Insights into Alpha-Hemolysin (Hla) evolution and expression among Staphylococcus aureus clones with hospital and community origin

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Tavares, Ana ^a   Nielsen, Jesper B ^b   Boye, Kit ^b   Rohde, Susanne ^b   Paulo, Ana C ^a   Westh, Henrik ^b,c   Schønning, Kristian ^b,c   De Lencastre, Hermínia ^a,d   Miragaia, Maria ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b Mental Health Center Glostrup   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA HEMOLYSIN; AMINO ACID; METICILLIN; VIRULENCE FACTOR; BACTERIAL DNA; BACTERIAL TOXIN; HEMOLYSIN; STAPHYLOCOCCAL ALPHA-TOXIN;

ALLELE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; COMMUNITY CARE; CONTROLLED STUDY; EVOLUTION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE SEQUENCE; GENETIC VARIABILITY; HOSPITAL CARE; HOST CELL; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHYLOGENY; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; COMMUNITY ACQUIRED INFECTION; CROSS INFECTION; DNA SEQUENCE; ENZYMOLOGY; GENETICS; HUMAN; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MULTILOCUS SEQUENCE TYPING; PATHOGENICITY; PENICILLIN RESISTANCE; SINGLE NUCLEOTIDE POLYMORPHISM;

BACTERIAL TOXINS; BASE SEQUENCE; COMMUNITY-ACQUIRED INFECTIONS; CROSS INFECTION; DNA, BACTERIAL; HEMOLYSIN PROTEINS; HUMANS; METHICILLIN RESISTANCE; MICROBIAL SENSITIVITY TESTS; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, DNA; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE FACTORS;

EID: 84904479787     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098634     Document Type: Article

References (50)

1. Deurenberg RH, Stobberingh EE (2009) The molecular evolution of hospital-and community-associated methicillin-resistant Staphylococcus aureus. Curr Mol Med 9: 100-115.
2. David MZ, Daum RS (2010) Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 23: 616-687.
3. Otto M (2013) Community-associated MRSA: What makes them special? Int J Med Microbiol.
4. Kobayashi SD, Voyich JM, Burlak C, DeLeo FR (2005) Neutrophils in the innate immune response. Arch Immunol Ther Exp (Warsz) 53: 505-517. (Pubitemid 43035779)
5. Baba T, Takeuchi F, Kuroda M, Yuzawa H, Aoki K, et al. (2002) Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359: 1819-1827. (Pubitemid 34607058)
6. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, et al. (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367: 731-739. (Pubitemid 43326291)
7. Burlak C, Hammer CH, Robinson MA, Whitney AR, McGavin MJ, et al. (2007) Global analysis of community-associated methicillin-resistant Staphylococcus aureus exoproteins reveals molecules produced in vitro and during infection. Cell Microbiol 9: 1172-1190. (Pubitemid 46547137)
8. Loughman JA, Fritz SA, Storch GA, Hunstad DA (2009) Virulence gene expression in human community-acquired Staphylococcus aureus infection. J Infect Dis 199: 294-301.
9. Li M, Cheung GY, Hu J, Wang D, Joo HS, et al. (2010) Comparative analysis of virulence and toxin expression of global community-associated methicillin-resistant Staphylococcus aureus strains. J Infect Dis 202: 1866-1876.
10. Berube BJ, Bubeck Wardenburg J (2013) Staphylococcus aureus alpha-Toxin: Nearly a Century of Intrigue. Toxins (Basel) 5: 1140-1166.
11. Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, et al. (1996) Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274: 1859-1866. (Pubitemid 26424757)
12. Valeva A, Palmer M, Bhakdi S (1997) Staphylococcal alpha-toxin: formation of the heptameric pore is partially cooperative and proceeds through multiple intermediate stages. Biochemistry 36: 13298-13304. (Pubitemid 27473377)
13. Novick RP, Ross HF, Projan SJ, Kornblum J, Kreiswirth B, et al. (1993) Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 12: 3967-3975. (Pubitemid 23282772)
14. Ballal A, Ray B, Manna AC (2009) sarZ, a sarA family gene, is transcriptionally activated by MgrA and is involved in the regulation of genes encoding exoproteins in Staphylococcus aureus. J Bacteriol 191: 1656-1665.
15. Liang X, Yu C, Sun J, Liu H, Landwehr C, et al. (2006) Inactivation of a two-component signal transduction system, SaeRS, eliminates adherence and attenuates virulence of Staphylococcus aureus. Infect Immun 74: 4655-4665. (Pubitemid 44157253)
16. Liang X, Zheng L, Landwehr C, Lunsford D, Holmes D, et al. (2005) Global regulation of gene expression by ArlRS, a two-component signal transduction regulatory system of Staphylococcus aureus. J Bacteriol 187: 5486-5492. (Pubitemid 41022967)
17. Schmidt KA, Manna AC, Gill S, Cheung AL (2001) SarT, a repressor of alpha-hemolysin in Staphylococcus aureus. Infect Immun 69: 4749-4758. (Pubitemid 32674452)
18. Liang X, Hall JW, Yang J, Yan M, Doll K, et al. (2011) Identification of single nucleotide polymorphisms associated with hyperproduction of alpha-toxin in Staphylococcus aureus. PLoS One 6: e18428.
19. Bubeck Wardenburg J, Bae T, Otto M, Deleo FR, Schneewind O (2007) Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat Med 13: 1405-1406. (Pubitemid 350224232)
20. Bubeck Wardenburg J, Patel RJ, Schneewind O (2007) Surface proteins and exotoxins are required for the pathogenesis of Staphylococcus aureus pneumonia. Infect Immun 75: 1040-1044. (Pubitemid 46203470)
21. Inoshima I, Inoshima N, Wilke GA, Powers ME, Frank KM, et al. (2011) A Staphylococcus aureus pore-forming toxin subverts the activity of ADAM10 to cause lethal infection in mice. Nat Med 17: 1310-1314.
22. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101: 11030-11035. (Pubitemid 38989579)
23. 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.
24. Zielinska AK, Beenken KE, Joo HS, Mrak LN, Griffin LM, et al. (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.
25. De'ath G, Fabricius KE (2000) Classification and regression trees: a powerful yet simple thechnique for ecological data analysis. Ecology. Ecology 81: 3178-3192.
26. Morfeldt E, Taylor D, von Gabain A, Arvidson S (1995) Activation of alphatoxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J 14: 4569-4577.
27. Wilson GJ, Seo KS, Cartwright RA, Connelley T, Chuang-Smith ON, et al. (2011) A novel core genome-encoded superantigen contributes to lethality of community-associated MRSA necrotizing pneumonia. PLoS Pathog 7: e1002271.
28. Montoya M, Gouaux E (2003) Beta-barrel membrane protein folding and structure viewed through the lens of alpha-hemolysin. Biochim Biophys Acta 1609: 19-27. (Pubitemid 36044061)
29. Walker B, Bayley H (1995) 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 270: 23065-23071.
30. DeLeo FR, Kennedy AD, Chen L, Bubeck Wardenburg J, Kobayashi SD, et al. (2011) Molecular differentiation of historic phage-type 80/81 and contemporary epidemic Staphylococcus aureus . Proc Natl Acad Sci U S A 108: 18091-18096.
31. Castillo-Ramirez S, Harris SR, Holden MT, He M, Parkhill J, et al. (2011) The impact of recombination on dN/dS within recently emerged bacterial clones. PLoS Pathog 7: e1002129.
32. Kuhn G, Francioli P, Blanc DS (2006) Evidence for clonal evolution among highly polymorphic genes in methicillin-resistant Staphylococcus aureus. J Bacteriol 188: 169-178.
33. Novick RP (2003) Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48: 1429-1449.
34. Thoendel M, Kavanaugh JS, Flack CE, Horswill AR (2011) Peptide signaling in the staphylococci. Chem Rev 111: 117-151.
35. Tavares A, Miragaia M, Rolo J, Coelho C, de Lencastre H (2013) High prevalence of hospital-associated methicillin-resistant Staphylococcus aureus in the community in Portugal: evidence for the blurring of community-hospital boundaries. Eur J Clin Microbiol Infect Dis 32: 1269-1283.
36. Oliveira DC, Tomasz A, de Lencastre H (2001) The evolution of pandemic clones of methicillin-resistant Staphylococcus aureus: identification of two ancestral genetic backgrounds and the associated mec elements. Microb Drug Resist 7: 349-361. (Pubitemid 34106309)
37. Roberts RB, de Lencastre A, Eisner W, Severina EP, Shopsin B, et al. (1998) Molecular epidemiology of methicillin-resistant Staphylococcus aureus in 12 New York hospitals. MRSA Collaborative Study Group. J Infect Dis 178: 164-171. (Pubitemid 28328089)
38. Aires-de-Sousa M, Correia B, de Lencastre H (2008) Changing patterns in frequency of recovery of five methicillin-resistant Staphylococcus aureus clones in Portuguese hospitals: surveillance over a 16-year period. J Clin Microbiol 46: 2912-2917.
39. Rolo J, Miragaia M, Turlej-Rogacka A, Empel J, Bouchami O, et al. (2012) High Genetic Diversity among Community-Associated Staphylococcus aureus in Europe: Results from a Multicenter Study. PLoS One 7: e34768.
40. Conceicao T, Tavares A, Miragaia M, Hyde K, Aires-de-Sousa M, et al. (2010) Prevalence and clonality of methicillin-resistant Staphylococcus aureus (MRSA) in the Atlantic Azores islands: predominance of SCCmec types IV, V and VI. Eur J Clin Microbiol Infect Dis 29: 543-550.
41. Sa-Leao R, Santos Sanches I, Dias D, Peres I, Barros RM, et al. (1999) Detection of an archaic clone of Staphylococcus aureus with low-level resistance to methicillin in a pediatric hospital in Portugal and in international samples: relics of a formerly widely disseminated strain? J Clin Microbiol 37: 1913-1920. (Pubitemid 29235245)
42. Amorim ML, Aires de Sousa M, Sanches IS, Sa-Leao R, Cabeda JM, et al. (2002) Clonal and antibiotic resistance profiles of methicillin-resistant Staphylococcus aureus (MRSA) from a Portuguese hospital over time. Microb Drug Resist 8: 301-309. (Pubitemid 36043696)
43. Milheirico C, Oliveira DC, de Lencastre H (2007) Multiplex PCR strategy for subtyping the staphylococcal cassette chromosome mec type IV in methicillin-resistant Staphylococcus aureus: 'SCCmec IV multiplex'. J Antimicrob Chemother 60: 42-48. (Pubitemid 47073274)
44. Richardson JF, Reith S (1993) Characterization of a strain of methicillin-resistant Staphylococcus aureus (EMRSA-15) by conventional and molecular methods. J Hosp Infect 25: 45-52. (Pubitemid 23301507)
45. Oliveira DC, Milheirico C, Vinga S, de Lencastre H (2006) Assessment of allelic variation in the ccrAB locus in methicillin-resistant Staphylococcus aureus clones. J Antimicrob Chemother 58: 23-30. (Pubitemid 44294983)
46. Faria NA, Oliveira DC, Westh H, Monnet DL, Larsen AR, et al. (2005) Epidemiology of emerging methicillin-resistant Staphylococcus aureus (MRSA) in Denmark: a nationwide study in a country with low prevalence of MRSA infection. J Clin Microbiol 43: 1836-1842.
47. Sanches IS, Ramirez M, Troni H, Abecassis M, Padua M, et al. (1995) Evidence for the geographic spread of a methicillin-resistant Staphylococcus aureus clone between Portugal and Spain. J Clin Microbiol 33: 1243-1246.
48. de Lencastre H, Chung M, Westh H (2000) Archaic strains of methicillin-resistant Staphylococcus aureus: molecular and microbiological properties of isolates from the 1960s in Denmark. Microb Drug Resist 6: 1-10. (Pubitemid 30367845)
49. Crisostomo MI, Westh H, Tomasz A, Chung M, Oliveira DC, et al. (2001) The evolution of methicillin resistance in Staphylococcus aureus: similarity of genetic backgrounds in historically early methicillin-susceptible and -resistant isolates and contemporary epidemic clones. Proc Natl Acad Sci U S A 98: 9865-9870. (Pubitemid 32769395)
50. McDougal LK, Steward CD, Killgore GE, Chaitram JM, McAllister SK, et al. (2003) Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database. J Clin Microbiol 41: 5113-5120. (Pubitemid 37429924)