SarA-mediated repression of protease production plays a key role in the pathogenesis of Staphylococcus aureus USA300 isolates

Molecular Microbiology

Volumn 86, Issue 5, 2012, Pages 1183-1196

  Zielinska, Agnieszka K ^a   Beenken, Karen E ^a   Mrak, Lara N ^a   Spencer, Horace J ^a   Post, Ginell R ^a   Skinner, Robert A ^a   Tackett, Alan J ^a   Horswill, Alexander R ^b   Smeltzer, Mark S ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINASE; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEREMIA; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BIOFILM; ENZYME SYNTHESIS; GENE MUTATION; GENETIC CODE; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; STAPHYLOCOCCUS AUREUS;

ANIMALS; ANIMALS, OUTBRED STRAINS; ANTI-BACTERIAL AGENTS; BACTEREMIA; BACTERIAL PROTEINS; BIOFILMS; CATHETER-RELATED INFECTIONS; DAPTOMYCIN; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MICE; MICROBIAL SENSITIVITY TESTS; PEPTIDE HYDROLASES; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE; VIRULENCE FACTORS;

MURINAE; STAPHYLOCOCCUS AUREUS;

EID: 84870236227     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12048     Document Type: Article

References (60)

1. Abraham, N.M., and Jefferson, K.K. (2012) Staphylococcus aureus clumping factor B mediates biofilm formation in the absence of calcium. Microbiology 158: 1504-1512.
2. Artini, M., Scoarughi, G.L., Papa, R., Cellini, A., Carpentieri, A., Pucci, P., etal. (2011) A new anti-infective strategy to reduce adhesion-mediated virulence in Staphylococcus aureus affecting surface proteins. Int J Immunopathol Pharmacol 24: 661-672.
3. Beenken, K.E., Mrak, L.N., Griffin, L.M., Zielinska, A.K., Shaw, L.N., Rice, K.C., etal. (2010) Epistatic relationships between sarA and agr in Staphylococcus aureus biofilm formation. PLoS ONE 5: e10790.
4. Beenken, K.E., Spencer, H., Griffin, L.M., and Smeltzer, M.S. (2012) Impact of extracellular nuclease production on the biofilm phenotype of Staphylococcus aureus under in vitro and in vivo conditions. Infect Immun 80: 1634-1638.
5. Bischoff, M., and Berger-Bächi, B. (2001) Teicoplanin stress-selected mutations increasing sigma(B) activity in Staphylococcus aureus. Antimicrob Agents Chemother 45: 1714-1720.
6. Blevins, J.S., Gillaspy, A.F., Rechtin, T.M., Hurlburt, B.K., and Smeltzer, M.S. (1999) The staphylococcal accessory regulator (sar) represses transcription of the Staphylococcus aureus collagen adhesion gene (cna) in an agr-independent manner. Mol Microbiol 33: 317-326.
7. Blevins, J.S., Beenken, K.E., Elasri, M.O., Hurlburt, B.K., and Smeltzer, M.S. (2002) Strain-dependent differences in the regulatory roles of sarA and agr in Staphylococcus aureus. Infect Immun 70: 470-480.
8. Blevins, J.S., Elasri, M.O., Allmendinger, S.D., Beenken, K.E., Skinner, R.A., Thomas, J.R., Smeltzer, M.S. (2003) Role of sarA in the pathogenesis of Staphylococcus aureus musculoskeletal infection. Infect Immun 71: 516-523.
9. Booth, M.C., Cheung, A.L., Hatter, K.L., Jett, B.D., Callegan, M.C., Gilmore, M.S. (1997) Staphylococcal accessory regulator (sar) in conjunction with agr contributes to Staphylococcus aureus virulence in endophthalmitis. Infect Immun 65: 1550-1556.
10. Carneiro, C.R., Postol, E., Nomizo, R., Reis, L.F., and Brentani, R.R. (2004) Identification of enolase as a laminin-binding protein on the surface of Staphylococcus aureus. Microbes Infect 6: 604-608.
11. Cassat, J., Dunman, P.M., Murphy, E., Projan, S.J., Beenken, K.E., Palm, K.J., etal. (2006) Transcriptional profiling of a Staphylococcus aureus clinical isolate and its isogenic agr and sarA mutants reveals global differences in comparison to the laboratory strain RN6390. Microbiology 152: 3075-3090.
12. Cheng, A.G., Kim, H.K., Burts, M.L., Krausz, T., Schneewind, O., Missiakas, D.M. (2009) Genetic requirements for Staphylococcus aureus abscess formation and persistence in host tissues. FASEB J 23: 3393-3404.
13. Cheung, A.L., and Ying, P. (1994) Regulation of alpha- and beta-hemolysins by the sar locus of Staphylococcus aureus. J Bacteriol 176: 580-585.
14. Cheung, G.Y., Wang, R., Khan, B.A., Sturdevant, D.E., and Otto, M. (2011) Role of the accessory gene regulator agr in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. Infect Immun 79: 1927-1935.
15. Chien, Y., Manna, A.C., Projan, S.J., and Cheung, A.L. (1999) SarA, a global regulator of virulence determinants in Staphylococcus aureus, binds to a conserved motif essential for sar-dependent gene regulation. J Biol Chem 274: 37169-37176.
16. Corrigan, R.M., Miajlovic, H., and Foster, T.J. (2009) Surface proteins that promote adherence of Staphylococcus aureus to human desquamated nasal epithelial cells. BMC Microbiol 9: 22.
17. Didier, J.P., Cozzone, A.J., and Duclos, B. (2010) Phosphorylation of the virulence regulator SarA modulates its ability to bind DNA in Staphylococcus aureus. FEMS Microbiol Lett 306: 30-36.
18. Diep, B.A., Gill, S.R., Chang, R.F., Phan, T.H., Chen, J.H., Davidson, M.G., etal. (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367: 731-739.
19. Dinges, M.M., Orwin, P.M., and Schlievert, P.M. (2000) Exotoxins of Staphylococcus aureus. Clin Microbiol Rev 13: 16-34.
20. Dunman, P.M., Murphy, E., Haney, S., Palacios, D., Tucker-Kellogg, G., Wu, S., etal. (2001) Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J Bacteriol 183: 7341-7353.
21. Fujimoto, D.F., Higginbotham, R.H., Sterba, K.M., Maleki, S.J., Segall, A.M., Smeltzer, M.S., Hurlburt, B.K. (2009) Staphylococcus aureus SarA is a regulatory protein responsive to redox and pH that can support bacteriophage lambda integrase-mediated excision/recombination. Mol Microbiol 74: 1445-1458.
22. Haupt, K., Reuter, M., van den Elsen, J., Burman, J., Halbich, S., Richter, J., etal. (2008) The Staphylococcus aureus protein Sbi acts as a complement inhibitor and forms a tripartite complex with host complement Factor H and C3b. PLoS Pathog 4: e1000250.
23. Heilmann, C., Hartleib, J., Hussain, M.S., and Peters, G. (2005) The multifunctional Staphylococcus aureus autolysin AAA mediates adherence to immobilized fibrinogen and fibronectin. Infect Immun 73: 4793-4802.
24. Houston, P., Rowe, S.E., Pozzi, C., Waters, E.M., and O'Gara, J.P. (2011) Essential role for the major autolysin in the fibronectin-binding protein-mediated Staphylococcus aureus biofilm phenotype. Infect Immun 79: 1153-1165.
25. Hsieh, H.Y., Tseng, C.W., and Stewart, G.C. (2008) Regulation of Rot expression in Staphylococcus aureus. J Bacteriol 190: 546-554.
26. Hu, C., Xiong, N., Zhang, Y., Rayner, S., and Chen, S. (2012) Functional characterization of lipase in the pathogenesis of Staphylococcus aureus. Biochem Biophys Res Commun 419: 617-620.
27. Jacobsson, G., Colque-Navarro, P., Gustafsson, E., Andersson, R., and Mollby, R. (2010) Antibody responses in patients with invasive Staphylococcus aureus infections. Eur J Clin Microbiol Infect Dis 29: 715-725.
28. Jones, R.C., Deck, J., Edmondson, R.D., and Hart, M.E. (2008) Relative quantitative comparisons of the extracellular protein profiles of Staphylococcus aureus UAMS-1 and its sarA, agr, and sarA agr regulatory mutants using one-dimensional polyacrylamide gel electrophoresis and nanocapillary liquid chromatography coupled with tandem mass spectrometry. J Bacteriol 190: 5265-5278.
29. Kalscheur, V.L. (2001) Bone and cartilage changes in osteoarthritis: a proteoglycan stain. Histologic 34: 14-15.
30. Karlsson, A., Saravia-Otten, P., Tegmark, K., Morfeldt, E., and Arvidson, S. (2001) Decreased amounts of cell wall-associated protein A and fibronectin-binding proteins in Staphylococcus aureus sarA mutants due to up-regulation of extracellular proteases. Infect Immun 69: 4742-4748.
31. Kennedy, A.D., Otto, M., Braughton, K.R., Whitney, A.R., Chen, L., Mathema, B., etal. (2008) Epidemic community-associated methicillin-resistant Staphylococcus aureus: recent clonal expansion and diversification. Proc Natl Acad Sci USA 105: 1327-1332.
32. Kielian, T., Cheung, A., and Hickey, W.F. (2001) Diminished virulence of an alpha-toxin mutant of Staphylococcus aureus in experimental brain abscesses. Infect Immun 69: 6902-6911.
33. Kwiecinski, J., Josefsson, E., Mitchell, J., Higgins, J., Magnusson, M., Foster, T., etal. (2010) Activation of plasminogen by staphylokinase reduces the severity of Staphylococcus aureus systemic infection. J Infect Dis 202: 1041-1049.
34. Li, M., Cheung, G.Y., Hu, J., Wang, D., and Joo, H.S. (2010) Comparative analysis of virulence and toxin expression of global community-associated methicillin-resistant Staphylococcus aureus strains. J Infect Dis 202: 1866-1876.
35. Lin, M.H., Shu, J.C., Huang, H.Y., and Cheng, Y.C. (2012) Involvement of iron in biofilm formation by Staphylococcus aureus. PLoS ONE 7: e34388.
36. Merino, N., Toledo-Arana, A., Vergara-Irigaray, M., Valle, J., Solano, C., Calvo, E., etal. (2009) Protein A-mediated multicellular behavior in Staphylococcus aureus. J Bacteriol 191: 832-843.
37. Molkanen, T., Tyynela, J., Helin, J., Kalkkinen, N., and Kuusela, P. (2002) Enhanced activation of bound plasminogen on Staphylococcus aureus by staphylokinase. FEBS Lett 517: 72-78.
38. Morrison, J.M.A.K., Beenken, K.E., Smeltzer, M.S., and Dunman, P.M. (2012) The staphylococcal accessory regulator, SarA, is an RNA-binding protein that modulates the mRNA turnover properties of late-exponential and stationary phase Staphylococcus aureus cells. Front Cell Infect Microbiol 2: 26.
39. Mrak, L.N., Zielinska, A.K., Beenken, K.E., Mrak, I.N., and Atwood, D.N. (2012) saeRS and sarA act synergistically to repress protease production and promote biofilm formation in Staphylococcus aureus. PLoS ONE 7: e38453.
40. Nakakido, M., Tanaka, Y., and Tsumoto, K. (2007) The N-terminal domain of elastin-binding protein of Staphylococcus aureus changes its secondary structure in a membrane-mimetic environment. J Biochem 142: 131-134.
41. Nilsson, I.M., Bremell, T., Rydén, C., Cheung, A.L., and Tarkowski, A. (1996) Role of the staphylococcal accessory gene regulator (sar) in septic arthritis. Infect Immun 64: 4438-4443.
42. Nilsson, I.M., Hartford, O., Foster, T., and Tarkowski, A. (1999) Alpha-toxin and gamma-toxin jointly promote Staphylococcus aureus virulence in murine septic arthritis. Infect Immun 67: 1045-1049.
43. Novick, R.P. (2003) Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 49: 93-105.
44. O'Brien, L., Kerrigan, S.W., Kaw, G., Hogan, M., Penades, J., Litt, D., etal. (2002) Multiple mechanisms for the activation of human platelet aggregation by Staphylococcus aureus: roles for the clumping factors ClfA and ClfB, the serine-aspartate repeat protein SdrE and protein A. Mol Microbiol 44: 1033-1044.
45. Oscarsson, J., Kanth, A., Tegmark-Wisell, K., and Arvidson, S. (2006) SarA is a repressor of hla (alpha-hemolysin) transcription in Staphylococcus aureus: its apparent role as an activator of hla in the prototype strain NCTC 8325 depends on reduced expression of sarS. J Bacteriol 188: 8526-8533.
46. Park, P.W., Rosenbloom, J., Abrams, W.R., and Mecham, R.P. (1996) Molecular cloning and expression of the gene for elastin-binding protein (ebpS) in Staphylococcus aureus. J Biol Chem 271: 15803-15809.
47. Rechtin, T.M., Gillaspy, A.F., Schumacher, M.A., Brennan, R.G., Smeltzer, M.S., Hurlburt, B.K. (1999) Characterization of the SarA virulence gene regulator of Staphylococcus aureus. Mol Microbiol 33: 307-316.
48. Reyes, D., Andrey, D.O., Monod, A., Kelley, W.L., Zhang, G., Cheung, A.L. (2011) Coordinated regulation by AgrA, SarA, and SarR to control agr expression in Staphylococcus aureus. J Bacteriol 193: 6020-6031.
49. Roberts, C., Anderson, K.L., Murphy, E., Projan, S.J., Mounts, W., Hurlburt, B., etal. (2006) Characterizing the effect of the Staphylococcus aureus virulence factor regulator, SarA, on log-phase mRNA half-lives. J Bacteriol 188: 2593-2603.
50. Schlievert, P.M., Jablonski, L.M., Roggiani, M., Sadler, I., Callantine, S., Mitchell, D.T., etal. (2000) Pyrogenic toxin superantigen site specificity in toxic shock syndrome and food poisoning in animals. Infect Immun 68: 3630-3634.
51. Skinner, R.A., Hickmon, S.G., Nelson, C.L., and Germer, R.A. (1992) Modified stain for identification of Staphylococcus aureus in osteomyelitis. J Histotechnol 15: 303-306.
52. Skinner, R.A., Hickmon, S.G., Lumpkin, C.K., Aronson, J.A., and Nicholas, R.W. (1997) Decalcified bone: twenty years of successful specimen management. J Histotechnol 20: 267-277.
53. Smith, E.J., Corrigan, R.M., van der Sluis, T., Grundling, A., Speziale, P., Geoghegan, J.A., Foster, T.J. (2012) The immune evasion protein Sbi of Staphylococcus aureus occurs both extracellularly and anchored to the cell envelope by binding lipoteichoic acid. Mol Microbiol 83: 789-804.
54. Somerville, G.A., and Proctor, R.A. (2009) At the crossroads of bacterial metabolism and virulence factor synthesis in staphylococci. Microbiol Mol Biol Rev 73: 233-248.
55. Sterba, K.M., Mackintosh, S.G., Blevins, J.S., Hurlburt, B.K., and Smeltzer, M.S. (2003) Characterization of Staphylococcus aureus SarA binding sites. J Bacteriol 185: 4410-4417.
56. Thurlow, L.R., Hanke, M.L., Fritz, T., Angle, A., Aldrich, A., Williams, S.H., etal. (2011) Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. J Immunol 186: 6585-6596.
57. Weiss, E.C., Spencer, H.J., Daily, S.J., Weiss, B.D., and Smeltzer, M.S. (2009a) Impact of sarA on antibiotic susceptibility of Staphylococcus aureus in a catheter-associated in vitro model of biofilm formation. Antimicrob Agents Chemother 53: 2475-2482.
58. Weiss, E.C., Zielinska, A., Beenken, K.E., Spencer, H.J., Daily, S.J., Smeltzer, M.S. (2009b) Impact of sarA on daptomycin susceptibility of Staphylococcus aureus biofilms in vivo. Antimicrob Agents Chemother 53: 4096-4102.
59. Wörmann, M.E., Reichmann, N.T., Malone, C.L., Horswill, A.R., and Gründling, A. (2011) Proteolytic cleavage inactivates the Staphylococcus aureus lipoteichoic acid synthase. J Bacteriol 193: 5279-5291.
60. Zielinska, A.K., Beenken, K.E., Joo, H.S., Mrak, L.N., Griffin, L.M., Luong, T.T., etal. (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.