952. Staphylococcal coagulase; mode of action and antigenicity. J. Gen. Microbiol. 6:95-107.
15. Felden B, Vandenesch F, Bouloc P, Romby P. 2011. The Staphylococcus aureus RNome and its commitment to virulence. PLoS Pathog. 7:e1002006. doi:10.1371/journal.ppat.1002006.
16. Foster TJ. 2005. Immune evasion by staphylococci. Nat. Rev. Microbiol. 3:948-958.
17. Fraser JD, Proft T. 2008. The bacterial superantigen and superantigenlike proteins. Immunol. Rev. 225:226-243.
18. Geiger T, Goerke C, Mainiero M, Kraus D, Wolz C. 2008. The virulence regulator Sae of Staphylococcus aureus: promoter activities and response to phagocytosis-related signals. J. Bacteriol. 190:3419-3428.
19. Geisinger E, Adhikari RP, Jin R, Ross HF, Novick RP. 2006. Inhibition of rot translation by RNAIII, a key feature of agr function. Mol. Microbiol. 61:1038-1048.
20. Gillaspy AF, et al. 1995. Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis. Infect. Immun. 63:3373-3380.
21. Giraudo AT, Calzolari A, Cataldi AA, Bogni C, Nagel R. 1999. The sae locus of Staphylococcus aureus encodes a two-component regulatory system. FEMS Microbiol. Lett. 177:15-22.
22. Giraudo AT, Cheung AL, Nagel R. 1997. The sae locus of Staphylococcus aureus controls exoprotein synthesis at the transcriptional level. Arch. Microbiol. 168:53-58.
23. Giraudo AT, Mansilla C, Chan A, Raspanti C, Nagel R. 2003. Studies on the expression of regulatory locus sae in Staphylococcus aureus. Curr. Microbiol. 46:246-250.
24. Giraudo AT, Martinez GL, Calzolari A, Nagel R. 1994. Characterization of a Tn925-induced mutant of Staphylococcus aureus altered in exoprotein production. J. Basic Microbiol. 34:317-322.
25. Goerke C, et al. 2005. Role of Staphylococcus aureus global regulators sae and sigmaB in virulence gene expression during device-related infection. Infect. Immun. 73:3415-3421.
26. Jeong DW, et al. 2011. Identification of the P3 promoter and distinct roles of the two promoters of the SaeRS two-component system in Staphylococcus aureus. J. Bacteriol. 193:4672-4684.
27. Koenig RL, Ray JL, Maleki SJ, Smeltzer MS, Hurlburt BK. 2004. Staphylococcus aureus AgrA binding to the RNAIII-agr regulatory region. J. Bacteriol. 186:7549-7555.
28. Kreiswirth BN, et al. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709-712.
29. Lauderdale KJ, Malone CL, Boles BR, Morcuende J, Horswill AR. 2010. Biofilm dispersal of community-associated methicillin-resistant Staphylococcus aureus on orthopedic implant material. J. Orthop. Res. 28:55-61.
30. Li D, Cheung A. 2008. Repression of hla by rot is dependent on sae in Staphylococcus aureus. Infect. Immun. 76:1068-1075.
31. Luong TT, et al. 2011. Staphylococcus aureus ClpC divergently regulates capsule via sae and codY in strain Newman but activates capsule via codY in strain UAMS-1 and in strain Newman with repaired saeS. J. Bacteriol. 193:686-694.
32. Mainiero M, et al. 2010. Differential target gene activation by the Staphylococcus aureus two-component system saeRS. J. Bacteriol. 192:613-623.
33. Malachowa N, et al. 2011. Global changes in Staphylococcus aureus gene expression in human blood. PLoS One 6:e18617. doi:10.1371/journal.pone.0018617.
34. McNamara PJ, Bayer AS. 2005. A rot mutation restores parental virulence to an agr-null Staphylococcus aureus strain in a rabbit model of endocarditis. Infect. Immun. 73:3806-3809.
35. McNamara PJ, Milligan-Monroe KC, Khalili S, Proctor RA. 2000. Identification, cloning, and initial characterization of rot, a locus encoding a regulator of virulence factor expression in Staphylococcus aureus. J. Bacteriol. 182:3197-3203.
36. Montgomery CP, Boyle-Vavra S, Daum RS. 2010. Importance of the global regulators Agr and SaeRS in the pathogenesis of CA-MRSA USA300 infection. PLoS One 5:e15177. doi:10.1371/journal.pone.0015177.
37. Morfeldt E, Taylor D, von Gabain A, Arvidson S. 1995. Activation of alpha-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J. 14:4569-4577.
38. Morfeldt E, Tegmark K, Arvidson S. 1996. Transcriptional control of the agr-dependent virulence gene regulator, RNAIII, in Staphylococcus aureus. Mol. Microbiol. 21:1227-1237.
39. Nizet V. 2007. Understanding how leading bacterial pathogens subvert innate immunity to reveal novel therapeutic targets. J. Allergy Clin. Immunol. 120:13-22.
40. Novick RP. 2003. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 48:1429-1449.
41. Novick RP, Geisinger E. 2008. Quorum sensing in staphylococci. Annu. Rev. Genet. 42:541-564.
42. Nygaard TK, et al. 2010. SaeR binds a consensus sequence within virulence gene promoters to advance USA300 pathogenesis. J. Infect. Dis. 201:241-254.
43. Palazzolo-Ballance AM, et al. 2008. Neutrophil microbicides induce a pathogen survival response in community-associated methicillinresistant Staphylococcus aureus. J. Immunol. 180:500-509.
44. Pantrangi M, Singh VK, Wolz C, Shukla SK. 2010. Staphylococcal superantigen-like genes, ssl5 and ssl8, are positively regulated by Sae and negatively by Agr in the Newman strain. FEMS Microbiol. Lett. 308:175-184.
45. Roberts RB, et al. 1998. Molecular epidemiology of methicillin-resistant Staphylococcus aureus in 12 New York hospitals. MRSA Collaborative Study Group. J. Infect. Dis. 178:164-171.
46. Rogasch K, et al. 2006. Influence of the two-component system SaeRS on global gene expression in two different Staphylococcus aureus strains. J. Bacteriol. 188:7742-7758.
47. Said-Salim B, et al. 2003. Global regulation of Staphylococcus aureus genes by Rot. J. Bacteriol. 185:610-619.
48. Schafer D, et al. 2009. A point mutation in the sensor histidine kinase SaeS of Staphylococcus aureus strain Newman alters the response to biocide exposure. J. Bacteriol. 191:7306-7314.
49. Sun F, et al. 2010. In the Staphylococcus aureus two-component system sae, the response regulator SaeR binds to a direct repeat sequence and DNA binding requires phosphorylation by the sensor kinase SaeS. J. Bacteriol. 192:2111-2127.
50. Thoendel M, Kavanaugh JS, Flack CE, Horswill AR. 2011. Peptide signaling in the staphylococci. Chem. Rev. 111:117-151.
51. Torres VJ, et al. 2010. Staphylococcus aureus fur regulates the expression of virulence factors that contribute to the pathogenesis of pneumonia. Infect. Immun. 78:1618-1628.
52. Torres VJ, et al. 2007. A Staphylococcus aureus regulatory system that responds to host heme and modulates virulence. Cell Host Microbe 1:109-119.
53. Tseng CW, Stewart GC. 2005. Rot repression of enterotoxin B expression in Staphylococcus aureus. J. Bacteriol. 187:5301-5309.
54. Tseng CW, Zhang S, Stewart GC. 2004. Accessory gene regulator control of staphyloccoccal enterotoxin d gene expression. J. Bacteriol. 186:1793-1801.
55. Voyich JM, et al. 2005. Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J. Immunol. 175:3907-3919.
56. Voyich JM, et al. 2009. The SaeR/S gene regulatory system is essential for innate immune evasion by Staphylococcus aureus. J. Infect. Dis. 199:1698-1706.
57. Watkins RL, Pallister KB, Voyich JM. 2011. The SaeR/S gene regulatory system induces a pro-inflammatory cytokine response during Staphylococcus aureus infection. PLoS One 6:e19939. doi:10.1371/journal.pone.0019939.
58. Zielinska AK, et al. 2011. Defining the strain-dependent impact of the staphylococcal accessory regulator (sarA) on the alpha-toxin phenotype of Staphylococcus aureus. J. Bacteriol. 193:2948-2958.