VfrB is a key activator of the staphylococcus aureus SaeRS two- component system

Journal of Bacteriology

Volumn 199, Issue 5, 2017, Pages

  Krute, Christina N ^a   Rice, Kelly C ^b   Bose, Jeffrey L ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Fatty acid kinase; Regulation; SaeRS; Two component system; VfrB

Indexed keywords

ALPHA HEMOLYSIN; ASPARTIC ACID; BACTERIAL PROTEIN; HUMAN NEUTROPHIL PEPTIDE 1; MYRISTIC ACID; PEPTIDE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; VIRULENCE FACTOR REGULATOR B; PROTEIN KINASE; SAER PROTEIN, STAPHYLOCOCCUS AUREUS; SAES PROTEIN, STAPHYLOCOCCUS AUREUS;

ARTICLE; AUTOREGULATION; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM MUTANT; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; FATTY ACID METABOLISM; GENE REGULATORY NETWORK; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SAERS GENE; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION REGULATION; WILD TYPE; AMINO ACID SEQUENCE; CONSERVED SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CONSERVED SEQUENCE; GENE EXPRESSION REGULATION, BACTERIAL; PROTEIN KINASES; STAPHYLOCOCCUS AUREUS;

EID: 85013931428     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00828-16     Document Type: Article

References (59)

1. Becker RE, Bubeck Wardenburg J. 2015. Staphylococcus aureus and the skin: a longstanding and complex interaction. Skinmed 13:111-119.
2. Duerden B, Fry C, Johnson AP, Wilcox MH. 2015. The control of methicillin-resistant Staphylococcus aureus blood stream infections in England. Open Forum Infect Dis 2:ofv035. https://doi.org/10.1093/ofid/ ofv035.
3. Murray RJ. 2005. Staphylococcus aureus infective endocarditis: diagnosis and management guidelines. Intern Med J 35(Suppl 2):S25-S44. https:// doi.org/10.1111/j.1444-0903.2005.00978.x.
4. Pendleton A, Kocher MS. 2015. Methicillin-resistant Staphylococcus aureus bone and joint infections in children. J Am Acad Orthop Surg 23:29 -37. https://doi.org/10.5435/JAAOS-23-01-29.
5. Sanders JE, Garcia SE. 2015. Evidence-based management of skin and soft-tissue infections in pediatric patients in the emergency department. Pediatr Emerg Med Pract 12:1-23.
6. 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. https://doi.org/10.1016/S0928 -8244(03)00309-2.
7. Cue D, Junecko JM, Lei MG, Blevins JS, Smeltzer MS, Lee CY. 2015. SaeRS-dependent inhibition of biofilm formation in Staphylococcus aureus Newman. PLoS One 10:e0123027. https://doi.org/10.1371/journal .pone.0123027.
8. 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. https://doi.org/10.1007/s002030050469.
9. Luong TT, Sau K, Roux C, Sau S, Dunman PM, Lee CY. 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. https:// doi.org/10.1128/JB.00987-10.
10. Mrak LN, Zielinska AK, Beenken KE, Mrak IN, Atwood DN, Griffin LM, Lee CY, Smeltzer MS. 2012. saeRS and sarA act synergistically to repress protease production and promote biofilm formation in Staphylococcus aureus. PLoS One 7:e38453. https://doi.org/10.1371/journal.pone .0038453.
11. Voyich JM, Vuong C, DeWald M, Nygaard TK, Kocianova S, Griffith S, Jones J, Iverson C, Sturdevant DE, Braughton KR, Whitney AR, Otto M, DeLeo FR. 2009. The SaeR/S gene regulatory system is essential for innate immune evasion by Staphylococcus aureus. J Infect Dis 199: 1698-1706. https://doi.org/10.1086/598967.
12. Flack CE, Zurek OW, Meishery DD, Pallister KB, Malone CL, Horswill AR, Voyich JM. 2014. Differential regulation of staphylococcal virulence by the sensor kinase SaeS in response to neutrophil-derived stimuli. Proc Natl Acad Sci U S A 111:E2037-E2045. https://doi.org/10.1073/ pnas.1322125111.
13. Liu Q, Cho H, Yeo WS, Bae T. 2015. The extracytoplasmic linker peptide of the sensor protein SaeS tunes the kinase activity required for staphylococcal virulence in response to host signals. PLoS Pathog 11: e1004799. https://doi.org/10.1371/journal.ppat.1004799.
14. Sun F, Li C, Jeong D, Sohn C, He C, Bae T. 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. https://doi.org/ 10.1128/JB.01524-09.
15. Jeong DW, Cho H, Jones MB, Shatzkes K, Sun F, Ji Q, Liu Q, Peterson SN, He C, Bae T. 2012. The auxiliary protein complex SaePQ activates the phosphatase activity of sensor kinase SaeS in the SaeRS two-component system of Staphylococcus aureus. Mol Microbiol 86:331-348. https:// doi.org/10.1111/j.1365-2958.2012.08198.x.
16. Jeong DW, Cho H, Lee H, Li C, Garza J, Fried M, Bae T. 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. https://doi.org/10.1128/JB.00353-11.
17. 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. https:// doi.org/10.1128/JB.01927-07.
18. Steinhuber A, Goerke C, Bayer MG, Doring G, Wolz C. 2003. Molecular architecture of the regulatory locus sae of Staphylococcus aureus and its impact on expression of virulence factors. J Bacteriol 185:6278-6286. https://doi.org/10.1128/JB.185.21.6278-6286.2003.
19. Novick RP, Jiang D. 2003. The staphylococcal saeRS system coordinates environmental signals with agr quorum sensing. Microbiology 149: 2709-2717. https://doi.org/10.1099/mic.0.26575-0.
20. Kuroda H, Kuroda M, Cui L, Hiramatsu K. 2007. Subinhibitory concentrations of β-lactam induce haemolytic activity in Staphylococcus aureus through the SaeRS two-component system. FEMS Microbiol Lett 268: 98-105. https://doi.org/10.1111/j.1574-6968.2006.00568.x.
21. Kuroda M, Kuroda H, Oshima T, Takeuchi F, Mori H, Hiramatsu K. 2003. Two-component system VraSR positively modulates the regulation of cell-wall biosynthesis pathway in Staphylococcus aureus. Mol Microbiol 49:807- 821.
22. Cho H, Jeong DW, Liu Q, Yeo WS, Vogl T, Skaar EP, Chazin WJ, Bae T. 2015. Calprotectin increases the activity of the SaeRS two component system and murine mortality during Staphylococcus aureus infections. PLoS Pathog 11:e1005026. https://doi.org/10.1371/journal.ppat.1005026.
23. Mainiero M, Goerke C, Geiger T, Gonser C, Herbert S, Wolz C. 2010. Differential target gene activation by the Staphylococcus aureus twocomponent system saeRS. J Bacteriol 192:613- 623. https://doi.org/ 10.1128/JB.01242-09.
24. Rogasch K, Ruhmling V, Pane-Farre J, Hoper D, Weinberg C, Fuchs S, Schmudde M, Broker BM, Wolz C, Hecker M, Engelmann S. 2006. Influence of the two-component system SaeRS on global gene expression in two different Staphylococcus aureus strains. J Bacteriol 188:7742-7758. https://doi.org/10.1128/JB.00555-06.
25. Cho H, Jeong DW, Li C, Bae T. 2012. Organizational requirements of the SaeR binding sites for a functional P1 promoter of the sae operon in Staphylococcus aureus. J Bacteriol 194:2865-2876. https://doi.org/ 10.1128/JB.06771-11.
26. Bose JL, Daly SM, Hall PR, Bayles KW. 2014. Identification of the Staphylococcus aureus vfrAB operon, a novel virulence factor regulatory locus. Infect Immun 82:1813-1822. https://doi.org/10.1128/IAI.01655-13.
27. Parsons JB, Broussard TC, Bose JL, Rosch JW, Jackson P, Subramanian C, Rock CO. 2014. Identification of a two-component fatty acid kinase responsible for host fatty acid incorporation by Staphylococcus aureus. Proc Natl Acad Sci U S A 111:10532-10537. https://doi.org/10.1073/ pnas.1408797111.
28. Giraudo AT, Raspanti CG, Calzolari A, Nagel R. 1994. Characterization of a Tn551-mutant of Staphylococcus aureus defective in the production of several exoproteins. Can J Microbiol 40:677- 681. https://doi.org/ 10.1139/m94-107.
29. Vandenesch F, Kornblum J, Novick RP. 1991. A temporal signal, independent of agr, is required for hla but not spa transcription in Staphylococcus aureus. J Bacteriol 173:6313- 6320. https://doi.org/10.1128/ jb.173.20.6313-6320.1991.
30. Cheung AL, Projan SJ. 1994. Cloning and sequencing of sarA of Staphylococcus aureus, a gene required for the expression of agr. J Bacteriol 176:4168-4172. https://doi.org/10.1128/jb.176.13.4168-4172.1994.
31. 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.
32. 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. https://doi.org/10.1128/JB.182.11.3197-3203.2000.
33. Schmidt KA, Manna AC, Gill S, Cheung AL. 2001. SarT, a repressor of α-hemolysin in Staphylococcus aureus. Infect Immun 69:4749-4758. https://doi.org/10.1128/IAI.69.8.4749-4758.2001.
34. Blevins JS, Beenken KE, Elasri MO, Hurlburt BK, Smeltzer MS. 2002. Strain-dependent differences in the regulatory roles of sarA and agr in Staphylococcus aureus. Infect Immun 70:470-480. https://doi.org/ 10.1128/IAI.70.2.470-480.2002.
35. Lebeau C, Vandenesch F, Greenland T, Novick RP, Etienne J. 1994. Coagulase expression in Staphylococcus aureus is positively and negatively modulated by an agr-dependent mechanism. J Bacteriol 176: 5534-5536. https://doi.org/10.1128/jb.176.17.5534-5536.1994.
36. Siebold C, Arnold I, Garcia-Alles LF, Baumann U, Erni B. 2003. Crystal structure of the Citrobacter freundii dihydroxyacetone kinase reveals an eight-stranded α-helical barrel ATP-binding domain. J Biol Chem 278: 48236-48244. https://doi.org/10.1074/jbc.M305942200.
37. Dintner S, Staron A, Berchtold E, Petri T, Mascher T, Gebhard S. 2011. Coevolution of ABC transporters and two-component regulatory systems as resistance modules against antimicrobial peptides in Firmicutes bacteria. J Bacteriol 193:3851-3862. https://doi.org/10.1128/JB.05175-11.
38. Ouyang J, Tian XL, Versey J, Wishart A, Li YH. 2010. The BceABRS four-component system regulates the bacitracin-induced cell envelope stress response in Streptococcus mutans. Antimicrob Agents Chemother 54:3895-3906. https://doi.org/10.1128/AAC.01802-09.
39. Rietkotter E, Hoyer D, Mascher T. 2008. Bacitracin sensing in Bacillus subtilis. Mol Microbiol 68:768 -785. https://doi.org/10.1111/j.1365 -2958.2008.06194.x.
40. Bernard R, Guiseppi A, Chippaux M, Foglino M, Denizot F. 2007. Resistance to bacitracin in Bacillus subtilis: unexpected requirement of the BceAB ABC transporter in the control of expression of its own structural genes. J Bacteriol 189:8636-8642. https://doi.org/10.1128/JB.01132-07.
41. Ninfa AJ, Jiang P. 2005. PII signal transduction proteins: sensors of α-ketoglutarate that regulate nitrogen metabolism. Curr Opin Microbiol 8:168 -173. https://doi.org/10.1016/j.mib.2005.02.011.
42. Henke JM, Bassler BL. 2004. Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J Bacteriol 186:6902- 6914. https://doi.org/10.1128/JB.186.20.6902-6914.2004.
43. Jiang M, Shao W, Perego M, Hoch JA. 2000. Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol Microbiol 38:535-542. https://doi.org/10.1046/j.1365-2958.2000 .02148.x.
44. Laub MT, Goulian M. 2007. Specificity in two-component signal transduction pathways. Annu Rev Genet 41:121-145. https://doi.org/10.1146/ annurev.genet.41.042007.170548.
45. Mehta P, Goyal S, Long T, Bassler BL, Wingreen NS. 2009. Information processing and signal integration in bacterial quorum sensing. Mol Syst Biol 5:325.
46. Ninfa AJ. 1991. Protein phosphorylation and the regulation of cellular processes by the homologous two-component regulatory systems of bacteria. Genet Eng (N Y) 13:39 -72.
47. Wanner BL. 1992. Is cross regulation by phosphorylation of twocomponent response regulator proteins important in bacteria? J Bacteriol 174:2053-2058. https://doi.org/10.1128/jb.174.7.2053-2058.1992.
48. Yamamoto K, Hirao K, Oshima T, Aiba H, Utsumi R, Ishihama A. 2005. Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J Biol Chem 280:1448 -1456. https://doi.org/10.1074/jbc.M410104200.
49. Neumann Y, Ohlsen K, Donat S, Engelmann S, Kusch H, Albrecht D, Cartron M, Hurd A, Foster SJ. 2015. The effect of skin fatty acids on Staphylococcus aureus. Arch Microbiol 197:245-267. https://doi.org/ 10.1007/s00203-014-1048-1.
50. Bose JL. 2014. Genetic manipulation of staphylococci. Methods Mol Biol 1106:101-111. https://doi.org/10.1007/978-1-62703-736-5_8.
51. Krausz KL, Bose JL. 2016. Bacteriophage transduction in Staphylococcus aureus: broth-based method. Methods Mol Biol 1373:63- 68.
52. Lehman MK, Bose JL, Bayles KW. 2016. Allelic exchange. Methods Mol Biol 1373:89 -96.
53. Lehman MK, Bose JL, Sharma-Kuinkel BK, Moormeier DE, Endres JL, Sadykov MR, Biswas I, Bayles KW. 2015. Identification of the amino acids essential for LytSR-mediated signal transduction in Staphylococcus aureus and their roles in biofilm-specific gene expression. Mol Microbiol 95:723-737. https://doi.org/10.1111/mmi.12902.
54. Boles BR, Thoendel M, Roth AJ, Horswill AR. 2010. Identification of genes involved in polysaccharide-independent Staphylococcus aureus biofilm formation. PLoS One 5:e10146. https://doi.org/10.1371/journal.pone .0010146.
55. Fey PD, Endres JL, Yajjala VK, Widhelm TJ, Boissy RJ, Bose JL, Bayles KW. A genetic resource for rapid and comprehensive phenotype screening of nonessential Staphylococcus aureus genes. mBio 4:e00537-12.
56. Duthie ES, Lorenz LL. 1952. Staphylococcal coagulase: mode of action and antigenicity. J Gen Microbiol 6:95-107.
57. Kreiswirth BN, Lofdahl S, Betley MJ, O'Reilly M, Schlievert PM, Bergdoll MS, Novick RP. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709 -712. https://doi.org/10.1038/305709a0.
58. Pang YY, Schwartz J, Thoendel M, Ackermann LW, Horswill AR, Nauseef WM. 2010. agr-Dependent interactions of Staphylococcus aureus USA300 with human polymorphonuclear neutrophils. J Innate Immun 2:546 -559. https://doi.org/10.1159/000319855.
59. Bose JL, Fey PD, Bayles KW. 2013. Genetic tools to enhance the study of gene function and regulation in Staphylococcus aureus. Appl Environ Microbiol 79:2218 -2224. https://doi.org/10.1128/AEM.00136-13.