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Powerful usage of phylogenetically diverse Staphylococcus aureus control strains for detecting multidrug resistance genes in transcriptomics studies

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Molecules and Cells

Abstract

Staphylococcus aureus is an important human pathogen responsible for life-threatening septicemia, endocarditis, and toxic shock syndrome. Although positive (MRSA; ATCC 33591) and negative (MSSA; ATCC 25923) control strains have been used for various pathogenesis or assay studies, little is known about the genomic structure of the strains, and there has been little genome-wide expression analysis. Phylogenetic analyses revealed that ATCC 33591 and ATCC 25923 are the most genetically diverse strains of the 15 S. aureus genomes studied. Microarray analysis showed that the most significantly upregulated group of MRSA genes was the transport group, which includes ATP-binding cassette (ABC) transporters, the two-component system, and the phosphotransferase system. Analysis of the KEGG pathway showed that ABC transporters and the two-component system were the most significantly altered in MRSA. Transcriptional profiling showed a clear difference in gene expression between MRSA and MSSA due to the great genetic distance between the two control strains. Therefore, we suggest that use of the two control strains in comparative genomics or transcriptomics studies would facilitate the identification of major genes for drug resistance in S. aureus.

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References

  • Al-Talib, H., Yean, C.Y., Al-Khateeb, A., Hassan, H., Singh, K.K., Al-Jashamy, K., and Ravichandran, M. (2009). A pentaplex PCR assay for the rapid detection of methicillin-resistant Staphylococcus aureus and Panton-Valentine Leucocidin. BMC Microbiol. 9, 113.

    Article  PubMed  Google Scholar 

  • Baba, T., Bae, T., Schneewind, O., Takeuchi, F., and 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.

    Article  CAS  PubMed  Google Scholar 

  • Cespedes, C., Said-Salim, B., Miller, M., Lo, S.H., Kreiswirth, B.N., Gordon, R.J., Vavagiakis, P., Klein, R.S., and Lowy, F.D. (2005). The clonality of Staphylococcus aureus nasal carriage. J. Infect. Dis. 191, 444–452.

    Article  PubMed  Google Scholar 

  • Corey, G.R. (2009). Staphylococcus aureus bloodstream infections: definitions and treatment. Clin. Infect. Dis. 48, S254–259.

    Article  PubMed  Google Scholar 

  • Dawson, R.J., and Locher, K.P. (2006). Structure of a bacterial multidrug ABC transporter. Nature 443, 180–185.

    Article  CAS  PubMed  Google Scholar 

  • Dawson, R.J., and Locher, K.P. (2007). Structure of the multidrug ABC transporter Sav1866 from Staphylococcus aureus in complex with AMP-PNP. FEBS Lett. 581, 935–938.

    Article  CAS  PubMed  Google Scholar 

  • Diep, B.A., Palazzolo-Ballance, A.M., Tattevin, P., Basuino, L., Braughton, K.R., Whitney, A.R., Chen, L., Kreiswirth, B.N., Otto, M., DeLeo, F.R., et al. (2008). Contribution of Panton-Valentine leukocidin in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. PLoS One 3, e3198.

    Article  PubMed  Google Scholar 

  • Gautier, L., Cope, L., Bolstad, B.M., and Irizarry, R.A. (2004). affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20, 307–315.

    Article  CAS  PubMed  Google Scholar 

  • Gottesman, M.M., and Ambudkar, S.V. (2001). Overview: ABC transporters and human disease. J. Bioenerg. Biomembr. 33, 453–458.

    Article  CAS  PubMed  Google Scholar 

  • Gould, I.M. (2005). The clinical significance of methicillin-resistant Staphylococcus aureus. J. Hosp. Infect. 61, 277–282.

    Article  CAS  PubMed  Google Scholar 

  • Hamdad, F., Donda, F., Lefebvre, J.F., Laurans, G., Biendo, M., Thomas, D., Canarelli, B., Rousseau, F., and Eb, F. (2006). Detection of methicillin/oxacillin resistance and typing in aminoglycoside-susceptible methicillin-resistant and kanamycin-tobramycin-resistant methicillin-susceptible Staphylococcus aureus. Microb. Drug Resist. 12, 177–185.

    Article  CAS  PubMed  Google Scholar 

  • Hirakawa, H., Nishino, K., Hirata, T., and Yamaguchi, A. (2003). Comprehensive studies of drug resistance mediated by over-expression of response regulators of two-component signal transduction systems in Escherichia coli. J. Bacteriol. 185, 1851–1856.

    Article  CAS  PubMed  Google Scholar 

  • Holden, M.T.G., Feil, E.J., Lindsay, J.A., Peacock, S.J., Day, N.P.J., Enright, M.C., Foster, T.J., Moore, C.E., Hurst, L., Atkin, R., et al. (2004). Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc. Natl. Acad. Sci. USA 101, 9786–9791.

    Article  CAS  PubMed  Google Scholar 

  • Huang, D.W., Sherman, B.T., and Lempicki, R.A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44–57.

    Article  CAS  Google Scholar 

  • Huijsdens, X.W., van Dijke, B.J., Spalburg, E., van Santen-Verheuvel, M.G., Heck, M.E., Pluister, G.N., Voss, A., Wannet, W.J., and de Neeling, A.J. (2006). Community-acquired MRSA and pig-farming. Ann. Clin. Microbiol. Antimicrob. 5, 26.

    Article  PubMed  Google Scholar 

  • Jansen, A., Turck, M., Szekat, C., Nagel, M., Clever, I., and Bierbaum, G. (2007). Role of insertion elements and yycFG in the development of decreased susceptibility to vancomycin in Staphylococcus aureus. Int. J. Med. Microbiol. 297, 205–215.

    Article  CAS  PubMed  Google Scholar 

  • Kluytmans, J., van Belkum, A., and Verbrugh, H. (1997). Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin. Microbiol. Rev. 10, 505–520.

    CAS  PubMed  Google Scholar 

  • Lemaire, S., Fuda, C., Van Bambeke, F., Tulkens, P.M., and Mobashery, S. (2008a). Restoration of susceptibility of methicillin-resistant Staphylococcus aureus to beta-lactam antibiotics by acidic pH: role of penicillin-binding protein PBP 2a. J. Biol. Chem. 283, 12769–12776.

    Article  CAS  PubMed  Google Scholar 

  • Lemaire, S., Olivier, A., Van Bambeke, F., Tulkens, P.M., Appelbaum, P.C., and Glupczynski, Y. (2008b). Restoration of susceptibility of intracellular methicillin-resistant Staphylococcus aureus to beta-lactams: comparison of strains, cells, and antibiotics. Antimicrob. Agents Chemother. 52, 2797–2805.

    Article  CAS  PubMed  Google Scholar 

  • Lindsay, J.A., and Holden, M.T. (2004). Staphylococcus aureus: superbug, super genome? Trends Microbiol. 12, 378–385.

    Article  CAS  PubMed  Google Scholar 

  • Lindsay, J.A., and Holden, M.T. (2006). Understanding the rise of the superbug: investigation of the evolution and genomic variation of Staphylococcus aureus. Funct. Integr. Genomics 6, 186–201.

    Article  CAS  PubMed  Google Scholar 

  • Loeffler, A., Boag, A.K., Sung, J., Lindsay, J.A., Guardabassi, L., Dalsgaard, A., Smith, H., Stevens, K.B., and Lloyd, D.H. (2005). Prevalence of methicillin-resistant Staphylococcus aureus among staff and pets in a small animal referral hospital in the UK. J. Antimicrob. Chemother. 56, 692–697.

    Article  CAS  PubMed  Google Scholar 

  • Macielag, M.J., and Goldschmidt, R. (2000). Inhibitors of bacterial two-component signalling systems. Expert Opin. Investig. Drugs 9, 2351–2369.

    Article  CAS  PubMed  Google Scholar 

  • Matsushita, M., and Janda, K.D. (2002). Histidine kinases as targets for new antimicrobial agents. Bioorg. Med. Chem. 10, 855–867.

    Article  CAS  PubMed  Google Scholar 

  • Page, R.D.M. (1996). TreeView: An application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12, 357–358.

    CAS  PubMed  Google Scholar 

  • Posada, D., and Crandall, K.A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.

    Article  CAS  PubMed  Google Scholar 

  • Robinson, D.A., and Enright, M.C. (2003). Evolutionary models of the emergence of methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 47, 3926–3934.

    Article  CAS  PubMed  Google Scholar 

  • Ronquist, F., and Huelsenbeck, J.P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.

    Article  CAS  PubMed  Google Scholar 

  • Saiful, A.J., Mastura, M., Zarizal, S., Mazurah, M.I., Shuhaimi, M., and Ali, A.M. (2006). Detection of methicillin-resistant Staphylococcus aureus using mecA/nuc genes and antibiotic susceptibility profile of Malaysian clinical isolates. World J. Microb. Biot. 22, 1289–1294.

    Article  CAS  Google Scholar 

  • Sears, P.M., and McCarthy, K.K. (2003). Management and treatment of staphylococcal mastitis. Vet. Clin. North Am. Food Anim. Pract. 19, 171–185, vii.

    Article  PubMed  Google Scholar 

  • Sergi, S., Donnarumma, F., Mastromei, G., Goti, E., Nicoletti, P., Pecile, P., Cecconi, D., Mannino, R., Fanci, R., Bosi, A., et al. (2009). Molecular surveillance and population structure analysis of methicillin-susceptible and methicillin-resistant Staphylococcus aureus in high-risk wards. J. Clin. Microbiol. 47, 3246–3254.

    Article  CAS  PubMed  Google Scholar 

  • Suhaili, Z., Johari, S.A., Mohtar, M., Abdullah, A.R.T., Ahmad, A., and Ali, A.M. (2009). Detection of Malaysian methicillin-resistant Staphylococcus aureus (MRSA) clinical isolates using simplex and duplex real-time PCR. World J. Microb. Biot. 25, 253–258.

    Article  CAS  Google Scholar 

  • Sung, J.M., Lloyd, D.H., and Lindsay, J.A. (2008). Staphylococcus aureus host specificity: comparative genomics of human versus animal isolates by multi-strain microarray. Microbiology 154, 1949–1959.

    Article  CAS  PubMed  Google Scholar 

  • Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876–4882.

    Article  CAS  PubMed  Google Scholar 

  • Weese, J.S., Archambault, M., Willey, B.M., Hearn, P., Kreiswirth, B.N., Said-Salim, B., McGeer, A., Likhoshvay, Y., Prescott, J.F., and Low, D.E. (2005). Methicillin-resistant Staphylococcus aureus in horses and horse personnel, 2000–2002. Emerg. Infect. Dis. 11, 430–435.

    CAS  PubMed  Google Scholar 

  • Witte, W. (2000). Selective pressure by antibiotic use in livestock. Int. J. Antimicrob. Agents 16, S19–24.

    Article  CAS  PubMed  Google Scholar 

  • Woo, J.H., Kim, Y.S., and Hwang, S.D. (1997). Regulation of toxic shock syndrome toxin-1 gene in Staphylococcus aureus. Mol. Cells 7, 28–33.

    CAS  PubMed  Google Scholar 

  • Yarwood, J.M., Paquette, K.M., Tikh, I.B., Volper, E.M., and Greenberg, E.P. (2007). Generation of virulence factor variants in Staphylococcus aureus biofilms. J. Bacteriol. 189, 7961–7967.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Bioinformatics and Population Genetics, Department of Agricultural Biotechnology, Seoul National University, Seoul, 151-742, Korea

    Taeheon Lee, Bo-Young Lee, Sook Hee Yoon & Heebal Kim

  2. National Institute of Animal Science, Rural Development Administration, Suwon, 441-706, Korea

    Jun-Sang Ham, Seung-Gyu Lee, Seok-Geun Jeong, Mi-Hwa Oh & Dong-Hun Kim

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  1. Jun-Sang Ham
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  2. Seung-Gyu Lee
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Ham, JS., Lee, SG., Jeong, SG. et al. Powerful usage of phylogenetically diverse Staphylococcus aureus control strains for detecting multidrug resistance genes in transcriptomics studies. Mol Cells 30, 71–76 (2010). https://doi.org/10.1007/s10059-010-0090-3

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  • DOI: https://doi.org/10.1007/s10059-010-0090-3

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