Bactericidal activity of the human skin fatty acid cis-6-hexadecanoic acid on Staphylococcus aureus

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 7, 2014, Pages 3599-3609

  Cartron, Michaël L ^a   England, Simon R ^a   Chiriac, Alina Iulia ^b   Josten, Michaele ^b   Turner, Robert ^a   Rauter, Yvonne ^a,c   Hurd, Alexander ^a   Sahl, Hans Georg ^b   Jones, Simon ^a   Foster, Simon J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF BONN   (Germany)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CIS FATTY ACID; PALMITIC ACID; ADENOSINE TRIPHOSPHATE; LIPOSOME;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERICIDAL ACTIVITY; COMMENSAL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ECOLOGY; ELECTRON TRANSPORT; HUMAN; MEMBRANE FLUIDITY; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTON MOTIVE FORCE; SKIN FLORA; SKIN PROTECTION; STAPHYLOCOCCUS AUREUS; ANTAGONISTS AND INHIBITORS; CELL MEMBRANE PERMEABILITY; CHEMISTRY; DRUG EFFECTS; MEMBRANE POTENTIAL; METABOLISM; MICROBIAL SENSITIVITY TEST; POLYMERIZATION; SKIN;

ADENOSINE TRIPHOSPHATE; CELL MEMBRANE PERMEABILITY; DRUG RESISTANCE, BACTERIAL; ELECTRON TRANSPORT; HUMANS; LIPOSOMES; MEMBRANE FLUIDITY; MEMBRANE POTENTIALS; MICROBIAL SENSITIVITY TESTS; PALMITIC ACID; POLYMERIZATION; SKIN; STAPHYLOCOCCUS AUREUS;

EID: 84903121577     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01043-13     Document Type: Article

References (53)

1. Ong PY, Ohtake T, Brandt C, Strickland I, Boguniewicz M, Ganz T, Gallo RL, Leung DY. 2002. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N. Engl. J. Med. 347:1151-1160. http://dx.doi.org/10.1056/ NEJMoa021481.
2. Niyonsaba F, Ogawa H. 2005. Protective roles of the skin against infection: implication of naturally occurring human antimicrobial agents beta-defensins, cathelicidin LL-37 and lysozyme. J. Dermatol. Sci. 40:157-168. http://dx.doi.org/10.1016/j.jdermsci.2005.07.009. (Pubitemid 41728963)
3. Wille JJ, Kydonieus A. 2003. Palmitoleic acid isomer (C16:1delta6) in human skin sebum is effective against Gram-positive bacteria. Skin Pharmacol. Appl. Skin Physiol. 16:176-187. http://dx.doi.org/10.1159/000069757. (Pubitemid 36407893)
4. Korting HC, Lukacs A, Braun-Falco O. 1988. Microbial flora and odor of the healthy human skin. Hautarzt 39:564-568. (In German.)
5. Kluytmans JA, Wertheim HF. 2005. Nasal carriage of Staphylococcus aureus and prevention of nosocomial infections. Infection 33:3-8. http://dx.doi.org/10. 1007/s15010-005-4012-9. (Pubitemid 40585492)
6. Miller SJ, Aly R, Shinefeld HR, Elias PM. 1988. In vitro and in vivo antistaphylococcal activity of human stratum corneum lipids. Arch. Dermatol. 124:209-215. (Pubitemid 18054501)
7. 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. http://dx.doi.org/10.1159/000087018. (Pubitemid 41415864)
8. Georgel P, Crozat K, Lauth X, Makrantonaki E, Seltmann H, Sovath S, Hoebe K, Du X, Rutschmann S, Jiang Z, Bigby T, Nizet V, Zouboulis CC, Beutler B. 2005. A toll-like receptor 2-responsive lipid effector pathway protects mammals against skin infections with Gram-positive bacteria. Infect. Immun. 73:4512-4521. http://dx.doi.org/10.1128/IAI.73.8.4512-4521.2005. (Pubitemid 41105605)
9. Clarke SR, Mohamed R, Bian L, Routh AF, Kokai-Kun JF, Mond JJ, Tarkowski A, Foster SJ. 2007. The Staphylococcus aureus surface protein IsdA mediates resistance to innate defenses of human skin. Cell Host Microbe 1:199-212. http://dx.doi.org/10.1016/j.chom.2007.04.005. (Pubitemid 46706363)
10. Dye ES, Kapral FA. 1981. Characterization of a bactericidal lipid developing within staphylococcal abscesses. Infect. Immun. 32:98-104. (Pubitemid 11156909)
11. Kohler T, Weidenmaier C, Peschel A. 2009. Wall teichoic acid protects Staphylococcus aureus against antimicrobial fatty acids from human skin. J. Bacteriol. 191:4482-4484. http://dx.doi.org/10.1128/JB.00221-09.
12. 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. http://dx.doi.org/10.1099/00221287-115-1-233. (Pubitemid 10200272)
13. Galbraith H, Miller TB. 1973. Effect of long-chain fatty acids on bacterial respiration and amino acid uptake. J. Appl. Bacteriol. 36:659-675. http://dx.doi.org/10.1111/j.1365-2672.1973.tb04151.x.
14. Greenway DL, Dyke KG. 1980. Isolation and properties of a linoleic acid-resistant mutant of Staphylococcus aureus. J. Gen. Microbiol. 118: 267-270. (Pubitemid 10013788)
15. Memon RA, Staprans I, Noor M, Holleran WM, Uchida Y, Moser AH, Feingold KR, Grunfeld C. 2000. Infection and inflammation induce LDL oxidation in vivo. Arterioscler. Thromb. Vasc. Biol. 20:1536-1542. http://dx.doi.org/10.1161/01. ATV.20.6.1536. (Pubitemid 30353885)
16. Klomsiri C, Panmanee W, Dharmsthiti S, Vattanaviboon P, Mongkolsuk S. 2005. Novel roles of ohrR-ohr in Xanthomonas sensing, metabolism, and physiological adaptive response to lipid hydroperoxide. J. Bacteriol. 187: 3277-3281. http://dx.doi.org/10.1128/JB.187.9.3277-3281.2005. (Pubitemid 40571623)
17. Hussain M, Hastings JG, White PJ. 1991. A chemically defined medium for slime production by coagulase-negative staphylococci. J. Med. Microbiol. 34:143-147. http://dx.doi.org/10.1099/00222615-34-3-143.
18. Ganzle MG, Vogel RF. 2003. Studies on the mode of action of reutericyclin. Appl. Environ. Microbiol. 69:1305-1307. http://dx.doi.org/10. 1128/AEM.69.2.1305-1307.2003. (Pubitemid 36204868)
19. Schneider T, Senn MM, Berger-Bachi B, Tossi A, Sahl HG, Wiedemann I. 2004. In vitro assembly of a complete, pentaglycine interpeptide bridge containing cell wall precursor (lipid II-Gly5) of Staphylococcus aureus. Mol. Microbiol. 53:675-685. http://dx.doi.org/10.1111/j.1365-2958.2004.04149.x. (Pubitemid 38998184)
20. Rick PD, Hubbard GL, Kitaoka M, Nagaki H, Kinoshita T, Dowd S, Simplaceanu V, Ho C. 1998. Characterization of the lipid-carrier involved in the synthesis of enterobacterial common antigen (ECA) and identification of a novel phosphoglyceride in a mutant of Salmonella Typhimurium defective in ECA synthesis. Glycobiology 8:557-567. http://dx.doi.org/10.1093/glycob/8.6.557. (Pubitemid 28270577)
21. Martinez B, Bottiger T, Schneider T, Rodriguez A, Sahl HG, Wiedemann I. 2008. Specific interaction of the unmodified bacteriocin Lactococcin 972 with the cell wall precursor lipid II. Appl. Environ. Microbiol. 74:4666-4670. http://dx.doi.org/10.1128/AEM.00092-08.
22. Kohlrausch U, Holtje JV. 1991. One-step purification procedure for UDP-N-acetylmuramyl-peptide murein precursors from Bacillus cereus. FEMS Microbiol. Lett. 62:253-257.
23. Raafat D, von Bargen K, Haas A, Sahl HG. 2008. Insights into the mode of action of chitosan as an antibacterial compound. Appl. Environ. Microbiol. 74:3764-3773. http://dx.doi.org/10.1128/AEM.00453-08. (Pubitemid 351874908)
24. Breeuwer P, Drocourt J, Rombouts FM, Abee T. 1996. A novel method for continuous determination of the intracellular pH in bacteria with the internally conjugated fluorescent probe 5 (and 6-)-carboxyfluorescein succinimidyl ester. Appl. Environ. Microbiol. 62:178-183.
25. Bayer AS, Prasad R, Chandra J, Koul A, Smriti M, Varma A, Skurray RA, Firth N, Brown MH, Koo SP, Yeaman MR. 2000. In vitro resistance of Staphylococcus aureus to thrombin-induced platelet microbicidal protein is associated with alterations in cytoplasmic membrane fluidity. Infect. Immun. 68:3548-3553. http://dx.doi.org/10.1128/IAI.68.6.3548-3553.2000. (Pubitemid 30340456)
26. Camargo IL, Neoh HM, Cui L, Hiramatsu K. 2008. Serial daptomycin selection generates daptomycin-nonsusceptible Staphylococcus aureus strains with a heterogeneous vancomycin-intermediate phenotype. Antimicrob. Agents Chemother. 52:4289-4299. http://dx.doi.org/10.1128/AAC.00417-08.
27. Mishra NN, Yang SJ, Sawa A, Rubio A, Nast CC, Yeaman MR, Bayer AS. 2009. Analysis of cell membrane characteristics of in vitro-selected daptomycin-resistant strains of methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 53:2312-2318. http://dx.doi.org/10.1128/AAC.01682- 08.
28. Smith JJ, McFeters GA. 1997. Mechanisms of INT (2-(4-iodophenyl)-3-(4- nitrophenyl)-5-phenyl tetrazolium chloride), and CTC (5-cyano-2,3-ditolyl tetrazolium chloride) reduction in Escherichia coli K-12. J. Microbiol. Methods 29:161-175. http://dx.doi.org/10.1016/S0167-7012(97)00036-5. (Pubitemid 27374973)
29. Burstein C, Tiankova L, Kepes A. 1979. Respiratory control in Escherichia coli K-12. Eur. J. Biochem. 94:387-392. http://dx.doi.org/10.1111/j.1432-1033. 1979.tb12905.x.
30. Bonelli RR, Schneider T, Sahl HG, Wiedemann I. 2006. Insights into in vivo activities of lantibiotics from gallidermin and epidermin mode-of-action studies. Antimicrob. Agents Chemother. 50:1449-1457. http://dx.doi.org/10.1128/ AAC.50.4.1449-1457.2006.
31. Fu Y, Weng Y, Hong WX, Zhang Q. 2010. Efficient synthesis of unsaturated 1-monoacyl glycerols for in meso crystallization of membrane proteins. Synlett 2011:809-812. http://dx.doi.org/10.1055/s-0030-1259912.
32. Watson SP, Clements MO, Foster SJ. 1998. Characterization of the starvation-survival response of Staphylococcus aureus. J. Bacteriol. 180: 1750-1758. (Pubitemid 28173053)
33. Turner RD, Ratcliffe EC, Wheeler R, Golestanian R, Hobbs JK, Foster SJ. 2010. Peptidoglycan architecture can specify division planes in Staphylococcus aureus. Nat. Commun. 1:26. http://dx.doi.org/10.1038/ncomms1025.
34. Levin J, Maibach H. 2008. Human skin buffering capacity: an overview. Skin Res. Technol. 14:121-126. http://dx.doi.org/10.1111/j.1600-0846.2007.00271. x. (Pubitemid 351560369)
35. Schonfeld P, Gerke S, Bohnensack R, Wojtczak L. 2003. Stimulation of potassium cycling in mitochondria by long-chain fatty acids. Biochim. Biophys. Acta 1604: 125-133. http://dx.doi.org/10.1016/S0005-2728(03)00043-4. (Pubitemid 36588697)
36. Bierbaum G, Sahl HG. 2009. Lantibiotics: mode of action, biosynthesis and bioengineering. Curr. Pharm. Biotechnol. 10:2-18. http://dx.doi.org/10.2174/ 138920109787048616.
37. Felle H, Bentrup FW. 1977. A study of the primary effect of the uncoupler carbonyl cyanide m-chlorophenylhydrazone on membrane potential and conductance in Riccia fluitans. Biochim. Biophys. Acta 464:179-187. http://dx.doi.org/10. 1016/0005-2736(77)90380-7.
38. Willett NP, Morse GE. 1966. Long-chain fatty acid inhibition of growth of Streptococcus agalactiae in a chemically defined medium. J. Bacteriol. 91:2245-2250.
39. Butcher GW, King G, Dyke KG. 1976. Sensitivity of Staphylococcus aureus to unsaturated fatty acids. J. Gen. Microbiol. 94:290-296. http://dx.doi.org/10. 1099/00221287-94-2-290.
40. Wojtczak L, Wieckowski MR. 1999. The mechanisms of fatty acid-induced proton permeability of the inner mitochondrial membrane. J. Bioenerg. Biomembr. 31:447-455. http://dx.doi.org/10.1023/A:1005444322823. (Pubitemid 30053958)
41. Kelsey JA, Bayles KW, Shafii B, McGuire MA. 2006. Fatty acids and monoacylglycerols inhibit growth of Staphylococcus aureus. Lipids 41: 951-961. http://dx.doi.org/10.1007/s11745-006-5048-z. (Pubitemid 44871582)
42. Downing DT, Strauss JS. 1974. Synthesis and composition of surface lipids of human skin. J. Investig. Dermatol. 62:228. http://dx.doi.org/10.1111/1523- 1747.ep12676793.
43. James AT, Wheatley VR. 1956. Studies of sebum. 6. The determination of the component fatty acids of human forearm sebum by gas-liquid chromatography. Biochem. J. 63:269-273.
44. Ge L, Gordon JS, Hsuan C, Stenn K, Prouty SM. 2003. Identification of the delta-6 desaturase of human sebaceous glands: expression and enzyme activity. J. Invest. Dermatol. 120:707-714. http://dx.doi.org/10.1046/j.1523-1747.2003. 12123.x. (Pubitemid 36529068)
45. Cirillo VP. 1966. Symposium on bioelectrochemistry of microorganisms. I. Membrane potentials and permeability. Bacteriol. Rev. 30:68-79.
46. + gradient. FEBS Lett. 87:171-179. http://dx.doi.org/10.1016/0014-5793(78)80326-3.
47. + and other cations across phospholipid membranes by nonesterified fatty acids. J. Membr. Biol. 141:21-28.
48. Skulachev VP. 1998. Uncoupling: new approaches to an old problem of bioenergetics. Biochim. Biophys. Acta 1363:100-124. http://dx.doi.org/10.1016/ S0005-2728(97)00091-1. (Pubitemid 28129344)
49. Nicholls DG. 2001. A history of UCP1. Biochem. Soc. Trans. 29:751-755. http://dx.doi.org/10.1042/BST0290751.
50. Schonfeld P, Wojtczak L. 2007. Fatty acids decrease mitochondrial generation of reactive oxygen species at the reverse electron transport but increase it at the forward transport. Biochim. Biophys. Acta 1767: 1032-1040. http://dx.doi.org/10.1016/j.bbabio.2007.04.005. (Pubitemid 47101786)
51. Skulachev VP. 1991. Fatty acid circuit as a physiological mechanism of uncoupling of oxidative phosphorylation. FEBS Lett. 294:158-162. http://dx.doi.org/10.1016/0014-5793(91)80658-P.
52. Di Paola M, Lorusso M. 2006. Interaction of free fatty acids with mitochondria: coupling, uncoupling and permeability transition. Biochim. Biophys. Acta 1757:1330-1337. http://dx.doi.org/10.1016/j.bbabio.2006.03.024. (Pubitemid 44442109)
53. Kenny JG, Ward D, Josefsson E, Jonsson IM, Hinds J, Rees HH, Lindsay JA, Tarkowski A, Horsburgh MJ. 2009. The Staphylococcus aureus response to unsaturated long-chain free fatty acids: survival mechanisms and virulence implications. PLoS One 4:e4344. http://dx.doi.org/10.1371/journal.pone.0004344.