Global changes in staphylococcus aureus gene expression in human blood

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Malachowa, Natalia ^a   Whitney, Adeline R ^a   Kobayashi, Scott D ^a   Sturdevant, Daniel E ^a   Kennedy, Adam D ^a   Braughton, Kevin R ^a   Shabb, Duncan W ^a   Diep, Binh An ^b   Chambers, Henry F ^b   Otto, Michael ^c   DeLeo, Frank R ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA HEMOLYSIN SUBUNIT A; GAMMA HEMOLYSIN SUBUNIT B; GAMMA HEMOLYSIN SUBUNIT C; HEMOLYSIN; LEUKOTOXIN; LEUKOTOXIN D; LEUKOTOXIN E; PANTON VALENTINE LEUKOCIDIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BACTERIAL TOXIN; EXOTOXIN; GAMMA HEMOLYSIN, STAPHYLOCOCCUS AUREUS; GAMMA-HEMOLYSIN, STAPHYLOCOCCUS AUREUS; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEREMIA; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BLOOD CULTURE; CONTROLLED STUDY; CULTURE MEDIUM; ERYTHROPHAGOCYTOSIS; FEMALE; GENE EXPRESSION REGULATION; HEMOLYSIS; HUMAN; HUMAN CELL; MOUSE; NEUTROPHIL; NONHUMAN; SKIN INFECTION; STAPHYLOCOCCUS AUREUS; STRAIN DIFFERENCE; SUPERNATANT; UPREGULATION; WILD TYPE; ANIMAL; CELL MEMBRANE PERMEABILITY; CYTOLOGY; DISEASE MODEL; GENE DELETION; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PATHOGENICITY; POROSITY; SERUM; STAPHYLOCOCCUS INFECTION; VIRULENCE;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CELL MEMBRANE PERMEABILITY; DISEASE MODELS, ANIMAL; EXOTOXINS; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HEMOLYSIN PROTEINS; HUMANS; MICE; MICROBIAL VIABILITY; NEUTROPHILS; POROSITY; RNA, MESSENGER; SERUM; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE;

EID: 79954531233     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018617     Document Type: Article

References (46)

1. DeLeo FR, Otto M, Kreiswirth BN, Chambers HF, (2010) Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375: 1557-1568.
2. Chambers HF, DeLeo FR, (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7: 2464-2474.
3. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, et al. (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298: 1763-1771.
4. Laupland KB, Ross T, Gregson DB, (2008) Staphylococcus aureus bloodstream infections: risk factors, outcomes, and the influence of methicillin resistance in Calgary, Canada, 2000-2006. J Infect Dis 198: 336-343.
5. Seybold U, Kourbatova EV, Johnson JG, Halvosa SJ, Wang YF, et al. (2006) Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health care-associated blood stream infections. Clin Infect Dis 42: 647-656.
6. Kempker RR, Farley MM, Ladson JL, Satola S, Ray SM, (2010) Association of methicillin-resistant Staphylococcus aureus (MRSA) USA300 genotype with mortality in MRSA Bacteremia. J Infect 61: 372-381.
7. Jenkins TC, McCollister BD, Sharma R, McFann KK, Madinger NE, et al. (2009) Epidemiology of healthcare-associated bloodstream infection caused by USA300 strains of methicillin-resistant Staphylococcus aureus in 3 affiliated hospitals. Infect Control Hosp Epidemiol 30: 233-241.
8. Kobayashi SD, Braughton KR, Palazzolo-Ballance AM, Kennedy AD, Sampaio E, et al. (2010) Rapid neutrophil destruction following phagocytosis of Staphylococcus aureus. J Innate Immun 2: 560-575.
9. Voyich JM, Braughton KR, Sturdevant DE, Whitney AR, Said-Salim B, et al. (2005) Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J Immunol 175: 3907-3919.
10. Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, et al. (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906-909.
11. Skaar EP, Schneewind O, (2004) Iron-regulated surface determinants (Isd) of Staphylococcus aureus: stealing iron from heme. Microbes Infect 6: 390-397.
12. Sebulsky MT, Hohnstein D, Hunter MD, Heinrichs DE, (2000) Identification and characterization of a membrane permease involved in iron-hydroxamate transport in Staphylococcus aureus. J Bacteriol 182: 4394-4400.
13. Sebulsky MT, Shilton BH, Speziali CD, Heinrichs DE, (2003) The role of FhuD2 in iron(III)-hydroxamate transport in Staphylococcus aureus. Demonstration that FhuD2 binds iron(III)-hydroxamates but with minimal conformational change and implication of mutations on transport. J Biol Chem 278: 49890-49900.
14. Sebulsky MT, Heinrichs DE, (2001) Identification and characterization of fhuD1 and fhuD2, two genes involved in iron-hydroxamate uptake in Staphylococcus aureus. J Bacteriol 183: 4994-5000.
15. Dale SE, Sebulsky MT, Heinrichs DE, (2004) Involvement of SirABC in iron-siderophore import in Staphylococcus aureus. J Bacteriol 186: 8356-8362.
16. Heinrichs JH, Gatlin LE, Kunsch C, Choi GH, Hanson MS, (1999) Identification and characterization of SirA, an iron-regulated protein from Staphylococcus aureus. J Bacteriol 181: 1436-1443.
17. Beasley FC, Heinrichs DE, (2010) Siderophore-mediated iron acquisition in the staphylococci. J Inorg Biochem 104: 282-288.
18. Rosso ML, Chauvaux S, Dessein R, Laurans C, Frangeul L, et al. (2008) Growth of Yersinia pseudotuberculosis in human plasma: impacts on virulence and metabolic gene expression. BMC Microbiol 8: 211.
19. Chauvaux S, Rosso ML, Frangeul L, Lacroix C, Labarre L, et al. (2007) Transcriptome analysis of Yersinia pestis in human plasma: an approach for discovering bacterial genes involved in septicaemic plague. Microbiology 153: 3112-3124.
20. Ventura CL, Malachowa N, Hammer CH, Nardone GA, Robinson MA, et al. (2010) Identification of a novel Staphylococcus aureus two-component leukotoxin using cell surface proteomics. PLoS ONE 5: e11634.
21. Palazzolo-Ballance AM, Reniere ML, Braughton KR, Sturdevant DE, Otto M, et al. (2008) Neutrophil microbicides induce a pathogen survival response in community-associated methicillin-resistant Staphylococcus aureus. J Immunol 180: 500-509.
22. Bubeck Wardenburg J, Palazzolo-Ballance AM, Otto M, Schneewind O, DeLeo FR, (2008) Panton-Valentine leukocidin is not a virulence determinant in murine models of community-associated methicillin-resistant Staphylococcus aureus disease. J Infect Dis 198: 1166-1170.
23. Voyich JM, Otto M, Mathema B, Braughton KR, Whitney AR, et al. (2006) Is Panton-Valentine leukocidin the major virulence determinant in community-associated methicillin-resistant Staphylococcus aureus disease? J Infect Dis 194: 1761-1770.
24. Graves SF, Kobayashi SD, Braughton KR, Diep BA, Chambers HF, et al. (2010) Relative contribution of Panton-Valentine leukocidin to PMN plasma membrane permeability and lysis caused by USA300 and USA400 culture supernatants. Microbes Infect 12: 446-456.
25. Graham MR, Virtaneva K, Porcella SF, Barry WT, Gowen BB, et al. (2005) Group A Streptococcus transcriptome dynamics during growth in human blood reveals bacterial adaptive and survival strategies. Am J Pathol 166: 455-465.
26. Mereghetti L, Sitkiewicz I, Green NM, Musser JM, (2008) Extensive adaptive changes occur in the transcriptome of Streptococcus agalactiae (group B streptococcus) in response to incubation with human blood. PLoS ONE 3: e3143.
27. Vebo HC, Snipen L, Nes IF, Brede DA, (2009) The transcriptome of the nosocomial pathogen Enterococcus faecalis V583 reveals adaptive responses to growth in blood. PLoS ONE 4: e7660.
28. Andrews SC, Robinson AK, Rodriguez-Quinones F, (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27: 215-237.
29. Yamazaki K, Kato F, Kamio Y, Kaneko J, (2006) Expression of gamma-hemolysin regulated by sae in Staphylococcus aureus strain Smith 5R. FEMS Microbiol Lett 259: 174-180.
30. Cooney J, Kienle Z, Foster TJ, O'Toole PW, (1993) The gamma-hemolysin locus of Staphylococcus aureus comprises three linked genes, two of which are identical to the genes for the F and S components of leukocidin. Infect Immun 61: 768-771.
31. Rahman A, Izaki K, Kamio Y, (1993) Gamma-hemolysin genes in the same family with lukF and lukS genes in methicillin resistant Staphylococcus aureus. Biosci Biotechnol Biochem 57: 1234-1236.
32. Prevost G, Cribier B, Couppie P, Petiau P, Supersac G, et al. (1995) Panton-Valentine leucocidin and gamma-hemolysin from Staphylococcus aureus ATCC 49775 are encoded by distinct genetic loci and have different biological activities. Infect Immun 63: 4121-4129.
33. Supersac G, Piemont Y, Kubina M, Prevost G, Foster TJ, (1998) Assessment of the role of gamma-toxin in experimental endophthalmitis using a hlg-deficient mutant of Staphylococcus aureus. Microb Pathog 24: 241-251.
34. Siqueira JA, Speeg-Schatz C, Freitas FI, Sahel J, Monteil H, et al. (1997) Channel-forming leucotoxins from Staphylococcus aureus cause severe inflammatory reactions in a rabbit eye model. J Med Microbiol 46: 486-494.
35. Ferreras M, Hoper F, Dalla SM, Colin DA, Prevost G, et al. (1998) The interaction of Staphylococcus aureus bi-component gamma-hemolysins and leucocidins with cells and lipid membranes. Biochim Biophys Acta 1414: 108-126.
36. Skaar EP, Humayun M, Bae T, DeBord KL, Schneewind O, (2004) Iron-source preference of Staphylococcus aureus infections. Science 305: 1626-1628.
37. Dale SE, Doherty-Kirby A, Lajoie G, Heinrichs DE, (2004) Role of siderophore biosynthesis in virulence of Staphylococcus aureus: identification and characterization of genes involved in production of a siderophore. Infect Immun 72: 29-37.
38. Torres VJ, Attia AS, Mason WJ, Hood MI, Corbin BD, et al. (2010) Staphylococcus aureus fur regulates the expression of virulence factors that contribute to the pathogenesis of pneumonia. Infect Immun 78: 1618-1628.
39. Wang R, Braughton KR, Kretschmer D, Bach TH, Queck SY, et al. (2007) Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat Med 13: 1510-1514.
40. Bae T, Schneewind O, (2006) Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55: 58-63.
41. Diep BA, Stone GG, Basuino L, Graber CJ, Miller A, et al. (2008) The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J Infect Dis 197: 1523-1530.
42. Diep BA, Palazzolo-Ballance AM, Tattevin P, Basuino L, Braughton KR, et al. (2008) Contribution of Panton-Valentine leukocidin in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. PLoS ONE 3: e3198.
43. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Statist Soc B 57: 289-300.
44. Kobayashi SD, Voyich JM, Buhl CL, Stahl RM, DeLeo FR, (2002) Global changes in gene expression by human polymorphonuclear leukocytes during receptor-mediated phagocytosis: Cell fate is regulated at the level of gene expression. Proc Natl Acad Sci USA 99: 6901-6906.
45. Kennedy AD, Bubeck WJ, Gardner DJ, Long D, Whitney AR, et al. (2010) Targeting of alpha-hemolysin by active or passive immunization decreases severity of USA300 skin infection in a mouse model. J Infect Dis 202: 1050-1058.
46. Bunce C, Wheeler L, Reed G, Musser J, Barg N, (1992) Murine model of cutaneous infection with gram-positive cocci. Infect Immun 60: 2636-2640.