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Advances in Dermatology and Allergology/Postępy Dermatologii i Alergologii
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1/2019
vol. 36
 
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abstract:
Review paper

Staphylococcus aureus: an underestimated factor in the pathogenesis of atopic dermatitis?

Leszek Blicharz, Lidia Rudnicka, Zbigniew Samochocki

Adv Dermatol Allergol 2019; XXXVI (1): 11-17
Online publish date: 2019/02/22
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Atopic dermatitis is a common, recurrent pruritic dermatosis with a complex pathogenesis. It has been associated with disordered patterns of immunological response and impaired epithelial barrier integrity. These features predispose the patients to robust colonization of skin lesions by Staphylococcus aureus. Virulence factors of S. aureus (e.g. superantigens, - and -toxin, protein A) have been shown to exacerbate and perpetuate the course of atopic dermatitis. Novel therapeutic options with potential for restoring natural microbiome composition are being elaborated and may enter clinical practice in the future.
keywords:

atopic dermatitis, pathogenesis, Staphylococcus aureus

references:
Leung DY. New insights into atopic dermatitis: role of skin barrier and immune dysregulation. Allergol Int 2013; 62: 151-61.
Werfel T, Allam JP, Biedermann T, et al. Cellular and molecular immunologic mechanisms in patients with atopic dermatitis. J Allergy Clin Immunol 2016; 138: 336-49.
Grice EA, Segre JA. The skin microbiome. Nat Rev Microbiol 2011; 9: 244-53.
Adamczyk K, Garncarczyk A, Antończak P. The microbiome of the skin. Dermatol Rev 2018; 105: 285-97.
Grice EA, Kong HH, Conlan S, et al. Topographical and temporal diversity of the human skin microbiome. Science 2009; 324: 1190-2.
Bach JF. The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med 2002; 347: 911-20.
Braun-Fahrländer C, Riedler J, Herz U, et al. Environmental exposure to endotoxin and its relation to asthma in school-age children. Allergy 2007; 62: 1387-93.
Rivers DA, Stern R, Maibach HI. A defective inflammatory response may underlie cases of atopic dermatitis. J Eur Acad Dermatol Venereol 2016 Dec 21 [Epub Ahead of print].
De Vuyst É, Mound A, Lambert de Rouvroit C, Poumay Y. Modelling atopic dermatitis during the morphogenetic process involved in reconstruction of a human epidermis. Curr Res Transl Med 2016; 64: 179-83.
Hönzke S, Wallmeyer L, Ostrowski A, et al. Influence of Th2 cytokines on the cornified envelope, tight junction proteins, and beta-defensins in filaggrin-deficient skin equivalents. J Invest Dermatol 2016; 136: 631-9.
Naik S, Bouladoux N, Wilhelm C, et al. Compartmentalized control of skin immunity by resident commensals. Science 2012; 337: 1115-9.
Kuo IH, Yoshida T, De Benedetto A, Beck LA. The cutaneous innate immune response in patients with atopic dermatitis. J Allergy Clin Immunol 2013; 131: 266-78.
Hasannejad H, Takahashi R, Kimishima M, et al. Selective impairment of Toll-like receptor 2-mediated proinflammatory cytokine production by monocytes from patients with atopic dermatitis. J Allergy Clin Immunol 2007; 120: 69-75.
Niebuhr M, Lutat C, Sigel S, Werfel T. Impaired TLR-2 expression and TLR-2-mediated cytokine secretion in macrophages from patients with atopic dermatitis. Allergy 2009; 64: 1580-7.
Kuo IH, Carpenter-Mendini A, Yoshida T, et al. Activation of epidermal toll-like receptor 2 enhances tight junction function: implications for atopic dermatitis and skin barrier repair. J Invest Dermatol 2013; 133: 988-98.
Bäsler K, Galliano MF, Bergmann S, et al. Biphasic influence of Staphylococcus aureus on human epidermal tight junctions. Ann N Y Acad Sci 2017; 1405: 53-70.
Ishikawa J, Narita H, Kondo N, et al. Changes in the ceramide profile of atopic dermatitis patients. J Invest Dermatol 2010; 130: 2511-4.
van Smeden J, Janssens M, Kaye EC, et al. The importance of free fatty acid chain length for the skin barrier function in atopic eczema patients. Exp Dermatol 2014; 23: 45-52.
Bäsler K, Brandner JM. Tight junctions in skin inflammation. Pflugers Arch 2017; 469: 3-14.
Gruber R, Börnchen C, Rose K, et al. Diverse regulation of claudin-1 and claudin-4 in atopic dermatitis. Am J Pathol 2015; 185: 2777-89.
Sinha B, François PP, Nüsse O, et al. Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell Microbiol 1999; 1: 101-17.
Cho SH, Strickland I, Boguniewicz M, Leung DY. Fibronectin and fibrinogen contribute to the enhanced binding of Staphylococcus aureus to atopic skin. J Allergy Clin Immunol 2001; 108: 269-74.
Fleury OM, McAleer MA, Feuillie C, et al. Clumping factor B promotes adherence of Staphylococcus aureus to corneocytes in atopic dermatitis. Infect Immun 2017; 85: pii: e00994-16.
Ogawa H, Yoshiike T. A speculative view of atopic dermatitis: barrier dysfunction in pathogenesis. J Dermatol Sci 1993; 5: 197-204.
Berard F, Marty JP, Nicolas JF. Allergen penetration through the skin. Eur J Dermatol 2003; 13: 324-30.
Kamata Y, Tominaga M, Takamori K. Itch in atopic dermatitis management. Curr Probl Dermatol 2016; 50: 86-93.
Hirota T, Takahashi A, Kubo M, et al. Genome-wide association study identifies eight new susceptibility loci for atopic dermatitis in the Japanese population. Nat Genet 2012; 44: 1222-6.
Ellinghaus D, Baurecht H, Esparza-Gordillo J, et al. High-density genotyping study identifies four new susceptibility loci for atopic dermatitis. Nat Genet 2013; 45: 808-12.
Virtue A, Wang H, Yang XF. MicroRNAs and toll-like receptor/interleukin-1 receptor signaling. J Hematol Oncol 2012; 5: 66.
He X, Jing Z, Cheng G. MicroRNAs: new regulators of Toll-like receptor signalling pathways. Biomed Res Int 2014; 2014: 945169.
O’Neill LA, Sheedy FJ, McCoy CE. MicroRNAs: the fine-tuners of Toll-like receptor signalling. Nat Rev Immunol 2011; 11: 163-75.
Malnick SD, Zimhony O. Treatment of Clostridium difficile-associated diarrhea. Ann Pharmacother 2002; 36: 1767-75.
Fredricks DN, Fiedler TL, Marrazzo JM. Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med 2005; 353: 1899-911.
Leyden JJ, Marples RR, Kligman AM. Staphylococcus aureus in the lesions of atopic dermatitis. Br J Dermatol 1974; 90: 525-30.
Park HY, Kim CR, Huh IS, et al. Staphylococcus aureus colonization in acute and chronic skin lesions of patients with atopic dermatitis. Ann Dermatol 2013; 25: 410-6.
Kong HH, Oh J, Deming C, et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 2012; 22: 850-9.
Salava A, Lauerma A. Role of the skin microbiome in atopic dermatitis. Clin Transl Allergy 2014; 4: 33.
Wong SM, Ng TG, Baba R. Efficacy and safety of sodium hypochlorite (bleach) baths in patients with moderate to severe atopic dermatitis in Malaysia. J Dermatol 2013; 40: 874-80.
Meylan P, Lang C, Mermoud S, et al. Skin colonization by Staphylococcus aureus precedes the clinical diagnosis of atopic dermatitis in infancy. J Invest Dermatol 2017; 137: 2497-504.
Nowrouzian FL, Lina G, Hodille E, et al. Superantigens and adhesins of infant gut commensal Staphylococcus aureus strains and association with subsequent development of atopic eczema. Br J Dermatol 2017; 176: 439-45.
Kennedy EA, Connolly J, Hourihane JO, et al. Skin microbiome before development of atopic dermatitis: early colonization with commensal staphylococci at 2 months is associated with a lower risk of atopic dermatitis at 1 year. J Allergy Clin Immunol 2017; 139: 166-72.
Ong PY, Leung DY. Bacterial and viral infections in atopic dermatitis: a comprehensive review. Clin Rev Allergy Immunol 2016; 51: 329-37.
Hon KL, Tsang YC, Pong NH. Exploring Staphylococcus epidermidis in atopic eczema: friend or foe? Clin Exp Dermatol 2016; 41: 659-63.
Lai Y, Cogen AL, Radek KA, et al. Activation of TLR2 by a small molecule produced by Staphylococcus epidermidis increases antimicrobial defense against bacterial skin infections. J Invest Dermatol 2010; 130: 2211-21.
Cogen AL, Yamasaki K, Sanchez KM, et al. Selective antimicrobial action is provided by phenol-soluble modulins derived from Staphylococcus epidermidis, a normal resident of the skin. J Invest Dermatol 2010; 130: 192-200.
Otto M. Staphylococcus colonization of the skin and antimicrobial peptides. Expert Rev Dermatol 2010; 5: 183-95.
Sugimoto S, Iwamoto T, Takada K, et al. Staphylococcus epidermidis Esp degrades specific proteins associated with Staphylococcus aureus biofilm formation and host-pathogen interaction. J Bacteriol 2013; 195: 1645-55.
Iwase T, Uehara Y, Shinji H, et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 2010; 465: 346-9.
Lai Y, Di Nardo A, Nakatsuji T, et al. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat Med 2009; 15: 1377-82.
Vandecandelaere I, Depuydt P, Nelis HJ, Coenye T. Protease production by Staphylococcus epidermidis and its effect on Staphylococcus aureus biofilms. Pathog Dis 2014; 70: 321-31.
Gonzalez T, Biagini Myers JM, Herr AB, Khurana Hershey GK. Staphylococcal biofilms in atopic dermatitis. Curr Allergy Asthma Rep 2017; 17: 81.
Sonesson A, Przybyszewska K, Eriksson S, et al. Identification of bacterial biofilm and the Staphylococcus aureus derived protease, staphopain, on the skin surface of patients with atopic dermatitis. Sci Rep 2017; 7: 8689.
Miedzobrodzki J, Kaszycki P, Bialecka A, Kasprowicz A. Proteolytic activity of Staphylococcus aureus strains isolated from the colonized skin of patients with acute-phase atopic dermatitis. Eur J Clin Microbiol Infect Dis 2002; 21: 269-76.
Takai T, Ikeda S. Barrier dysfunction caused by environmental proteases in the pathogenesis of allergic diseases. Allergol Int 2011; 60: 25-35.
Nakatsuji T, Chen TH, Two AM, et al. Staphylococcus aureus exploits epidermal barrier defects in atopic dermatitis to trigger cytokine expression. J Invest Dermatol 2016; 136: 2192-200.
Wang B, McHugh BJ, Qureshi A, et al. IL-1B induced protection of keratinocytes against Staphylococcus aureus-secreted proteases is mediated by human b-defensin 2. J Invest Dermatol 2017; 137: 95-105.
Nada HA, Gomaa NI, Elakhras A, et al. Skin colonization by superantigen-producing Staphylococcus aureus in Egyptian patients with atopic dermatitis and its relation to disease severity and serum interleukin-4 level. Int J Infect Dis 2012; 16: e29-33.
Na SY, Roh JY, Kim JM, et al. Analysis of colonization and genotyping of the exotoxins of Staphylococcus aureus in patients with atopic dermatitis. Ann Dermatol 2012; 24: 413-9.
Xu SX, McCormick JK. Staphylococcal superantigens in colonization and disease. Front Cell Infect Microbiol 2012; 2: 52.
Lehmann HS, Heaton T, Mallon D, Holt PG. Staphylococcal enterotoxin-B-mediated stimulation of interleukin-13 production as a potential aetiologic factor in eczema in infants. Int Arch Allergy Immunol 2004; 135: 306-12.
Gould HJ, Takhar P, Harries HE, et al. The allergic march from Staphylococcus aureus superantigens to immunoglobulin E. Chem Immunol Allergy 2007; 93: 106-36.
Schlievert PM, Case LC, Strandberg KL, et al. Superantigen profile of Staphylococcus aureus isolates from patients with steroid-resistant atopic dermatitis. Clin Infect Dis 2008; 46: 1562-7.
Fukushima H, Hirano T, Shibayama N, et al. The role of immune response to Staphylococcus aureus superantigens and disease severity in relation to the sensitivity to tacrolimus in atopic dermatitis. Int Arch Allergy Immunol 2006; 141: 281-9.
Krogman A, Tilahun A, David CS, et al. HLA-DR polymorphisms influence in vivo responses to staphylococcal toxic shock syndrome toxin-1 in a transgenic mouse model. HLA 2017; 89: 20-8.
Orfali RL, Sato MN, Santos VG, et al. Staphylococcal enterotoxin B induces specific IgG4 and IgE antibody serum levels in atopic dermatitis. Int J Dermatol 2015; 54: 898-904.
Lin YT, Wang CT, Chao PS, et al. Skin-homing CD4+ Foxp3+ T cells exert Th2-like function after staphylococcal superantigen stimulation in atopic dermatitis patients. Clin Exp Allergy 2011; 41: 516-25.
Matsui K, Nishikawa A. Lipoteichoic acid from Staphylococcus aureus enhances allergen-specific immunoglobulin E production in mice. Clin Exp Allergy 2003; 33: 842-8.
Hon KL, Tsang KY, Kung JS, et al. Clinical signs, staphylococcus and atopic eczema-related seromarkers. Molecules 2017; 22: pii: E291.
Zhang X, Shang W, Yuan J, et al. Positive feedback cycle of TNFαlpha promotes staphylococcal enterotoxin B-induced THP-1 cell apoptosis. Front Cell Infect Microbiol 2016; 6: 109.
Sonkoly E, Muller A, Lauerma AI, et al. IL-31: a new link between T cells and pruritus in atopic skin inflammation. J Allergy Clin Immunol 2006; 117: 411-7.
van Drongelen V, Haisma EM, Out-Luiting JJ, et al. Reduced filaggrin expression is accompanied by increased Staphylococcus aureus colonization of epidermal skin models. Clin Exp Allergy 2014; 44: 1515-24.
Bin L, Kim BE, Brauweiler A, et al. Staphylococcus aureus alpha-toxin modulates skin host response to viral infection. J Allergy Clin Immunol 2012; 130: 683-91.e2.
Brauweiler AM, Goleva E, Leung DYM. Th2 cytokines increase Staphylococcus aureus alpha toxin-induced keratinocyte death through the signal transducer and activator of transcription 6 (STAT6). J Invest Dermatol 2014; 134: 2114-21.
Hong SW, Choi EB, Min TK, et al. An important role of alpha-hemolysin in extracellular vesicles on the development of atopic dermatitis induced by Staphylococcus aureus. PLoS One 2014; 9: e100499.
Olsen JR, Piguet V, Gallacher J, Francis NA. Molluscum contagiosum and associations with atopic eczema in children: a retrospective longitudinal study in primary care. Br J Gen Pract 2016; 66: e53-8.
Cheung GY, Joo HS, Chatterjee SS, Otto M. Phenol-soluble modulins – critical determinants of staphylococcal virulence. FEMS Microbiol Rev 2014; 38: 698-719.
Nakamura Y, Oscherwitz J, Cease KB, et al. Staphylococcus delta-toxin induces allergic skin disease by activating mast cells. Nature 2013; 503: 397-401.
Syed AK, Reed TJ, Clark KL, et al. Staphlyococcus aureus phenol-soluble modulins stimulate the release of proinflammatory cytokines from keratinocytes and are required for induction of skin inflammation. Infect Immun 2015; 83: 3428-37.
Votintseva AA, Fung R, Miller RR, et al. Prevalence of Staphylococcus aureus protein A (spa) mutants in the community and hospitals in Oxfordshire. BMC Microbiol 2014; 14: 63.
Ezepchuk YV, Leung DY, Middleton MH, et al. Staphylococcal toxins and protein A differentially induce cytotoxicity and release of tumor necrosis factor-alpha from human keratinocytes. J Invest Dermatol 1996; 107: 603-9.
Harkins CP, McAleer MA, Bennett D, et al. The widespread use of topical antimicrobials enriches for resistance in Staphylococcus aureus isolated from atopic dermatitis patients. Br J Dermatol 2018; 179: 951-8.
Błażewicz I, Jaśkiewicz M, Piechowicz L, et al. Activity of antimicrobial peptides and conventional antibiotics against superantigen positive Staphylococcus aureus isolated from patients with atopic dermatitis. Adv Dermatol Allergol 2018; 35: 74-82.
Guéniche A, Hennino A, Goujon C, et al. Improvement of atopic dermatitis skin symptoms by Vitreoscilla filiformis bacterial extract. Eur J Dermatol 2006; 16: 380-4.
Guéniche A, Cathelineau AC, Bastien P, et al. Vitreoscilla filiformis biomass improves seborrheic dermatitis. J Eur Acad Dermatol Venereol 2008; 22: 1014-5.
Gueniche A, Knaudt B, Schuck E, et al. Effects of nonpathogenic gram-negative bacterium Vitreoscilla filiformis lysate on atopic dermatitis: a prospective, randomized, double-blind, placebo-controlled clinical study. Br J Dermatol 2008; 159: 1357-63.
Volz T, Skabytska Y, Guenova E, et al. Nonpathogenic bacteria alleviating atopic dermatitis inflammation induce IL-10-producing dendritic cells and regulatory Tr1 cells. J Invest Dermatol 2014; 134: 96-104.
Mahe YF, Perez MJ, Tacheau C, et al. A new Vitreoscilla filiformis extract grown on spa water-enriched medium activates endogenous cutaneous antioxidant and antimicrobial defenses through a potential Toll-like receptor 2/protein kinase C, zeta transduction pathway. Clin Cosmet Investig Dermatol 2013; 6: 191-6.
Blanchet-Réthoré S, Bourdès V, Mercenier A, et al. Effect of a lotion containing the heat-treated probiotic strain Lactobacillus johnsonii NCC 533 on Staphylococcus aureus colonization in atopic dermatitis. Clin Cosmet Investig Dermatol 2017; 10: 249-57.
Nakatsuji T, Chen TH, Narala S, et al. Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis. Sci Transl Med 2017; 9: pii: eaah4680. doi: 10.1126/scitranslmed.aah4680.
Myles IA, Earland NJ, Anderson ED, et al. First-in-human topical microbiome transplantation with Roseomonas mucosa for atopic dermatitis. JCI Insight 2018; 3: pii: 120608.
Dawgul M, Baranska-Rybak W, Piechowicz L, et al. The antistaphylococcal activity of citropin 1.1 and temporin a against planktonic cells and biofilms formed by isolates from patients with atopic dermatitis: an assessment of their potential to induce microbial resistance compared to conventional antimicrobials. Pharmaceuticals (Basel) 2016; 9: pii: E30. doi: 10.3390/ph9020030.
Zapotoczna M, Forde É, Hogan S, et al. Eradication of Staphylococcus aureus biofilm infections using synthetic antimicrobial peptides. J Infect Dis 2017; 215: 975-83.
Ng SMS, Teo SW, Yong YE, et al. Preliminary investigations into developing all-D Omiganan for treating Mupirocin-resistant MRSA skin infections. Chem Biol Drug Des 2017; 90: 1155-60.
Fischetti VA. Lysin therapy for staphylococcus aureus and other bacterial pathogens. Curr Top Microbiol Immunol 2017; 409: 529-40.
Schuch R, Lee HM, Schneider BC, et al. Combination therapy with lysin CF-301 and antibiotic is superior to antibiotic alone for treating methicillin-resistant Staphylococcus aureus-induced murine bacteremia. J Infect Dis 2014; 209: 1469-78.
Totté JEE, van Doorn MB, Pasmans SGMA. successful treatment of chronic Staphylococcus aureus-related dermatoses with the topical endolysin staphefekt SA.100: a report of 3 cases. Case Rep Dermatol 2017; 9: 19-25.
Totté J, de Wit J, Pardo L, et al. Targeted anti-staphylococcal therapy with endolysins in atopic dermatitis and the effect on steroid use, disease severity and the microbiome: study protocol for a randomized controlled trial (MAAS trial). Trials 2017; 18: 404.
Baldry M, Nakamura Y, Nakagawa S, et al. Application of an agr-specific anti-virulence compound as therapy for Staphylococcus aureus-induced inflammatory skin disease. J Infect Dis 2018; 218: 1009-13.
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