Login Register Cart 0
Generic placeholder image

Current Genomics

Editor-in-Chief

ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
General Research Article

Genome Sequence of a Highly Virulent pvl-positive Vancomycin intermediate- resistant Staphylococcus aureus Sequence Type 30

Author(s): Raiane C. Chamon, Lucas M. Marques, Jorge Timenetsky, Caio T.C. da Costa Rachid, Rosana B.R. Ferreira, Tamara L.R. de Oliveira, Thais Glatthardt, Lilian de Oliveira Moreira* and Kátia R.N. dos Santos *

Volume 21, Issue 2, 2020

Page: [128 - 137] Pages: 10

DOI: 10.2174/1389202921666200327105756

Price: $65

Abstract

Background: Staphylococcus aureus isolates expressing the Panton-Valentine Leukocidin (PVL) have been related to a wide range of diseases. Recently, pvl-positive community-associated methicillin-resistant S. aureus belonging to USA1100 (ST30/CC30/SCCmec IV) lineage has emerged in Brazilian hospitals.

Objective: The aim of this work was to sequence the genome of a pvl-positive USA1100 Vancomycin- Intermediate-Resistant S. aureus (VISA) isolate from Rio de Janeiro, Brazil.

Methods: The 13420 genome was sequenced using the HiSeq 2500 platform. The draft genome, plasmids annotation, and genome analysis were performed using RAST. Comparison of the relative pvl gene expression of six S. aureus isolates was performed by qRT-PCR.

Results: The isolate presented the ϕPVL phage codifying for the H2b PVL protein isoform, and another prophage carrying a PVL variant named lukF and lukS-PV.2. The 13420 genome presented a high number of virulence determinants, such as genes codifying for serine-protease proteins, enterotoxins (egc), the immune evasion cluster (IEC), adhesion proteins, spermine/spermidine acetyltransferase gene (blt), superantigen-like proteins, as well as the ica operon. Point mutations at vraS, tcaA, and tcaB genes were detected. Moreover, the PVL mRNA relative expression of the 13420 isolate was five times higher than mRNA PVL levels of the USA300/ST8 reference strain.

Conclusion: We described for the first time the genome sequence of a VISA isolate harboring two pvl-associated genes and other virulence factors that may improve the USA1100/ST30 lineage fitness and impact its pathogenicity and spreading at Brazilian hospitals.

Keywords: S. aureus, pvl-positive, MRSA, VISA, USA1100/ST30, virulence.

« Previous Next »
Graphical Abstract

[1]
Turner, N.A.; Sharma-Kuinkel, B.K.; Maskarinec, S.A.; Eichenberger, E.M.; Shah, P.P.; Carugati, M.; Holland, T.L.; Fowler, V.G., Jr Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research. Nat. Rev. Microbiol., 2019, 17(4), 203-218.
[http://dx.doi.org/10.1038/s41579-018-0147-4] [PMID: 30737488]
[2]
Laurent, F.; Chardon, H.; Haenni, M.; Bes, M.; Reverdy, M.E.; Madec, J.Y.; Lagier, E.; Vandenesch, F.; Tristan, A. MRSA harboring mecA variant gene mecC, France. Emerg. Infect. Dis., 2012, 18(9), 1465-1467.
[http://dx.doi.org/10.3201/eid1809.111920] [PMID: 22932400]
[3]
Becker, K.; van Alen, S.; Idelevich, E.A.; Schleimer, N.; Seggewiß, J.; Mellmann, A.; Kaspar, U.; Peters, G. Plasmid-encoded transferable mecB-mediated methicillin resistance in Staphylococcus aureus. Emerg. Infect. Dis., 2018, 24(2), 242-248.
[http://dx.doi.org/10.3201/eid2402.171074] [PMID: 29350135]
[4]
McGuinness, W.A.; Malachowa, N.; DeLeo, F.R. Vancomycin resistance in Staphylococcus aureus. Yale J. Biol. Med., 2017, 90(2), 269-281.
[PMID: 28656013]
[5]
Howden, B.P.; Davies, J.K.; Johnson, P.D.; Stinear, T.P.; Grayson, M.L. Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomycin-intermediate and heterogeneous vancomycin-intermediate strains: resistance mechanisms, laboratory detection, and clinical implications. Clin. Microbiol. Rev., 2010, 23(1), 99-139.
[http://dx.doi.org/10.1128/CMR.00042-09] [PMID: 20065327]
[6]
Katayama, Y.; Sekine, M.; Hishinuma, T.; Aiba, Y.; Hiramatsu, K. Complete reconstitution of the vancomycin-intermediate Staphylococcus aureus phenotype of strain Mu50 in vancomycin-susceptible S. aureus. Antimicrob. Agents Chemother., 2016, 60(6), 3730-3742.
[http://dx.doi.org/10.1128/AAC.00420-16] [PMID: 27067329]
[7]
Kuroda, M.; Ohta, T.; Uchiyama, I.; Baba, T.; Yuzawa, H.; Kobayashi, I.; Cui, L.; Oguchi, A.; Aoki, K.; Nagai, Y.; Lian, J.; Ito, T.; Kanamori, M.; Matsumaru, H.; Maruyama, A.; Murakami, H.; Hosoyama, A.; Mizutani-Ui, Y.; Takahashi, N.K.; Sawano, T.; Inoue, R.; Kaito, C.; Sekimizu, K.; Hirakawa, H.; Kuhara, S.; Goto, S.; Yabuzaki, J.; Kanehisa, M.; Yamashita, A.; Oshima, K.; Furuya, K.; Yoshino, C.; Shiba, T.; Hattori, M.; Ogasawara, N.; Hayashi, H.; Hiramatsu, K. Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet, 2001, 357(9264), 1225-1240.
[http://dx.doi.org/10.1016/s0140-6736(00)04403-2] [PMID: 11418146]
[8]
Cui, L.; Neoh, H.M.; Shoji, M.; Hiramatsu, K. Contribution of vraSR and graSR point mutations to vancomycin resistance in vancomycin-intermediate Staphylococcus aureus. Antimicrob. Agents Chemother., 2009, 53(3), 1231-1234.
[http://dx.doi.org/10.1128/AAC.01173-08] [PMID: 19124662]
[9]
Spaan, A.N.; van Strijp, J.A.G.; Torres, V.J. Leukocidins: staphylococcal bi-component pore-forming toxins find their receptors. Nat. Rev. Microbiol., 2017, 15(7), 435-447.
[http://dx.doi.org/10.1038/nrmicro.2017.27] [PMID: 28420883]
[10]
Shallcross, L.J.; Fragaszy, E.; Johnson, A.M.; Hayward, A.C. The role of the Panton-Valentine leucocidin toxin in staphylococcal disease: a systematic review and meta-analysis. Lancet Infect. Dis., 2013, 13(1), 43-54.
[http://dx.doi.org/10.1016/S1473-3099(12)70238-4] [PMID: 23103172]
[11]
O’Hara, F.P.; Guex, N.; Word, J.M.; Miller, L.A.; Becker, J.A.; Walsh, S.L.; Scangarella, N.E.; West, J.M.; Shawar, R.M.; Amrine-Madsen, H. A geographic variant of the Staphylococcus aureus Panton-Valentine leukocidin toxin and the origin of community-associated methicillin-resistant S. aureus USA300. J. Infect. Dis., 2008, 197(2), 187-194.
[http://dx.doi.org/10.1086/524684] [PMID: 18177252]
[12]
Tong, S.Y.; Lilliebridge, R.A.; Holt, D.C.; Coombs, G.W.; Currie, B.J.; Giffard, P.M. Rapid detection of H and R Panton-Valentine leukocidin isoforms in Staphylococcus aureus by high-resolution melting analysis. Diagn. Microbiol. Infect. Dis., 2010, 67(4), 399-401.
[http://dx.doi.org/10.1016/j.diagmicrobio.2010.03.015] [PMID: 20638613]
[13]
Strauß, L.; Stegger, M.; Akpaka, P.E.; Alabi, A.; Breurec, S.; Coombs, G.; Egyir, B.; Larsen, A.R.; Laurent, F.; Monecke, S.; Peters, G.; Skov, R.; Strommenger, B.; Vandenesch, F.; Schaumburg, F.; Mellmann, A. Origin, evolution, and global transmission of community-acquired Staphylococcus aureus ST8. Proc. Natl. Acad. Sci. USA, 2017, 114(49), E10596-E10604.
[http://dx.doi.org/10.1073/pnas.1702472114] [PMID: 29158405]
[14]
Chamon, R.C.; Iorio, N.L.; da Silva Ribeiro, S.; Cavalcante, F.S.; Dos Santos, K.R. Molecular characterization of Staphylococcus aureus isolates carrying the Panton-Valentine leukocidin genes from Rio de Janeiro hospitals. Diagn. Microbiol. Infect. Dis., 2015, 83(4), 331-334.
[http://dx.doi.org/10.1016/j.diagmicrobio.2015.09.004] [PMID: 26431830]
[15]
Fernandez, S.; Ledo, C.; Lattar, S.; Noto Llana, M.; Bertelli, A.M.; Di Gregorio, S.; Sordelli, D.O.; Gómez, M.I.; Mollerach, M.E. High virulence of methicillin resistant Staphylococcus aureus ST30-SCCmecIVc-spat019, the dominant community-associated clone in Argentina. Int. J. Med. Microbiol., 2017, 307(4-5), 191-199.
[http://dx.doi.org/10.1016/j.ijmm.2017.05.003] [PMID: 28549830]
[16]
Alam, M.T.; Petit, R.A., III; Crispell, E.K.; Thornton, T.A.; Conneely, K.N.; Jiang, Y.; Satola, S.W.; Read, T.D. Dissecting vancomycin-intermediate resistance in staphylococcus aureus using genome-wide association. Genome Biol. Evol., 2014, 6(5), 1174-1185.
[http://dx.doi.org/10.1093/gbe/evu092] [PMID: 24787619]
[17]
da Costa, T.M.; Morgado, P.G.; Cavalcante, F.S.; Damasco, A.P.; Nouér, S.A.; Dos Santos, K.R. Clinical and microbiological characteristics of heteroresistant and vancomycin-intermediate Staphylococcus aureus from bloodstream infections in a Brazilian teaching hospital. PLoS One, 2016, 11(8) e0160506
[http://dx.doi.org/10.1371/journal.pone.0160506] [PMID: 27575698]
[18]
Milheiriço, C.; Oliveira, D.C.; de Lencastre, H. Update to the multiplex PCR strategy for assignment of mec element types in Staphylococcus aureus. Antimicrob. Agents Chemother., 2007, 51(9), 3374-3377.
[http://dx.doi.org/10.1128/AAC.00275-07] [PMID: 17576837]
[19]
Nurk, S.; Bankevich, A.; Antipov, D.; Gurevich, A.A.; Korobeynikov, A.; Lapidus, A.; Prjibelski, A.D.; Pyshkin, A.; Sirotkin, A.; Sirotkin, Y.; Stepanauskas, R.; Clingenpeel, S.R.; Woyke, T.; McLean, J.S.; Lasken, R.; Tesler, G.; Alekseyev, M.A.; Pevzner, P.A. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J. Comput. Biol., 2013, 20(10), 714-737.
[http://dx.doi.org/10.1089/cmb.2013.0084] [PMID: 24093227]
[20]
Darling, A.E.; Mau, B.; Perna, N.T. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One, 2010, 5(6) e11147
[http://dx.doi.org/10.1371/journal.pone.0011147] [PMID: 20593022]
[21]
Kolmogorov, M.; Raney, B.; Paten, B.; Pham, S. Ragout-a reference-assisted assembly tool for bacterial genomes. Bioinformatics, 2014, 30(12), i302-i309.
[http://dx.doi.org/10.1093/bioinformatics/btu280] [PMID: 24931998]
[22]
Alikhan, N.F.; Petty, N.K.; Ben Zakour, N.L.; Beatson, S.A. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics, 2011, 12, 402.
[http://dx.doi.org/10.1186/1471-2164-12-402] [PMID: 21824423]
[23]
Overbeek, R.; Olson, R.; Pusch, G.D.; Olsen, G.J.; Davis, J.J.; Disz, T.; Edwards, R.A.; Gerdes, S.; Parrello, B.; Shukla, M.; Vonstein, V.; Wattam, A.R.; Xia, F.; Stevens, R. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res., 2014, 42(Database issue), D206-D214.
[http://dx.doi.org/10.1093/nar/gkt1226] [PMID: 24293654]
[24]
Zhou, Y.; Liang, Y.; Lynch, K.H.; Dennis, J.J.; Wishart, D.S. PHAST: a fast phage search tool. Nucleic. Acids. Res, 2011, 39(Web Server issue), W347-W352.
[http://dx.doi.org/10.1093/nar/gkr485]
[25]
Wang, Y.; Coleman-Derr, D.; Chen, G.; Gu, Y.Q. OrthoVenn: a web server for genome wide comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res., 2015, 43(W1), W78-W84.
[http://dx.doi.org/10.1093/nar/gkv487] [PMID: 25964301]
[26]
Gill, S.R.; Fouts, D.E.; Archer, G.L.; Mongodin, E.F.; Deboy, R.T.; Ravel, J.; Paulsen, I.T.; Kolonay, J.F.; Brinkac, L.; Beanan, M.; Dodson, R.J.; Daugherty, S.C.; Madupu, R.; Angiuoli, S.V.; Durkin, A.S.; Haft, D.H.; Vamathevan, J.; Khouri, H.; Utterback, T.; Lee, C.; Dimitrov, G.; Jiang, L.; Qin, H.; Weidman, J.; Tran, K.; Kang, K.; Hance, I.R.; Nelson, K.E.; Fraser, C.M. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J. Bacteriol., 2005, 187(7), 2426-2438.
[http://dx.doi.org/10.1128/JB.187.7.2426-2438.2005] [PMID: 15774886]
[27]
Schuenck, R.P.; Nouér, S.A.; Winter, Cde.O.; Cavalcante, F.S.; Scotti, T.D.; Ferreira, A.L.; Giambiagi-de Marval, M.; dos Santos, K.R. Polyclonal presence of non-multiresistant methicillin-resistant Staphylococcus aureus isolates carrying SCCmec IV in health care-associated infections in a hospital in Rio de Janeiro, Brazil. Diagn. Microbiol. Infect. Dis., 2009, 64(4), 434-441.
[http://dx.doi.org/10.1016/j.diagmicrobio.2009.04.007] [PMID: 19631097]
[28]
Theis, T.; Skurray, R.A.; Brown, M.H. Identification of suitable internal controls to study expression of a Staphylococcus aureus multidrug resistance system by quantitative real-time PCR. J. Microbiol. Methods, 2007, 70(2), 355-362.
[http://dx.doi.org/10.1016/j.mimet.2007.05.011] [PMID: 17590462]
[29]
Dumitrescu, O.; Choudhury, P.; Boisset, S.; Badiou, C.; Bes, M.; Benito, Y.; Wolz, C.; Vandenesch, F.; Etienne, J.; Cheung, A.L.; Bowden, M.G.; Lina, G. Beta-lactams interfering with PBP1 induce Panton-Valentine leukocidin expression by triggering sarA and rot global regulators of Staphylococcus aureus. Antimicrob. Agents Chemother., 2011, 55(7), 3261-3271.
[http://dx.doi.org/10.1128/AAC.01401-10] [PMID: 21502633]
[30]
Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 2001, 25(4), 402-408.
[http://dx.doi.org/10.1006/meth.2001.1262] [PMID: 11846609]
[31]
Bustin, S.A.; Benes, V.; Garson, J.A.; Hellemans, J.; Huggett, J.; Kubista, M.; Mueller, R.; Nolan, T.; Pfaffl, M.W.; Shipley, G.L.; Vandesompele, J.; Wittwer, C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem., 2009, 55(4), 611-622.
[http://dx.doi.org/10.1373/clinchem.2008.112797] [PMID: 19246619]
[32]
Badarau, A.; Rouha, H.; Malafa, S.; Battles, M.B.; Walker, L.; Nielson, N.; Dolezilkova, I.; Teubenbacher, A.; Banerjee, S.; Maierhofer, B.; Weber, S.; Stulik, L.; Logan, D.T.; Welin, M.; Mirkina, I.; Pleban, C.; Zauner, G.; Gross, K.; Jägerhofer, M.; Magyarics, Z.; Nagy, E. Context matters: The importance of dimerization-induced conformation of the LukGH leukocidin of Staphylococcus aureus for the generation of neutralizing antibodies. MAbs, 2016, 8(7), 1347-1360.
[http://dx.doi.org/10.1080/19420862.2016.1215791] [PMID: 27467113]
[33]
Diep, B.A.; Gill, S.R.; Chang, R.F.; Phan, T.H.; Chen, J.H.; Davidson, M.G.; Lin, F.; Lin, J.; Carleton, H.A.; Mongodin, E.F.; Sensabaugh, G.F.; Perdreau-Remington, F. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet, 2006, 367(9512), 731-739.
[http://dx.doi.org/10.1016/S0140-6736(06)68231-7] [PMID: 16517273]
[34]
Holden, M.T.; Feil, E.J.; Lindsay, J.A.; Peacock, S.J.; Day, N.P.; Enright, M.C.; Foster, T.J.; Moore, C.E.; Hurst, L.; Atkin, R.; Barron, A.; Bason, N.; Bentley, S.D.; Chillingworth, C.; Chillingworth, T.; Churcher, C.; Clark, L.; Corton, C.; Cronin, A.; Doggett, J.; Dowd, L.; Feltwell, T.; Hance, Z.; Harris, B.; Hauser, H.; Holroyd, S.; Jagels, K.; James, K.D.; Lennard, N.; Line, A.; Mayes, R.; Moule, S.; Mungall, K.; Ormond, D. Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc. Natl. Acad. Sci. USA, 2004, 101(26), 9786-9791.
[http://dx.doi.org/10.1073/pnas.0402521101] [PMID: 15213324]
[35]
Bosi, E.; Monk, J.M.; Aziz, R.K.; Fondi, M.; Nizet, V.; Palsson, B.Ø. Comparative genome-scale modelling of Staphylococcus aureus strains identifies strain-specific metabolic capabilities linked to pathogenicity. Proc. Natl. Acad. Sci. USA, 2016, 113(26), E3801-E3809.
[http://dx.doi.org/10.1073/pnas.1523199113] [PMID: 27286824]
[36]
Arêde, P.; Ministro, J.; Oliveira, D.C. Redefining the role of the β-lactamase locus in methicillin-resistant Staphylococcus aureus: β-lactamase regulators disrupt the MecI-mediated strong repression on mecA and optimize the phenotypic expression of resistance in strains with constitutive mecA expression. Antimicrob. Agents Chemother., 2013, 57(7), 3037-3045.
[http://dx.doi.org/10.1128/AAC.02621-12] [PMID: 23587945]
[37]
Sieradzki, K.; Tomasz, A. Alterations of cell wall structure and metabolism accompany reduced susceptibility to vancomycin in an isogenic series of clinical isolates of Staphylococcus aureus. J. Bacteriol., 2003, 185(24), 7103-7110.
[http://dx.doi.org/10.1128/JB.185.24.7103-7110.2003] [PMID: 14645269]
[38]
Stentzel, S.; Teufelberger, A.; Nordengrün, M.; Kolata, J.; Schmidt, F.; van Crombruggen, K.; Michalik, S.; Kumpfmüller, J.; Tischer, S.; Schweder, T.; Hecker, M.; Engelmann, S.; Völker, U.; Krysko, O.; Bachert, C.; Bröker, B.M. Staphylococcal serine protease-like proteins are pacemakers of allergic airway reactions to Staphylococcus aureus. J. Allergy Clin. Immunol., 2017, 139(2), 492-500.e8.
[http://dx.doi.org/10.1016/j.jaci.2016.03.045] [PMID: 27315768]
[39]
Song, M.; Shi, C.; Xu, X.; Shi, X. Molecular typing and virulence gene profiles of enterotoxin gene cluster (egc)-positive Staphylococcus aureus isolates obtained from various food and clinical specimens. Foodborne Pathog. Dis., 2016, 13(11), 592-601.
[http://dx.doi.org/10.1089/fpd.2016.2162] [PMID: 27792397]
[40]
Jongerius, I.; Puister, M.; Wu, J.; Ruyken, M.; van Strijp, J.A.; Rooijakkers, S.H. Staphylococcal complement inhibitor modulates phagocyte responses by dimerization of convertases. J. Immunol., 2010, 184(1), 420-425.
[http://dx.doi.org/10.4049/jimmunol.0902865] [PMID: 19949103]
[41]
Haas, P.J.; de Haas, C.J.; Poppelier, M.J.; van Kessel, K.P.; van Strijp, J.A.; Dijkstra, K.; Scheek, R.M.; Fan, H.; Kruijtzer, J.A.; Liskamp, R.M.; Kemmink, J. The structure of the C5a receptor-blocking domain of chemotaxis inhibitory protein of Staphylococcus aureus is related to a group of immune evasive molecules. J. Mol. Biol., 2005, 353(4), 859-872.
[http://dx.doi.org/10.1016/j.jmb.2005.09.014] [PMID: 16213522]
[42]
Schaumburg, F.; Witten, A.; Flamen, A.; Stoll, M.; Alabi, A.S.; Kremsner, P.G.; Löffler, B.; Zipfel, P.F.; Velavan, T.P.; Peters, G. Complement 5a receptor polymorphisms are associated with Panton-Valentine Leukocidin-positive Staphylococcus aureus colonization in African pygmies. Clin. Infect. Dis., 2019, 68(5), 854-856.
[http://dx.doi.org/10.1093/cid/ciy666] [PMID: 30192927]
[43]
Jamrozy, D.M.; Harris, S.R.; Mohamed, N.; Peacock, S.J.; Tan, C.Y.; Parkhill, J.; Anderson, A.S.; Holden, M.T.G. Pan-genomic perspective on the evolution of the Staphylococcus aureus USA300 epidemic. Microb. Genom., 2016, 2(5) e000058
[http://dx.doi.org/10.1099/mgen.0.000058] [PMID: 28348852]
[44]
Seiler, N.; Atanassov, C.L. The natural polyamines and the immune system. Prog. Drug Res., 1994, 43, 87-141.
[http://dx.doi.org/10.1007/978-3-0348-7156-3_4] [PMID: 7855252]
[45]
Joshi, G.S.; Spontak, J.S.; Klapper, D.G.; Richardson, A.R. Arginine catabolic mobile element encoded speG abrogates the unique hypersensitivity of Staphylococcus aureus to exogenous polyamines. Mol. Microbiol., 2011, 82(1), 9-20.
[http://dx.doi.org/10.1111/j.1365-2958.2011.07809.x] [PMID: 21902734]
[46]
Planet, P.J. Life after USA300: The rise and fall of a superbug. J. Infect. Dis., 2017, 215(suppl_1), S71-S77.
[47]
Fournier, B.; Klier, A.; Rapoport, G. The two-component system ArlS-ArlR is a regulator of virulence gene expression in Staphylococcus aureus. Mol. Microbiol., 2001, 41(1), 247-261.
[http://dx.doi.org/10.1046/j.1365-2958.2001.02515.x] [PMID: 11454217]
[48]
Burgui, S.; Gil, C.; Solano, C.; Lasa, I.; Valle, J. A systematic evaluation of the two-component systems network reveals that ArlRS is a key regulator of catheter colonization by Staphylococcus aureus. Front. Microbiol., 2018, 9, 342.
[http://dx.doi.org/10.3389/fmicb.2018.00342] [PMID: 29563900]
[49]
Pragman, A.A.; Yarwood, J.M.; Tripp, T.J.; Schlievert, P.M. Characterization of virulence factor regulation by SrrAB, a two-component system in Staphylococcus aureus. J. Bacteriol., 2004, 186(8), 2430-2438.
[http://dx.doi.org/10.1128/JB.186.8.2430-2438.2004] [PMID: 15060046]
[50]
Lin, L.C.; Chang, S.C.; Ge, M.C.; Liu, T.P.; Lu, J.J. Novel single-nucleotide variations associated with vancomycin resistance in vancomycin-intermediate Staphylococcus aureus. Infect. Drug Resist., 2018, 11, 113-123.
[http://dx.doi.org/10.2147/IDR.S148335] [PMID: 29403293]
[51]
Yoo, J.I.; Kim, J.W.; Kang, G.S.; Kim, H.S.; Yoo, J.S.; Lee, Y.S. Prevalence of amino acid changes in the yvqF, vraSR, graSR, and tcaRAB genes from vancomycin intermediate resistant Staphylococcus aureus. J. Microbiol., 2013, 51(2), 160-165.
[http://dx.doi.org/10.1007/s12275-013-3088-7] [PMID: 23625215]
[52]
Boakes, E.; Kearns, A.M.; Ganner, M.; Perry, C.; Hill, R.L.; Ellington, M.J. Distinct bacteriophages encoding Panton-Valentine leukocidin (PVL) among international methicillin-resistant Staphylococcus aureus clones harboring PVL. J. Clin. Microbiol., 2011, 49(2), 684-692.
[http://dx.doi.org/10.1128/JCM.01917-10] [PMID: 21106787]
[53]
Hiramatsu, K.; Kayayama, Y.; Matsuo, M.; Aiba, Y.; Saito, M.; Hishinuma, T.; Iwamoto, A. Vancomycin-intermediate resistance in Staphylococcus aureus. J. Glob. Antimicrob. Resist., 2014, 2(4), 213-224.
[http://dx.doi.org/10.1016/j.jgar.2014.04.006] [PMID: 27873679]

Rights & Permissions Print Cite
Article Metrics
11
© 2024 Bentham Science Publishers | Privacy Policy