The Staphylococcus aureus response to unsaturated long chain free fatty acids: Survival mechanisms and virulence implications

PLoS ONE

Volumn 4, Issue 2, 2009, Pages

  Kenny, John G ^a   Ward, Deborah ^a   Josefsson, Elisabet ^b   Jonsson, Ing Marie ^b   Hinds, Jason ^c   Rees, Huw H ^a   Lindsay, Jodi A ^c   Tarkowski, Andrej ^b   Horsburgh, Malcolm J ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AEROBIC RESPIRATION CONTROL PROTEIN A; BACTERIAL RNA; LINOLEIC ACID; LONG CHAIN FATTY ACID; OLIGONUCLEOTIDE; PEPTIDOGLYCAN; PROTEIN AGR; PROTEIN CRTM; PROTEIN SASA; PROTEIN SASF; PROTEIN SIGB; PROTEIN VRAE; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC SENSITIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL ENERGY; CELL SURFACE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION AND TRANSLATION; HYDROPHOBICITY; MEMBRANE STABILIZATION; MICROARRAY ANALYSIS; NONHUMAN; PATHOGENESIS; PROTEIN FUNCTION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REGULON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEPSIS; STAPHYLOCOCCUS AUREUS; TRANSPOSON; UPREGULATION;

ARCA; BACTERIA (MICROORGANISMS); MURINAE; STAPHYLOCOCCUS AUREUS;

EID: 84887212397     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004344     Document Type: Article

References (92)

1. Rippke F, Schreiner V, Doering T, Maibach HI (2004) Stratum corneum pH in atopic dermatitis: impact on skin barrier function and colonization with Staphylococcus aureus. Am J Clin Dermatol 5: 217-223.
2. Schäfer L, Kragballe K (1991) Abnormalities in epidermal lipid metabolism in patients with atopic dermatitis. J Invest Dermatol 96: 10-15.
3. Takigawa H, Nakagawa H, Kuzukawa M, Mori H, Imokawa G (2005) Deficient production of hexadecenoic acid in the skin is associated in part with the vulnerability of atopic dermatitis patients to colonization by Staphylococcus aureus. Dermatology 211: 240-248.
4. Ansari MN, Nicolaides N, Fu HC (1970) Fatty acid composition of the living layer and stratum corneum lipids of human sole skin epidermis. Lipids 5: 838-845.
5. Drake DR, Brogden KA, Dawson DV, Wertz PW (2008) Thematic review series: skin lipids. Antimicrobial lipids at the skin surface. J Lipid Res 49: 4-11.
6. Pappas A, Anthonavage M, Gordon JS (2002) Metabolic fate and selective utilization of major fatty acids in human sebaceous gland. J Invest Dermatol 118: 164-171.
7. Do TQ, Moshkani S, Castillo P, Anunta S, Pogosyan A, et al. (2008) Lipids including cholesteryl linoleate and cholesteryl arachidonate contribute to the inherent antibacterial activity of human nasal fluid. J Immunol 181: 4177-4187.
8. Dye ES, Kapral FA (1981) Characterization of a bactericidal lipid developing within staphylococcal abscesses. Infect Immun 32: 98-104.
9. Engler HD, Kapral FA (1992) The production of a bactericidal monoglyceride in staphylococcal abscesses. J Med Microbiol 37: 238-244.
10. Shryock TR, Kapral FA (1992) The production of bactericidal fatty acids from glycerides in staphylococcal abscesses. J Med Microbiol 36: 288-92.
11. Bergsson G, Arnfinnsson J, Steingrímsson O, Thormar H (2001) Killing of Gram-positive cocci by fatty acids and monoglycerides. APMIS 109: 670-678.
12. Galbraith H, Miller TB (1973) Effect of long chain fatty acids on bacterial respiration and amino acid uptake. J Appl Bacteriol 36: 659-675.
13. Heczko PB, Lütticken R, Hryniewicz W, Neugebauer M, Pulverer G (1979) Susceptibility of Staphylococcus aureus and group A, B, C, and G streptococci to free fatty acids. J Clin Microbiol 9: 333-335.
14. Kabara JJ, Swieczkowski DM, Conley AJ, Truant JP (1972) Fatty acids and derivatives as antimicrobial agents. Antimicrob Agents Chemother 2: 23-28.
15. Kelsey JA, Bayles KW, Shafii B, McGuire MA (2006) Fatty acids and monoacylglycerols inhibit growth of Staphylococcus aureus. Lipids 41: 951-961.
16. Knapp HR, Melly MA (1986) Bactericidal effects of polyunsaturated fatty acids. J Infect Dis 154: 84-94.
17. Nieman C (1954) Influence of trace amounts of fatty acids on the growth of microorganisms. Bacteriol Rev 18: 147-161.
18. Speert DP, Wannamaker LW, Gray ED, Clawson CC (1979) Bactericidal effect of oleic acid on group A streptococci: mechanism of action. Infect Immun 26: 1202-1210.
19. Hilmarsson H, Traustason BS, Kristmundsdóttir T, Thormar H (2007) Virucidal activities of medium- and long-chain fatty alcohols and lipids against respiratory syncytial virus and parainfluenza virus type 2: comparison at different pH levels. Arch Virol 152: 2225-2236.
20. Hilmarsson H, Larusson LV, Thormar H (2006) Virucidal effect of lipids on visna virus, a lentivirus related to HIV. Arch Virol 151: 1217-1224.
21. Thormar H, Isaacs CE, Brown HR, Barshatzky MR, Pessolano T (1987) Inactivation of enveloped viruses and killing of cells by fatty acids and monoglycerides. Antimicrob Agents Chemother 31: 27-31.
22. Greenway DL, Dyke KG (1979) Mechanism of the inhibitory action of linoleic acid on the growth of Staphylococcus aureus. J Gen Microbiol 115: 233-245.
23. Zheng CJ, Yoo JS, Lee TG, Cho HY, Kim YH, et al. (2005) Fatty acid synthesis is a target for antibacterial activity of unsaturated fatty acids. FEBS Lett 579: 5157-5162.
24. Won SR, Hong MJ, Kim YM, Li CY, Kim JW, et al. (2007) Oleic acid: an efficient inhibitor of glucosyltransferase. FEBS Lett 581: 4999-5002.
25. Campbell IM, Crozier DN, Pawagi AB, Buivids IA (1983) In vitro response of Staphylococcus aureus from cystic fibrosis patients to combinations of linoleic and oleic acids added to nutrient medium. J Clin Microbiol 18: 408-415.
26. Chamberlain NR, Mehrtens BG, Xiong Z, Kapral FA, Boardman JL, et al. (1991) Correlation of carotenoid production, decreased membrane fluidity, and resistance to oleic acid killing in Staphylococcus aureus 18Z. Infect Immun 59: 4332-4337.
27. Grinsted J, Lacey RW (1973) Ecological and genetic implications of pigmentation in Staphylococcus aureus. J Gen Microbiol 75: 259-267.
28. Xiong Z, Kapral FA (1992) Carotenoid pigment levels in Staphylococcus aureus and sensitivity to oleic acid. J Med Microbiol 37: 192-194.
29. Chamberlain NR, Imanoel B (1996) Genetic regulation of fatty acid modifying enzyme from Staphylococcus aureus. J Med Microbiol 44: 125-129.
30. Kapral FA, Smith S, Lal D (1992) The esterification of fatty acids by Staphylococcus aureus fatty acid modifying enzyme (FAME) and its inhibition by glycerides. J Med Microbiol 37: 235-237.
31. Long JP, Hart J, Albers W, Kapral FA (1992) The production of fatty acid modifying enzyme (FAME) and lipase by various staphylococcal species. J Med Microbiol 37: 232-234.
32. Mortensen JE, Shryock TR, Kapral FA (1992) Modification of bactericidal fatty acids by an enzyme of Staphylococcus aureus. J Med Microbiol 36: 293-298.
33. Lee EH, Shafer WM (1999) The farAB-encoded efflux pump mediates resistance of gonococci to long-chained antibacterial fatty acids. Mol Microbiol 33: 839-845.
34. Clarke SR, Mohamed R, Bian L, Routh AF, Kokai-Kun JF, et al. (2007) The Staphylococcus aureus surface protein IsdA mediates resistance to innate defenses of human skin. Cell Host Microbe 1: 199-212.
35. Projan SJ, Brown-Skrobot S, Schlievert PM, Vandenesch F, Novick RP (1994) Glycerol monolaurate inhibits the production of beta-lactamase, toxic shock toxin-1, and other staphylococcal exoproteins by interfering with signal transduction. J Bacteriol 176: 4204-4209.
36. Ruzin A, Novick RP (2000) Equivalence of lauric acid and glycerol monolaurate as inhibitors of signal transduction in Staphylococcus aureus. J Bacteriol 182: 2668-2671.
37. Schlievert PM, Deringer JR, Kim MH, Projan SJ, Novick RP (1992) Effect of glycerol monolaurate on bacterial growth and toxin production. Antimicrob Agents Chemother 36: 626-631.
38. Peterson ML, Schlievert PM (2006) Glycerol monolaurate inhibits the effects of Gram-positive select agents on eukaryotic cells. Biochemistry 45: 2387-2397.
39. Ruzin A, Novick RP (1998) Glycerol monolaurate inhibits induction of vancomycin resistance in Enterococcus faecalis. J Bacteriol 180: 182-185.
40. Vetter SM, Schlievert PM (2005) Glycerol monolaurate inhibits virulence factor production in Bacillus anthracis. Antimicrob Agents Chemother 49: 1302-1305.
41. Burts ML, Williams WA, DeBord K, Missiakas DM (2005) EsxA and EsxB are secreted by an ESAT-6-like system that is required for the pathogenesis of Staphylococcus aureus infections. Proc Natl Acad Sci USA 102: 1169-1174.
42. McCallum N, Bischoff M, Maki H, Wada A, Berger-Bächi B (2004) TcaR, a putative MarR-like regulator of sarS expression. J Bacteriol 186: 2966-2972.
43. Bentley R, Meganathan R (1982) Biosynthesis of vitamin K (menaquinone) in bacteria. Microbiol Rev 46: 241-280.
44. Foster SJ (1995) Molecular characterization and functional analysis of the major autolysin of Staphylococcus aureus 8325/4. J Bacteriol 177: 5723-5725.
45. Brunskill EW, Bayles KW (1996) Identification and molecular characterization of a putative regulatory locus that affects autolysis in Staphylococcus aureus. J Bacteriol 178: 611-618.
46. Rice KC, Mann EE, Endres JL, Weiss EC, Cassat JE, et al. (2007) The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc Natl Acad Sci USA 104: 8113-8118.
47. Qoronfleh MW, Gustafson JE, Wilkinson BJ (1998) Conditions that induce Staphylococcus aureus heat shock proteins also inhibit autolysis. FEMS Microbiol Lett 166: 103-107.
48. Dufour M, Manson JM, Bremer PJ, Dufour JP, Cook GM, et al. (2007) Characterization of monolaurin resistance in Enterococcus faecalis. Appl Environ Microbiol. 73: 5507-5515.
49. Collins LV, Kristian SA, Weidenmaier C, Faigle M, Van Kessel KP, et al. (2002) Staphylococcus aureus strains lacking D-alanine modifications of teichoic acids are highly susceptible to human neutrophil killing and are virulence attenuated in mice. J Infect Dis 186: 214-219.
50. Peschel A, Jack RW, Otto M, Collins LV, Staubitz P, et al. (2001) Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with 1-lysine. J Exp Med 193: 1067-1076.
51. Weidenmaier C, Peschel A, Kempf VA, Lucindo N, Yeaman MR, et al. (2005) DltABCD- and MprF-mediated cell envelope modifications of Staphylococcus aureus confer resistance to platelet microbicidal proteins and contribute to virulence in a rabbit endocarditis model. Infect Immun 73: 8033-8038.
52. Holden MT, Feil EJ, Lindsay JA, Peacock SJ, Day NP, 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 U S A. 101: 9786-9791.
53. Chamberlain NR, Brueggemann SA (1997) Characterisation and expression of fatty acid modifying enzyme produced by Staphylococcus epidermidis. J Med Microbiol 46: 693-697.
54. Johnson AP, Pearson A, Duckworth G (2005) Surveillance and epidemiology of MRSA bacteraemia in the UK. J Antimicrob Chemother 56: 455-462.
55. Johnson AP, Aucken HM, Cavendish S, Ganner M, Wale MC, et al. (2001) Dominance of EMRSA-15 and -16 among MRSA causing nosocomial bacteraemia in the UK: analysis of isolates from the European Antimicrobial Resistance Surveillance System (EARSS). J Antimicrob Chemother 48: 143-144.
56. Goering RV, McDougal LK, Fosheim GE, Bonnstetter KK, Wolter DJ, et al. (2007) Epidemiologic distribution of the arginine catabolic mobile element among selected methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates. J Clin Microbiol 45: 1981-1984.
57. Roche FM, Massey R, Peacock SJ, Day NP, Visai L, et al. (2003) Characterization of novel LPXTG-containing proteins of Staphylococcus aureus identified from genome sequences. Microbiology 149: 643-654.
58. Oscarsson J, Kanth A, Tegmark-Wisell K, Arvidson S (2006) SarA is a repressor of hla (alpha-hemolysin) transcription in Staphylococcus aureus: its apparent role as an activator of hla in the prototype strain NCTC8325 depends on reduced expression of sarS. J Bacteriol 188: 8526-8533.
59. Kuroda M, Kuroda H, Oshima T, Takeuchi F, Mori H, et al. (2003) Two-component system VraSR positively modulates the regulation of cell-wall biosynthesis pathway in Staphylococcus aureus. Mol Microbiol 49: 807-821.
60. Neoh HM, Cui L, Yuzawa H, Takeuchi F, Matsuo M, et al. (2008) Mutated response regulator graR is responsible for phenotypic conversion of Staphylococcus aureus from heterogeneous vancomycin-intermediate resistance to vancomycin-intermediate resistance. Antimicrob Agents Chemother 52: 45-53.
61. De Lencastre H, Wu SW, Pinho MG, Ludovice AM, Filipe S, et al. (1999) Antibiotic resistance as a stress response: complete sequencing of a large number of chromosomal loci in Staphylococcus aureus strain COL that impact on the expression of resistance to methicillin. Microb Drug Resist 5: 163-175.
62. Sass V, Pag U, Tossi A, Bierbaum G, Sahl HG (2008) Mode of action of human beta-defensin 3 against Staphylococcus aureus and transcriptional analysis of responses to defensin challenge. Int J Med Microbiol 298: 619-633.
63. Tekaia F, Gordon SV, Garnier T, Brosch R, Barrell BG, et al. (1999) Analysis of the proteome of Mycobacterium tuberculosis in silico. Tuber Lung Dis 79: 329-342.
64. Wydro P, Krajewska B, Hac-Wydro K (2007) Chitosan as a lipid binder: a langmuir monolayer study of chitosan-lipid interactions. Biomacromolecules 8: 2611-2617.
65. Freiberg C, Fischer HP, Brunner NA (2005) Discovering the mechanism of action of novel antibacterial agents through transcriptional profiling of conditional mutants. Antimicrob Agents Chemother 49: 749-759.
66. Hutter B, Schaab C, Albrecht S, Borgmann M, Brunner NA, et al. (2004) Prediction of mechanisms of action of antibacterial compounds by gene expression profiling. Antimicrob Agents Chemother 48: 2838-2844.
67. Riordan JT, O'Leary JO, Gustafson JE (2006) Contributions of sigB and sarA to distinct multiple antimicrobial resistance mechanisms of Staphylococcus aureus. Int J Antimicrob Agents 28: 54-61.
68. Seggewiss J, Becker K, Kotte O, Eisenacher M, Yazdi MR, et al. (2006) Reporter metabolite analysis of transcriptional profiles of a Staphylococcus aureus strain with normal phenotype and its isogenic hemB mutant displaying the small-colony-variant phenotype. J Bacteriol 188: 7765-7777.
69. Camilli A, Portnoy A, Youngman P (1990) Insertional mutagenesis of Listeria monocytogenes with a novel Tn917 derivative that allows direct cloning of DNA flanking transposon insertions. J Bacteriol 172: 3738-3744.
70. Novick RP (1991) Genetic systems in staphylococci. Methods Enzymol 204: 587-636.
71. Begun J, Sifri CD, Goldman S, Calderwood SB, Ausubel FM (2005) Staphylococcus aureus virulence factors identified by using a high-throughput Caenorhabditis elegans-killing model. Infect Immun 73: 872-877.
72. Horsburgh MJ, Wiltshire MD, Crossley H, Ingham E, Foster SJ (2004) PheP, a putative amino acid permease of Staphylococcus aureus, contributes to survival in vivo and during starvation. Infect Immun 72: 3073-3076.
73. Guerot-Fleury AM, Shazand K, Frandsen N, Stragier P (1995) Antibiotic resistance cassettes for Bacillus subtilis. Gene 167: 335-336.
74. Schenk S, Ladagga RA (1992) Improved methods for electroporation of Staphylococcus aureus. FEMS Microbiol Lett 94: 133-138.
75. Grkovic S, Brown MH, Hardie KM, Firth N, Skurray RA (2003) Stable low-copy-number Staphylococcus aureus shuttle vectors. Microbiol 149: 785-794.
76. Witney AA, Marsden GL, Holden MTG, Stabler RA, Husain SE, et al. (2005) Design, validation and application of a seven strain Staphylococcus aureus microarray for comparative genomics. Appl Environ Microbiol 71: 7504-7514.
77. Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate: a Practical and Powerful Approach to Multiple Testing. J Royal Statistical Society 57: 289-300.
78. Yan J, Wait R, Berkelman T, Harry R, Westbrook J, et al. (2000) A modified silver staining protocol for visualization of proteins compatible with matrix-assisted laser desorption/ionization and electrospray ionization-mass spectrometry. Electrophoresis 21: 3666-3672.
79. Neuhoff V, Arold N, Taube D, Ehrhardt W (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9: 255-262.
80. Pappin DJ, Hojrup P, Bleasby AJ (1993) Rapid identification of proteins by peptide-mass fingerprinting. Curr Biol 3: 327-332.
81. Banner MA, Cunniffe JG, Macintosh RL, Foster TJ, Rohde H, et al. (2007) Localised tufts of fibrils on Staphylococcus epidermidis NCTC 11047 are comprised of the accumulation-associated protein. J Bacteriol 189: 2793-2804.
82. Blackman SA, Smith TJ, Foster SJ (1998) The role of autolysins during vegetative growth of Bacillus subtilis 168. Microbiology 144: 73-82.
83. Bremell T, Lange S, Yacoub A, Ryden C, Tarkowski A (1991) Experimental Staphylococcus aureus arthritis in mice. Infect Immun 59: 2615-2623.
84. Josefsson E, Kubica M, Mydel P, Potempa J, Tarkowski A (2008) In vivo sortase A and clumping factor A mRNA expression during Staphylococcus aureus infection. Microb Pathog 44: 103-110.
85. Sakiniene E, Bremell T, Tarkowski A (1996) Addition of corticosteroids to antibiotic treatment ameliorates the course of experimental Staphylococcus aureus arthritis. Arth Rheum 39: 1596-1605.
86. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor, N.Y.: Cold Spring Laboratory Press.
87. Horsburgh MJ, Aish JL, White IJ, Shaw L, Lithgow JK, et al. (2002) SigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J Bacteriol 184: 5457-5467.
88. Novick RP (1967) Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology 33: 155-166.
89. Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H, et al. (2001) Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet 357: 1225-1240.
90. Frees D, Chastanet A, Qazi S, Sorensen K, Hill P, et al. (2004) C1p ATPases are required for stress tolerance, intracellular replication and biofilm formation in Staphylococcus aureus. Mol Microbiol 54: 1445-1462.
91. Clauditz A, Resch A, Wieland KP, Peschel A, Götz F (2006) Staphyloxanthin plays a role in the fitness of Staphylococcus aureus and its ability to cope with oxidative stress. Infect Immun 74: 4950-4953.
92. Chan PF, Foster SJ, Ingham E, Clements MO (1998) The Staphylococcus aureus alternative sigma factor óB controls the environmental stress response but not starvation survival or pathogenicity in a mouse abscess model. J Bacteriol 180: 6082-6089.