The Staphylococcus aureus Surface Protein IsdA Mediates Resistance to Innate Defenses of Human Skin

Cell Host and Microbe

Volumn 1, Issue 3, 2007, Pages 199-212

  Clarke, Simon R ^a   Mohamed, Ramlan ^a   Bian, Li ^b   Routh, Alexander F ^c   Kokai Kun, John F ^d   Mond, James J ^d   Tarkowski, Andrej ^b   Foster, Simon J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d Biosynexus Incorporated   (United States)

Author keywords

HUMDISEASE; MICROBIO

Indexed keywords

ANTIBIOTIC AGENT; DECANOIC ACID; FATTY ACID; HEMOLYSIN; IRON RESPONSIVE SURFACE DETERMINANT A; LANTIBIOTIC; LAURIC ACID; LINOLEIC ACID; MEMBRANE PROTEIN; MERSACIDIN; NISIN; PALMITOLEIC ACID; PNEUMOLYSIN; PROTEIN A; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; BACTERIUM CARRIER; CONTROLLED STUDY; GRAM POSITIVE BACTERIUM; HOST RESISTANCE; HUMAN; HUMAN TISSUE; HYDROPHOBICITY; INFECTION RESISTANCE; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SEBUM; SKIN INFECTION; STAPHYLOCOCCUS AUREUS;

ADULT; ANTI-BACTERIAL AGENTS; ANTIGENS, BACTERIAL; ANTIMICROBIAL CATIONIC PEPTIDES; COLONY COUNT, MICROBIAL; FATTY ACIDS; HEMOLYSIN PROTEINS; HUMANS; HYDROPHOBICITY; MICROBIAL VIABILITY; SEBUM; SKIN; STAPHYLOCOCCAL SKIN INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

EID: 34248214172     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2007.04.005     Document Type: Article

References (67)

1. Absolom D.R. The role of bacterial hydrophobicity interaction: Bacterial adhesion and phagocytic ingestion. Can. J. Microbiol. 34 (1988) 287-298
2. Baldassarri L., Bertuccini L., Ammendolia M.G., Arciola C.R., and Montanaro L. Effect of iron limitation on slime production by Staphylococcus aureus. Eur. J. Clin. Microbiol. Infect. Dis. 20 (2001) 343-345
3. Bayer A.S., Prasad R., Chadra J., Koul A., Smriti M., Varma A., Skurray R.A., Firth N., Brown M.H., Koo S.P., et al. In vitro resistance of Staphylococcus aureus to thrombin-induced platelet microbicidal protein is associated with alterations in cytoplasmic membrane fluidity. Infect. Immun. 68 (2000) 3548-3553
4. Chamberlain N.R., and Brueggemann S.A. Characterisation and expression of fatty acid modifying enzyme produced by Staphylococcus epidermidis. J. Med. Microbiol. 46 (1997) 693-697
5. Chan-Ick C., and Pyun Y.-R. Nisin biosynthesis and its properties. Biotechnol. Lett. 27 (2005) 1641-1648
6. Chatterjee S., Chatterjee D.K., Jani R.H., Blumbach J., Ganguli B.N., Klesel N., Limbert M., and Seibert G. Mersacidin, a new antibiotic from Bacillus. In vitro and in vivo antibacterial activity. J. Antibiot. 45 (1992) 839-845
7. Clarke S.R., Wiltshire M.D., and Foster S.J. IsdA of Staphylococcus aureus is a broad spectrum iron-regulated adhesin. Mol. Microbiol. 51 (2004) 1509-1519
8. Clarke S.R., and Foster S.J. Surface adhesins of Staphylococcus aureus. Adv. Microb. Physiol. 51 (2006) 187-224
9. Clarke S.R., Brummell K.J., Horsburgh M.J., McDowell P.W., Syed Mohamad S.A., Stapleton M.R., Acevedo J., Read R.C., Day N.P.J., Peacock S.J., et al. Identification of in vivo-expressed antigens of Staphylococcus aureus and their use in vaccinations for protection against nasal carriage. J. Infect. Dis. 193 (2006) 1098-1108
10. Cohn J.R., and Emmett E.A. The excretion of trace metals in human sweat. Ann. Clin. Lab. Sci. 8 (1978) 270-275
11. Croft D.N. Body iron loss and cell loss from epithelia. Proc. R. Soc. Med. 63 (1970) 1221-1224
12. Davies E., Falahee M.B., and Adams M.R. Involvement of the cell envelope of Listeria monocytogenes in the acquisition of nisin resistance. J. Appl. Bacteriol. 81 (1996) 139-146
13. Dye E.S., and Kapral F.A. Survival of Staphylococcus aureus in intraperitoneal abscesses. J. Med. Microbiol. 14 (1981) 185-194
14. Fisher J.P. Soluble substances of human stratum corneum. I. Immunochemical and immunological study. J. Invest. Dermatol. 44 (1965) 43-50
15. Galbraith H., and Miller T.B. Effect of long chain fatty acids on bacterial respiration and amino acid uptake. J. Appl. Bacteriol. 36 (1973) 659-675
16. Georgel P., Crozat K., Lauth X., Makrantonaki E., Seltmann H., Sovath S., Hoebe K., Du X., Rutschmann S., Jiang Z., et al. A toll-like receptor 2-responsive lipid effector pathway protects mammals against skin infections with Gram-positive bacteria. Infect. Immun. 73 (2005) 4512-4521
17. Gilani S.J., Gonzalez M., Hussain I., Finlay A.Y., and Patel G.K. Staphylococcus aureus re-colonization in atopic dermatitis: Beyond the skin. Clin. Exp. Dermatol. 30 (2005) 10-13
18. Götz F. Staphylococcus and biofilms. Mol. Microbiol. 43 (2002) 1367-1378
19. Greenway D.L., and Dyke K.G. Mechanism of the inhibitory action of linoleic acid on the growth of Staphylococcus aureus. J. Gen. Microbiol. 115 (1979) 233-245
20. Greenway D.L., and Dyke K.G. Isolation and properties of a linoleic acid-resistant mutant of Staphylococcus aureus. J. Gen. Microbiol. 118 (1980) 267-270
21. Grigg J.C., Vermeiren C.L., Heinrichs D.E., and Murphy M.E.P. Haem recognition by a Staphylococcus aureus NEAT domain. Mol. Microbiol. 63 (2007) 139-149
22. Hackbarth C.J., and Chambers H.F. blaI and blaR1 regulate β-lactamase and PBP 2′ production in methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 37 (1993) 1144-1149
23. Horsburgh M.J., Ingham E., and Foster S.J. In Staphylococcus aureus, Fur is an interactive regulator with PerR, contributes to virulence, and is necessary for oxidative stress resistance through positive regulation of catalase and iron homeostasis. J. Bacteriol. 183 (2001) 468-475
24. Holland K.T., Taylor D., and Farrell A.M. The effect of glycerol monolaurate on growth of, and production of toxic shock syndrome toxin-1 and lipase by, Staphylococcus aureus. J. Antimicrob. Chemother. 33 (1994) 41-55
25. Jin T., Bokarewa M., Foster T., Mitchell J., Higgins J., and Tarkowski A. Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J. Immunol. 172 (2004) 1169-1176
26. Johnson M., Cockayne A., Williams P.H., and Morrissey J.A. Iron-responsive regulation of biofilm formation in Staphylococcus aureus involves fur-dependent and fur-independent mechanisms. J. Bacteriol. 187 (2005) 8211-8215
27. Klomsiri C., Panmanee W., Dharmsthiti S., Vattanaviboon P., and Mongkolsuk S. Novel roles of ohrR-ohr in Xanthomonas sensing, metabolism and physiological adaptive response to lipid hydroperoxide. J. Bacteriol. 187 (2005) 3277-3281
28. Komatsuzawa H., Ouhara K., Yamada S., Fujiwara T., Sayama K., Hashimoto K., and Sugai M. Innate defences against methicillin-resistant Staphylococcus aureus (MRSA) infection. J. Pathol. 208 (2006) 249-260
29. Kupferwasser L.I., Skurray R.A., Brown M.H., Firth N., Yeaman M.R., and Bayer A.S. Plasmid-mediated resistance to thrombin-induced platelet microbicidal protein in staphylococci: Role of the qacA locus. Antimicrob. Agents Chemother. 43 (1999) 2395-2399
30. Lacey R.W., and Lord V.L. Sensitivity of staphylococci to fatty acids: Novel inactivation of linoleic acid by serum. J. Med. Microbiol. 14 (1981) 41-49
31. Lai Y., Villaruz A.E., Li M., Cha D.J., Sturdevant D.E., and Otto M. The human anionic antimicrobial peptide dermcidin induces proteolytic defence mechanisms in staphylococci. Mol. Microbiol. 63 (2007) 497-506
32. Marchese A., Schito G.C., and Debbia E.A. Emergence of drug-resistant gram-positive pathogenic bacteria. J. Chemother. 12 (2000) 459-462
33. Matsuzaki K. Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim. Biophys. Acta 1462 (1999) 1-10
34. Mazmanian S.K., Liu G., Ton-That H., and Schneewind O. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285 (1999) 760-763
35. Mazmanian S.K., Ton-That H., Su K., and Schneewind O. An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis. Proc. Natl. Acad. Sci. USA 99 (2002) 2293-2298
36. Mazmanian S.K., Skaar E.P., Gasper E.H., Humayun M., Gorniki P., Jelenska J., Joachmiak A., Missiakis D., and Schneewind O. Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299 (2003) 906-909
37. Memon R.A., Staprans I., Noor M., Holleran W.M., Uchida Y., Mosser A.H., Feingold K.R., and Grunfeld C. Infection and inflammation induced LDL oxidation in vivo. Arterioscler. Thromb. Vasc. Biol. 20 (2000) 1536-1542
38. Miller S.J., Aly R., Shinefield H.R., and Elias P.M. Antimicrobial activity of stratum corneum lipids from normal and essential fatty acid-deficient mice. Arch. Dermatol. 124 (1988) 209-215
39. Milstone L.M., Adams B.D., Zhou J., Bruegel Sanchez V.L., and Shofner J. Stratum-specific expression of human transferrin receptor increases iron in mouse epidermis. J. Invest. Dermatol. 126 (2006) 648-652
40. Molin L., and Wester P.O. The estimated daily loss of trace elements from normal skin by desquamation. Scand. J. Clin. Lab. Invest. 36 (1976) 679-682
41. Nakayashiki N. Sweat protein components tested by SDS-polyacrylamide gel electrophoresis followed by immunoblotting. Tohoku J. Exp. Med. 161 (1990) 25-31
42. Niyonsaba F., and Ogawa H. Protective roles of the skin against infection: Implication of naturally occurring human antimicrobial agents β-defensins, cathelicidin LL-37 and lysozyme. J. Dermatol. Sci. 40 (2005) 157-168
43. Nizet V. Antimicrobial peptide resistance mechanisms of human bacterial pathogens. Curr. Issues Mol. Biol. 8 (2006) 11-26
44. Novick R. Properties of cryptic high-frequency transducing phage of Staphylococcus aureus. Virology 33 (1967) 155-166
45. Ong P.Y., Ohtake T., Brandt C., Strickland L., Boguniewics M., Ganz T., Gallo R.L., and Leung D.Y. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N. Engl. J. Med. 347 (2002) 1151-1160
46. Peschel A., Otto M., Jack R.W., Kalbacher H., Jung G., and Götz F. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to definsins, protegrins and other antimicrobial peptides. J. Biol. Chem. 274 (1999) 8405-8410
47. Peschel A., Jack R.W., Otto M., Collins L.V., Staubitz P., Nicholson G., Kalbacher H., Nieuwenhuizen W.F., Jung G., Tarkowski A., et al. 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 L-lysine. J. Exp. Med. 193 (2001) 1067-1076
48. Peschel A. How do bacteria resist human antimicrobial peptides?. Trends Microbiol. 10 (2002) 179-186
49. Peterson M., and Schlievert P.M. Glycerol monolaurate inhibits the effects of gram-positive select agents on eukaryotic cells. Biochemistry 45 (2006) 2387-2397
50. Projan S.J., Brown-Skrobot S., Schlievert P.M., Vandenesch F., and Novick R.P. Glycerol monolaurate inhibits the production of β-lactamase, toxic shock syndrome toxin-1, and other staphylococcal exoproteins by interfering with signal transduction. J. Bacteriol. 176 (1994) 4204-4209
51. Rosenberg M., Gutnick D., and Rosenberg E. Adherence of bacteria to hydrocarbon: A simple method for measuring cell-surface hydrophobicity. FEMS Microbiol. Lett. 9 (1980) 29-34
52. Ruzin A., and Novick R.P. Glycerol monolaurate inhibits induction of vancomycin resistance in Enterococcus faecalis. J. Bacteriol. 180 (1998) 182-185
53. Ruzin A., and Novick R.P. Effect of lauric acid and glycerol monolaurate as inhibitors of signal transduction in Staphylococcus aureus. J. Bacteriol. 182 (2000) 2668-2671
54. Ryan M.A., Akinbi H.T., Serrano A.G., Perez-Gil J., Wu H., McCormack F.X., and Weaver T.E. Antimicrobial activity of native and synthetic surfactant protein B peptides. J. Immunol. 176 (2006) 416-425
55. Schlievert P.M., Deringer J.R., Kim M.H., Projan S.J., and Novick R.P. Effect of glycerol monolaurate on bacterial growth and toxin production. Antimicrob. Agents Chemother. 36 (1992) 626-631
56. Shai Y. From innate immunity to de-novo designed antimicrobial peptides. Curr. Pharm. Des. 8 (2002) 715-725
57. Schaible U.E., and Kaufmann S.H.E. Iron and microbial infection. Nat. Rev. Microbiol. 2 (2004) 946-953
58. Sieprawska-Lupa M., Mydel P., Krawczyk K., Wojcik K., Puklo M., Lupa B., Suder P., Silberring J., Reed M., Pohl J., et al. Degradation of human antimicrobial peptide LL-37 by Staphylococcus aureus-derived proteinases. Antimicrob. Agents Chemother. 48 (2004) 4673-4679
59. Takigawa H., Nakagawa H., Kuzukawa M., Mori H., and Imokawa G. Deficient production of hexadecanoic acid in the skin is associated in part with the vulnerability of atopic dermatitis patients to colonization by Staphylococcus aureus. Dermatology 211 (2005) 240-248
60. Taylor J.M., and Heinrichs D.E. Transferrin binding in Staphylococcus aureus: Involvement of a cell wall-anchored protein. Mol. Microbiol. 43 (2002) 1603-1614
61. Vermeiren C.L., Pluym M., Mack J., Heinrichs D.E., and Stillman M.J. Characterization of the heme binding porperties of Staphylococcus aureus IsdA. Biochemistry 45 (2006) 12867-12875
62. Vetter S.M., and Schlievert P.M. Glycerol monolaurate inhibits virulence factor production in Bacillus anthracis. Antimicrob. Agents Chemother. 49 (2005) 1302-1305
63. Wadström T. Hydrophobic characteristics of staphylococci: Role of surface structures and role in adhesion and host colonization. In: Doyle R.J., and Rosenberg M. (Eds). Microbial Cell Surface Hydrophobicity (1990), American Society for Microbiology, Washington, D.C. 315-333
64. Waldvogel F.A. Staphylococcus aureus (including toxic shock syndrome). In: Bennett G.L., Bennett J.E., and Dolio R. (Eds). Principles and Practice of Infectious Diseases (1995), Churchill Livingstone, New York 1754-1777
65. Weidenmaier C., Peschel A., Kempf V.A., Lucindo N., Yeaman M.R., and Bayer A.S. 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 (2005) 8033-8038
66. Wille J.J., and Kydonieus A. Palmitoleic acid isomer (C16:1Δ6) in human skin sebum is effective against gram-positive bacteria. Skin Pharmacol. Appl. Skin Physiol. 16 (2003) 176-187
67. Wilson W.W., Wade M.M., Holman S.C., and Champlin F.R. Status of methods for assessing bacterial cell surface charge properties based on zeta potential measurements. J. Microbiol. Methods 43 (2001) 153-164