Nanovesicles from malassezia sympodialis and host exosomes induce cytokine responses - novel mechanisms for host-microbe interactions in atopic eczema

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Gehrmann, Ulf ^a   Qazi, Khaleda Rahman ^a   Johansson, Catharina ^a   Hultenby, Kjell ^b   Karlsson, Maria ^b   Lundeberg, Lena ^b   Gabrielsson, Susanne ^a   Scheynius, Annika ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; CD14 ANTIGEN; CD34 ANTIGEN; FUNGUS ANTIGEN; IMMUNOGLOBULIN E; INTERLEUKIN 4; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; NANOMATERIAL;

ADULT; ARTICLE; ATOPIC DERMATITIS; CD34 SELECTION; CELL SIZE; CELL VACUOLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; EXOSOME; FLOW CYTOMETRY; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOMODULATION; IMMUNOREGULATION; MALASSEZIA; MALASSEZIA SYMPODIALIS; MALE; MOLECULAR PATHOLOGY; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; SKIN SENSITIZATION; SUCROSE GRADIENT; T CELL DEPLETION; WESTERN BLOTTING; BIOSYNTHESIS; CASE CONTROL STUDY; COCULTURE; CYTOLOGY; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MIDDLE AGED; MONOCYTE; MONONUCLEAR CELL; PATHOLOGY;

FUNGI; MALASSEZIA SYMPODIALIS;

ADULT; ALLERGENS; CASE-CONTROL STUDIES; COCULTURE TECHNIQUES; CYTOKINES; DENDRITIC CELLS; DERMATITIS, ATOPIC; EXOSOMES; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOMODULATION; INTERLEUKIN-4; LEUKOCYTES, MONONUCLEAR; MALASSEZIA; MALE; MIDDLE AGED; MONOCYTES; NANOSTRUCTURES; TUMOR NECROSIS FACTOR-ALPHA; YOUNG ADULT;

EID: 79960675116     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021480     Document Type: Article

References (48)

1. Pan BT, Johnstone RM, (1983) Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 33: 967-978.
2. Pan BT, Teng K, Wu C, Adam M, Johnstone RM, (1985) Electron-microscopic evidence fore externalization of the transferrin receptor in vesicular form in sheep reticulocytes. Journal of Cell Biology 101: 942-948.
3. Admyre C, Telemo E, Almqvist N, Lotvall J, Lahesmaa R, et al. (2008) Exosomes- nanovesicles with possible roles in allergic inflammation. Allergy 63: 404-408.
4. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, et al. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659.
5. Korkut C, Ataman B, Ramachandran P, Ashley J, Barria R, et al. (2009) Trans-synaptic transmission of vesicular Wnt signals through Evi/Wntless. Cell 139: 393-404.
6. Bhatnagar S, Shinagawa K, Castellino F, Schorey J, (2007) Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo. Blood 110: 3234-3244.
7. Nguyen DG, Booth A, Gould SJ, Hildreth JE, (2003) Evidence that HIV budding in primary macrophages occurs through the exosome release pathway. J Biol Chem 278: 52347-52354.
8. Caby MP, Lankar D, Vincendeau-Scherrer C, Raposo G, Bonnerot C, (2005) Exosomal-like vesicles are present in human blood plasma. Int Immunol 17: 879-887.
9. Admyre C, Grunewald J, Thyberg J, Gripenback S, Tornling G, et al. (2003) Exosomes with major histocompatibility complex class II and co-stimulatory molecules are present in human BAL fluid. Eur Respir J 22: 578-583.
10. Admyre C, Johansson SM, Qazi KR, Filen JJ, Lahesmaa R, et al. (2007) Exosomes with immune modulatory features are present in human breast milk. J Immunol 179: 1969-1978.
11. Pisitkun T, Shen RF, Knepper MA, (2004) Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci U S A 101: 13368-13373.
12. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, et al. (1996) B lymphocytes secrete antigen-presenting vesicles. J Exp Med 183: 1161-1172.
13. Thery C, Duban L, Segura E, Veron P, Lantz O, et al. (2002) Indirect activation of naive CD4+ T cells by dendritic cell-derived exosomes. Nat Immunol 3: 1156-1162.
14. Chaput N, Schartz NE, Andre F, Taieb J, Novault S, et al. (2004) Exosomes as potent cell-free peptide-based vaccine. II. Exosomes in CpG adjuvants efficiently prime naive Tc1 lymphocytes leading to tumor rejection. J Immunol 172: 2137-2146.
15. Hao S, Yuan J, Xiang J, (2007) Nonspecific CD4(+) T cells with uptake of antigen-specific dendritic cell-released exosomes stimulate antigen-specific CD8(+) CTL responses and long-term T cell memory. J Leukoc Biol 82: 829-838.
16. Hao S, Liu Y, Yuan J, Zhang X, He T, et al. (2007) Novel exosome-targeted CD4+ T cell vaccine counteracting CD4+25+ regulatory T cell-mediated immune suppression and stimulating efficient central memory CD8+ CTL responses. J Immunol 179: 2731-2740.
17. Andre F, Chaput N, Schartz NE, Flament C, Aubert N, et al. (2004) Exosomes as potent cell-free peptide-based vaccine. I. Dendritic cell-derived exosomes transfer functional MHC class I/peptide complexes to dendritic cells. J Immunol 172: 2126-2136.
18. Beauvillain C, Juste MO, Dion S, Pierre J, Dimier-Poisson I, (2009) Exosomes are an effective vaccine against congenital toxoplasmosis in mice. Vaccine 27: 1750-1757.
19. Beauvillain C, Ruiz S, Guiton R, Bout D, Dimier-Poisson I, (2007) A vaccine based on exosomes secreted by a dendritic cell line confers protection against T. gondii infection in syngeneic and allogeneic mice. Microbes Infect 9: 1614-1622.
20. Admyre C, Bohle B, Johansson SM, Focke-Tejkl M, Valenta R, et al. (2007) B cell-derived exosomes can present allergen peptides and activate allergen-specific T cells to proliferate and produce TH2-like cytokines. J Allergy Clin Immunol 120: 1418-1424.
21. Akdis CA, Akdis M, Bieber T, Bindslev-Jensen C, Boguniewicz M, et al. (2006) Diagnosis and treatment of atopic dermatitis in children and adults: European Academy of Allergology and Clinical Immunology/American Academy of Allergy, Asthma and Immunology/PRACTALL Consensus Report. J Allergy Clinl Immunol 118: 152-169.
22. Bieber T, Novak N, (2009) Pathogenesis of atopic dermatitis: new developments. Curr Allergy Asthma Rep 9: 291-294.
23. Ashbee HR, Scheynius A, (2010) Malassezia. Pathogenic Yeasts, The Yeast Handbook pp. 209-230.
24. Gaitanis G, Mayser P, Scheynius A, Crameri R, (2010) Malassezia Yeasts in Seborrhoeic and Atopic Eczemas. Malassezia and the Skin pp. 201-229.
25. Buentke E, Zargari A, Heffler LC, Avila-Carino J, Savolainen J, et al. (2000) Uptake of the yeast Malassezia furfur and its allergenic components by human immature CD1a+ dendritic cells. Clin Exp Allergy 30: 1759-1770.
26. Buentke E, Heffler LC, Wallin RP, Lofman C, Ljunggren HG, et al. (2001) The allergenic yeast Malassezia furfur induces maturation of human dendritic cells. Clin Exp Allergy 31: 1583-1593.
27. Johansson C, Eshaghi H, Linder MT, Jakobson E, Scheynius A, (2002) Positive atopy patch test reaction to Malassezia furfur in atopic dermatitis correlates with a T helper 2-like peripheral blood mononuclear cells response. J Invest Dermatol 118: 1044-1051.
28. Albuquerque PC, Nakayasu ES, Rodrigues ML, Frases S, Casadevall A, et al. (2008) Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell Microbiol 10: 1695-1710.
29. Rodrigues ML, Nimrichter L, Oliveira DL, Frases S, Miranda K, et al. (2007) Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryot Cell 6: 48-59.
30. Casadevall A, Nosanchuk JD, Williamson P, Rodrigues ML, (2009) Vesicular transport across the fungal cell wall. Trends Microbiol 17: 158-162.
31. Oliveira DL, Freire-de-Lima CG, Nosanchuk JD, Casadevall A, Rodrigues ML, et al. Extracellular vesicles from Cryptococcus neoformans modulate macrophage functions. Infect Immun 78: 1601-1609.
32. Johansson C, Ahlborg N, Andersson A, Lundeberg L, Karlsson MA, et al. (2009) Elevated peripheral allergen-specific T cell response is crucial for a positive atopy patch test reaction. Int Arch Allergy Immunol 150: 51-58.
33. Sallusto F, Lanzavecchia A, (1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 179: 1109-1118.
34. Thery C, Amigorena S, Raposo G, Clayton A, (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol Chapter 3: Unit 3 22.
35. Johansson SM, Admyre C, Scheynius A, Gabrielsson S, (2008) Different types of in vitro generated human monocyte-derived dendritic cells release exosomes with distinct phenotypes. Immunology 123: 491-499.
36. Kim SH, Bianco NR, Shufesky WJ, Morelli AE, Robbins PD, (2007) MHC class II+ exosomes in plasma suppress inflammation in an antigen-specific and Fas ligand/Fas-dependent manner. J Immunol 179: 2235-2241.
37. Almqvist N, Lonnqvist A, Hultkrantz S, Rask C, Telemo E, (2008) Serum-derived exosomes from antigen-fed mice prevent allergic sensitization in a model of allergic asthma. Immunology 125: 21-27.
38. Gafvelin G, Thunberg S, Kronqvist M, Grönlund H, Grönneberg R, Troye-Blomberg M, et al. (2005) Cytokine and antibody responses in birch pollen-allergic patients treated with genetically modified derivatives of the major bitch pollen allergen bet v 1. Int Arch Allergy Immunol 138: 59-66.
39. Bhatnagar S, Schorey JS, (2007) Exosomes released from infected macrophages contain Mycobacterium avium glycopeptidolipids and are proinflammatory. J Biol Chem 282: 25779-25789.
40. 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.
41. Selander C, Zargari A, Mollby R, Rasool O, Scheynius A, (2006) Higher pH level, corresponding to that on the skin of patients with atopic eczema, stimulates the release of Malassezia sympodialis allergens. Allergy 61: 1002-1008.
42. Vilhelmsson M, Johansson C, Jacobsson-Ekman G, Crameri R, Zargari A, et al. (2007) The Malassezia sympodialis allergen Mala s 11 induces human dendritic cell maturation, in contrast to its human homologue manganese superoxide dismutase. Int Arch Allergy Immunol 143: 155-162.
43. Kesavan S, Walters CE, Holland KT, Ingham E, (1998) The effects of Malassezia on pro-inflammatory cytokine production by human peripheral blood mononuclear cells in vitro. Med Mycol 36: 97-106.
44. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, et al. (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10: 1470-1476.
45. Pfeiffer JR, McAovy BL, Fecteau RE, Deleault KM, Brooks SA, (2011) CARHSP1 is required for effective TNF-{alpha} mRNA stabilization and localizes to processing bodies and exosomes. Mol Cell Biol 31: 277-286.
46. Esser J, Gehrmann U, D'Alexandri FL, Hidalgo-Estevez AM, Wheelock CE, et al. (2010) Exosomes from human macrophages and dendritic cells contain enzymes for leukotriene biosynthesis and promote granulocyte migration. J Allergy Clin Immunol 126: 1032-1040.
47. Hood JL, Pan H, Lanza GM, Wickline SA, Consortium for Translational Research in Advanced Imaging and Nanomedicine (C-TRAIN) (2009) Paracrine induction of endothelium by tumor exosomes. Lab Invest 89: 1317-1328.
48. Kunz B, Oranje AP, Labreze L, Stalder JF, Ring J, et al. (1997) Clinical validation and guidelines for the SCORAD index: consensus report of the European Task Force on Atopic Dermatitis. Dermatology 195: 10-19.