Staphylococcus aureus-derived membrane vesicles exacerbate skin inflammation in atopic dermatitis

Clinical and Experimental Allergy

Volumn 47, Issue 1, 2017, Pages 85-96

  Jun, S H ^a   Lee, J H ^a   Kim, S I ^b   Choi, C W ^b   Park, T I ^a   Jung, H R ^c   Cho, J W ^c   Kim, S H ^a   Lee, J C ^a  

^a Kyungpook National University School of Medicine   (South Korea)

^b Korea Basic Science Institute (KBSI)   (South Korea)

^c Keimyung University   (South Korea)

Author keywords

atopic dermatitis; dermatology; innate immunity; membrane vesicle; Staphylococcus aureus

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 31; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; SMALL INTERFERING RNA; STAPHYLOCOCCUS PROTEIN A; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR; AUTACOID; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATOPIC DERMATITIS; BACTERIAL COLONIZATION; BACTERIAL MEMBRANE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE RESPONSE; ECZEMA; EPIDERMIS; FEMALE; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOLOGY; IN VITRO STUDY; INFLAMMATORY CELL; INTERCELLULAR SPACE; KERATINOCYTE; MEMBRANE VESICLE; MOUSE; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; SKIN PENETRATION; STAPHYLOCOCCUS AUREUS; TH1 TH2 BALANCE; UPREGULATION; ANIMAL; BIOPSY; COMPLICATION; DISEASE MODEL; IMMUNOLOGY; MEMBRANE MICROPARTICLE; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; SKIN; STAPHYLOCOCCUS INFECTION; ULTRASTRUCTURE;

ANIMALS; BIOPSY; CELL-DERIVED MICROPARTICLES; CYTOKINES; DERMATITIS, ATOPIC; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; INFLAMMATION MEDIATORS; MICE; SKIN; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 85006263340     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/cea.12851     Document Type: Article

References (44)

1. Kuo IH, Yoshida T, De Benedetto A et al. The cutaneous innate immune response in patients with atopic dermatitis. J Allergy Clin Immunol 2013; 131:266–78.
2. Liu FT, Goodarzi H, Chen HY. IgE, mast cells, and eosinophils in atopic dermatitis. Clin Rev Allergy Immunol 2011; 41:298–310.
3. Leung DY, Boguniewicz M, Howell MD et al. New insights into atopic dermatitis. J Clin Invest 2004; 113:651–7.
4. Garmhausen D, Hagemann T, Bieber T et al. Characterization of different courses of atopic dermatitis in adolescent and adult patients. Allergy 2013; 68:498–506.
5. Boguniewicz M, Leung DY. Atopic dermatitis: a disease of altered skin barrier and immune dysregulation. Immunol Rev 2011; 242:233–46.
6. 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.
7. Matsui K, Nishikawa A, Suto H et al. Comparative study of Staphylococcus aureus isolated from lesional and nonlesional skin of atopic dermatitis. Microbiol Immunol 2000; 44:945–7.
8. Tauber M, Balica S, Hsu CY et al. Staphylococcus aureus density on lesional and nonlesional skin is strongly associated with disease severity in atopic dermatitis. J Allergy Clin Immunol 2016; 137:1272–4.
9. Travers JB. Toxic interaction between Th2 cytokines and Staphylococcus aureus in atopic dermatitis. J Invest Dermatol 2014; 134:2069–71.
10. Niebuhr M, Baumert K, Heratizadeh A et al. Impaired NLRP3 inflammasome expression and function in atopic dermatitis due to Th2 milieu. Allergy 2014; 69:1058–67.
11. Sasaki T, Kano R, Sato H et al. Effects of staphylococci on cytokine production from human keratinocytes. Br J Dermatol 2003; 148:46–50.
12. Vu AT, Baba T, Chen X et al. Staphylococcus aureus membrane and diacylated lipopeptide induce thymic stromal lymphopoietin in keratinocytes through the Toll-like receptor 2-Toll-like receptor 6 pathway. J Allergy Clin Immunol 2010; 126:985–93.
13. Schlievert PM, Strandberg KL, Lin YC et al. Secreted virulence factor comparison between methicillin-resistant and methicillin-sensitive Staphylococcus aureus, and its relevance to atopic dermatitis. J Allergy Clin Immunol 2010; 125:39–49.
14. Cardona ID, Cho SH, Leung DY. Role of bacterial superantigens in atopic dermatitis: implications for future therapeutic strategies. Am J Clin Dermatol 2006; 7:273–9.
15. Skov L, Olsen JV, Giorno R et al. Application of staphylococcal enterotoxin B on normal and atopic skin induces up-regulation of T cells by a superantigen-mediated mechanism. J Allergy Clin Immunol 2000; 105:820–6.
16. Travers JB, Leung DY, Johnson C et al. Augmentation of staphylococcal alpha-toxin signaling by the epidermal platelet-activating factor receptor. J Invest Dermatol 2003; 120:789–94.
17. Travers JB, Kozman A, Mousdicas N et al. Infected atopic dermatitis lesions contain pharmacologic amounts of lipoteichoic acid. J Allergy Clin Immunol 2010; 125:146–52.
18. Matsui K, Nishikawa A. Lipoteichoic acid from Staphylococcus aureus induces Th2-prone dermatitis in mice sensitized percutaneously with an allergen. Clin Exp Allergy 2002; 32:783–8.
19. Matsui K, Wirotesangthongw M, Nishikawa A. Percutaneous application of peptidoglycan from Staphylococcus aureus induces eosinophil infiltration in mouse skin. Clin Exp Allergy 2007; 37:615–22.
20. H2 immune response in mice. J Investig Allergol Clin Immunol 2012; 22:80–6.
21. Terada M, Tsutsui H, Imai Y et al. Contribution of IL-18 to atopic-dermatitis-like skin inflammation induced by Staphylococcus aureus product in mice. Proc Natl Acad Sci USA 2006; 103:8816–21.
22. Yao Y, Kozman A, Al-Hassani M et al. Identification of staphylococcal protein A in infected atopic dermatitis lesions. J Invest Dermatol 2010; 130:2502–4.
23. Nakano H, Tsutsui H, Terada M et al. Persistent secretion of IL-18 in the skin contributes to IgE response in mice. Int Immunol 2003; 15:611–21.
24. Kozman A, Yao Y, Bina P et al. Encoding a superantigen by Staphylococcus aureus does not affect clinical characteristics of infected atopic dermatitis lesions. Br J Dermatol 2010; 163:1308–11.
25. Rojo A, Aguinaga A, Monecke S et al. Staphylococcus aureus genomic pattern and atopic dermatitis: may factors other than superantigens be involved? Eur J Clin Microbiol Infect Dis 2014; 33:651–8.
26. Gurung M, Moon DC, Choi CW et al. Staphylococcus aureus produces membrane-derived vesicles that induce host cell death. PLoS ONE 2011; 6:e27958.
27. Lee EY, Choi DY, Kim DK et al. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics 2009; 9:5425–36.
28. Thay B, Wai SN, Oscarsson J. Staphylococcus aureus α-toxin-dependent induction of host cell death by membrane-derived vesicles. PLoS ONE 2013; 8:e54661.
29. Lee HW, Kim SM, Kim JM et al. Potential immunoinflammatory role of staphylococcal enterotoxin A in atopic dermatitis: immunohistopathological analysis and in vitro assay. Ann Dermatol 2013; 25:173–80.
30. Hong SW, Kim MR, Lee EY et al. Extracellular vesicles derived from Staphylococcus aureus induce atopic dermatitis-like skin inflammation. Allergy 2011; 66:351–9.
31. Jeon H, Oh MH, Jun SH et al. Variation among Staphylococcus aureus membrane vesicle proteomes affects cytotoxicity of host cells. Microb Pathog 2016; 93:185–93.
32. Kim BS, Choi JK, Jung HJ et al. Effects of topical application of a recombinant staphylococcal enterotoxin A on DNCB and dust mite extract-induced atopic dermatitis-like lesions in a murine model. Eur J Dermatol 2014; 24:186–93.
33. Cho JW, Cho SY, Lee KS. Roles of SEA-expressing Staphylococcus aureus, isolated from an atopic dermatitis patient, on expressions of human β-defensin-2 and inflammatory cytokines in HaCaT cells. Int J Mol Med 2009; 23:331–5.
34. Choi EJ, Lee S, Kim HH et al. Suppression of dust mite extract and 2,4-dinitrochlorobenzene-induced atopic dermatitis by the water extract of Lindera obtusiloba. J Ethnopharmacol 2011; 137:802–7.
35. Choi JK, Oh HM, Lee S et al. Oleanolic acid acetate inhibits atopic dermatitis and allergic contact dermatitis in a murine model. Toxicol Appl Pharmacol 2013; 269:72–80.
36. Jun SH, Lee JH, Kim BR et al. Acinetobacter baumannii outer membrane vesicles elicit a potent innate immune response via membrane proteins. PLoS ONE 2013; 8:e71751.
37. Jagadeesan S, Kurien G, Divakaran MV et al. Methicillin-resistant Staphylococcus aureus colonization and disease severity in atopic dermatitis: a cross-sectional study from South India. Indian J Dermatol Venereol Leprol 2014; 80:229–34.
38. Niebuhr M, Baumert K, Werfel T. TLR-2-mediated cytokine and chemokine secretion in human keratinocytes. Exp Dermatol 2010; 19:873–7.
39. Morr M, Takeuchi O, Akira S et al. Differential recognition of structural details of bacterial lipopeptides by toll-like receptors. Eur J Immunol 2002; 32:3337–47.
40. Girardin SE, Travassos LH, Hervé M et al. Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J Biol Chem 2003; 278:41702–8.
41. Girardin SE, Boneca IG, Carneiro LA et al. Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 2003; 300:1584–7.
42. Girardin SE, Boneca IG, Viala J et al. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 2003; 278:8869–72.
43. Akdis CA, Akdis M. Immunological differences between intrinsic and extrinsic types of atopic dermatitis. Clin Exp Allergy 2003; 33:1618–21.
44. H17 immune activation compared with extrinsic atopic dermatitis. J Allergy Clin Immunol 2013; 132:361–70.