Genotypic diversity of Staphylococcus aureus α-hemolysin gene (HLA) and its association with clonal background: Implications for vaccine development

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Xiao, Meng ^a   Zhao, Rui ^b   Zhang, Qi ^a   Fan, Xin ^a   O'Sullivan, Matthew V N ^c,d   Li, Dong Fang ^e   Wang, Xin Ying ^e   Wu, Hong Long ^e   Kong, Fanrong ^c   Xu, Ying Chun ^a  

^a PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

^b BEIJING ELECTRIC POWER HOSPITAL   (China)

^c UNIVERSITY OF SYDNEY   (Australia)

^d University of Sydney   (Australia)

^e Tianjin Translational Genomics Center   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA HEMOLYSIN; BACTERIAL PROTEIN; BACTERIAL TOXIN; HEMOLYSIN; MECA PROTEIN, STAPHYLOCOCCUS AUREUS; PENICILLIN BINDING PROTEIN; STAPHYLOCOCCAL ALPHA-TOXIN; VIRULENCE FACTOR;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ISOLATE; CHINA; CONTROLLED STUDY; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HLA GENE; MECA GENE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN SUSCEPTIBLE STAPHYLOCOCCUS AUREUS; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PHENOTYPE; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIVERSITY; STAPHYLOCOCCUS AUREUS; ALGORITHM; GENETICS; HUMAN; MICROBIOLOGY; MUTATION; PENICILLIN RESISTANCE; STAPHYLOCOCCUS INFECTION;

ALGORITHMS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CHINA; GENOME, BACTERIAL; GENOTYPE; HEMOLYSIN PROTEINS; HUMANS; METHICILLIN RESISTANCE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MULTILOCUS SEQUENCE TYPING; MUTATION; PENICILLIN-BINDING PROTEINS; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE FACTORS;

EID: 84959378558     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0149112     Document Type: Article

References (33)

1. Stryjewski ME, Corey GR. Methicillin-resistant Staphylococcus aureus: an evolving pathogen. Clin Infect Dis. 2014; 58 Suppl 1:S10-9. doi: 10.1093/cid/cit613 PMID: 24343827.
2. Chen Y, Yeh AJ, Cheung GY, Villaruz AE, Tan VY, Joo HS, et al. Basis of virulence in a Panton-Valentine leukocidin-negative community-associated methicillin-resistant Staphylococcus aureus strain. J Infect Dis. 2015; 211(3):472-80. doi: 10.1093/infdis/jiu462 PMID: 25139021.
3. Foster TJ, Geoghegan JA, Ganesh VK, Hook M. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol. 2014; 12(1):49-62.
4. Berube BJ, Bubeck Wardenburg J. Staphylococcus aureus alpha-toxin: nearly a century of intrigue. Toxins (Basel). 2013; 5(6):1140-66.
5. Walker B, Krishnasastry M, Zorn L, Kasianowicz J, Bayley H. Functional expression of the alpha-hemolysin of Staphylococcus aureus in intact Escherichia coli and in cell lysates. J Biol Chem. 1992; 267 (15):10902-9. PMID: 1587866.
6. Menzies BE, Kernodle DS. Site-directed mutagenesis of the alpha-toxin gene of Staphylococcus aureus: role of histidines in toxin activity in vitro and in a murine model. Infect Immun. 1994; 62 (5):1843-7. PMID: 8168947; PubMed Central PMCID: PMC186423.
7. Walker B, Bayley H. Key residues for membrane binding, oligomerization, and pore forming activity of staphylococcal alpha-hemolysin identified by cysteine scanning mutagenesis and targeted chemical modification. J Biol Chem. 1995; 270(39):23065-71. PMID: 7559447.
8. Xiao M, Wang H, Zhao Y, Mao LL, Brown M, Yu YS, et al. National surveillance of methicillin-resistant Staphylococcus aureus in China highlights a still-evolving epidemiology with 15 novel emerging multilocus sequence types. J Clin Microbiol. 2013; 51(11):3638-44. doi: 10.1128/JCM.01375-13 PMID: 23985906; PubMed Central PMCID: PMC3889745.
9. Al-Talib H, Yean CY, Al-Khateeb A, Hassan H, Singh KK, Al-Jashamy K, et al. A pentaplex PCR assay for the rapid detection of methicillin-resistant Staphylococcus aureus and Panton-Valentine Leucocidin. BMC Microbiol. 2009; 9:113. doi: 10.1186/1471-2180-9-113 PMID: 19476638; PubMed Central PMCID: PMC2700277.
10. Gray GS, Kehoe M. Primary sequence of the alpha-toxin gene from Staphylococcus aureus wood 46. Infect Immun. 1984; 46(2):615-8. PMID: 6500704; PubMed Central PMCID: PMC261580.
11. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol. 2000; 38(3):1008-15. PMID: 10698988; PubMed Central PMCID: PMC86325.
12. Koreen L, Ramaswamy SV, Graviss EA, Naidich S, Musser JM, Kreiswirth BN. spa typing method for discriminating among Staphylococcus aureus isolates: implications for use of a single marker to detect genetic micro- and macrovariation. J Clin Microbiol. 2004; 42(2):792-9. PMID: 14766855; PubMed Central PMCID: PMC344479.
13. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol. 2004; 186(5):1518-30. PMID: 14973027; PubMed Central PMCID: PMC344416.
14. Chen L, Mediavilla JR, Oliveira DC, Willey BM, de Lencastre H, Kreiswirth BN. Multiplex real-time PCR for rapid Staphylococcal cassette chromosome mec typing. J Clin Microbiol. 2009; 47(11):3692-706. doi: 10.1128/JCM.00766-09 PMID: 19726600; PubMed Central PMCID: PMC2772623.
15. Stinear TP, Holt KE, Chua K, Stepnell J, Tuck KL, Coombs G, et al. Adaptive change inferred from genomic population analysis of the ST93 epidemic clone of community-associated methicillin-resistant Staphylococcus aureus. Genome Biol Evol. 2014; 6(2):366-78. doi: 10.1093/gbe/evu022 PMID: 24482534; PubMed Central PMCID: PMC3942038.
16. Holden MT, Hsu LY, Kurt K, Weinert LA, Mather AE, Harris SR, et al. A genomic portrait of the emergence, evolution, and global spread of a methicillin-resistant Staphylococcus aureus pandemic. Genome Res. 2013; 23(4):653-64. doi: 10.1101/gr.147710.112 PMID: 23299977; PubMed Central PMCID: PMC3613582.
17. McAdam PR, Templeton KE, Edwards GF, Holden MT, Feil EJ, Aanensen DM, et al. Molecular tracing of the emergence, adaptation, and transmission of hospital-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A. 2012; 109(23):9107-12. doi: 10.1073/pnas.1202869109 PMID: 22586109; PubMed Central PMCID: PMC3384211.
18. Kurt K, Rasigade JP, Laurent F, Goering RV, Zemlickova H, Machova I, et al. Subpopulations of Staphylococcus aureus clonal complex 121 are associated with distinct clinical entities. PLoS One. 2013; 8 (3):e58155. doi: 10.1371/journal.pone.0058155 PMID: 23505464; PubMed Central PMCID: PMC3591430.
19. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25(14):1754-60.
20. Mathur P, Singh S. Multidrug resistance in bacteria: a serious patient safety challenge for India. J Lab Physicians. 2013; 5(1):5-10. doi: 10.4103/0974-2727.115898 PMID: 24014960; PubMed Central PMCID: PMC3758706.
21. Xiao YH, Giske CG, Wei ZQ, Shen P, Heddini A, Li LJ. Epidemiology and characteristics of antimicrobial resistance in China. Drug Resist Updat. 2011; 14(4-5):236-50. doi: 10.1016/j.drup.2011.07.001 PMID: 21807550.
22. Ohlsen K, Lorenz U. Immunotherapeutic strategies to combat staphylococcal infections. Int J Med Microbiol. 2010; 300(6):402-10. doi: 10.1016/j.ijmm.2010.04.015 PMID: 20547101.
23. Vandenesch F, Lina G, Henry T. Staphylococcus aureus hemolysins, bi-component leukocidins, and cytolytic peptides: a redundant arsenal of membrane-damaging virulence factors? Front Cell Infect Microbiol. 2012; 2:12. doi: 10.3389/fcimb.2012.00012 PMID: 22919604; PubMed Central PMCID: PMC3417661.
24. Kennedy AD, Bubeck Wardenburg J, Gardner DJ, Long D, Whitney AR, Braughton KR, et al. Targeting of alpha-hemolysin by active or passive immunization decreases severity of USA300 skin infection in a mouse model. J Infect Dis. 2010; 202(7):1050-8. doi: 10.1086/656043 PMID: 20726702; PubMed Central PMCID: PMC2945289.
25. Mocca CP, Brady RA, Burns DL. Role of antibodies in protection elicited by active vaccination with genetically inactivated alpha hemolysin in a mouse model of Staphylococcus aureus skin and soft tissue infections. Clin Vaccine Immunol. 2014; 21(5):622-7. doi: 10.1128/CVI.00051-14 PMID: 24574539; PubMed Central PMCID: PMC4018873.
26. Ragle BE, Bubeck Wardenburg J. Anti-alpha-hemolysin monoclonal antibodies mediate protection against Staphylococcus aureus pneumonia. Infect Immun. 2009; 77(7):2712-8. doi: 10.1128/IAI. 00115-09 PMID: 19380475; PubMed Central PMCID: PMC2708543.
27. DeLeo FR, Kennedy AD, Chen L, Bubeck Wardenburg J, Kobayashi SD, Mathema B, et al. Molecular differentiation of historic phage-type 80/81 and contemporary epidemic Staphylococcus aureus. Proc Natl Acad Sci U S A. 2011; 108(44):18091-6. doi: 10.1073/pnas.1111084108 PMID: 22025717; PubMed Central PMCID: PMC3207694.
28. McGavin MJ, Arsic B, Nickerson NN. Evolutionary blueprint for host- and niche-adaptation in Staphylococcus aureus clonal complex CC30. Front Cell Infect Microbiol. 2012; 2:48. doi: 10.3389/fcimb.2012. 00048 PMID: 22919639; PubMed Central PMCID: PMC3417553.
29. Menzies BE, Kernodle DS. Passive immunization with antiserum to a nontoxic alpha-toxin mutant from Staphylococcus aureus is protective in a murine model. Infect Immun. 1996; 64(5):1839-41. PMID: 8613399; PubMed Central PMCID: PMC174000.
30. Carvalho KS, Mamizuka EM, Gontijo Filho PP. Methicillin/Oxacillin-resistant Staphylococcus aureus as a hospital and public health threat in Brazil. Braz J Infect Dis. 2010; 14(1):71-6. PMID: 20428658.
31. Chen H, Liu Y, Jiang X, Chen M, Wang H. Rapid change of methicillin-resistant Staphylococcus aureus clones in a Chinese tertiary care hospital over a 15-year period. Antimicrob Agents Chemother. 2010; 54(5):1842-7. doi: 10.1128/AAC.01563-09 PMID: 20176895; PubMed Central PMCID: PMC2863666.
32. Gray RR, Tatem AJ, Johnson JA, Alekseyenko AV, Pybus OG, Suchard MA, et al. Testing spatiotemporal hypothesis of bacterial evolution using methicillin-resistant Staphylococcus aureus ST239 genome-wide data within a bayesian framework. Mol Biol Evol. 2011; 28(5):1593-603. doi: 10.1093/molbev/msq319 PMID: 21112962; PubMed Central PMCID: PMC3115679.
33. Mediavilla JR, Chen L, Mathema B, Kreiswirth BN. Global epidemiology of community-associated methicillin resistant Staphylococcus aureus (CA-MRSA). Curr Opin Microbiol. 2012; 15(5):588-95.