Recognition of Candida albicans by Dectin-1 induces mast cell activation

Immunobiology

Volumn 220, Issue 9, 2015, Pages 1093-1100

  Nieto Patlán, Alejandro ^a,d   Campillo Navarro, Marcia ^a   Rodríguez Cortés, Octavio ^b   Muñoz Cruz, Samira ^c   Wong Baeza, Isabel ^a   Estrada Parra, Sergio ^a   Estrada García, Iris ^a   Serafín López, Jeanet ^a   Chacón Salinas, Rommel ^a  

^a INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^b ESM IPN   (Mexico)

^c INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^d IMAGINE INSTITUTE   (France)

Author keywords

Candida albicans; Chemokines; Cytokines; Dectin 1; Mast cell

Indexed keywords

DECTIN 1; I KAPPA B ALPHA; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; PROTEIN KINASE SYK; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; I KAPPA B KINASE; IL1B PROTEIN, RAT; LECTIN; PROTEIN TYROSINE KINASE; SIGNAL PEPTIDE;

ANIMAL CELL; ARTICLE; BONE MARROW DERIVED MAST CELL; CANDIDA ALBICANS; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FUNGUS HYPHAE; MALE; MAST CELL; MAST CELL DEGRANULATION; MOUSE; NONHUMAN; PERITONEUM MAST CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RAT; ANIMAL; BIOSYNTHESIS; CELL CULTURE; DEGRANULATION; IMMUNOLOGY; INFLAMMATION; METABOLISM; PHOSPHORYLATION; SPRAGUE DAWLEY RAT; YEAST;

ANIMALS; CANDIDA ALBICANS; CELL DEGRANULATION; CELLS, CULTURED; CHEMOKINE CCL3; CHEMOKINE CCL4; HYPHAE; I-KAPPA B KINASE; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LECTINS, C-TYPE; MALE; MAST CELLS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; TUMOR NECROSIS FACTOR-ALPHA; YEASTS;

EID: 84983187689     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2015.05.005     Document Type: Article

References (57)

1. Aoki R., Kawamura T., Goshima F., Ogawa Y., Nakae S., Nakao A., Moriishi K., Nishiyama Y., Shimada S. Mast cells play a key role in host defense against herpes simplex virus infection through TNF-alpha and IL-6 production. J. Invest. Dermatol. 2013, 133:2170.
2. Bassilana M., Hopkins J., Arkowitz R.A. Regulation of the Cdc42/Cdc24 GTPase module during Candida albicans hyphal growth. Eukaryot. Cell 2005, 4:588.
3. Biggs L., Yu C., Fedoric B., Lopez A.F., Galli S.J., Grimbaldeston M.A. Evidence that vitamin D(3) promotes mast cell-dependent reduction of chronic UVB-induced skin pathology in mice. J. Exp. Med. 2010, 207:455.
4. Brown G.D., Gordon S. Immune recognition. A new receptor for beta-glucans. Nature 2001, 413:36.
5. Campillo-Navarro M., Chavez-Blanco A.D., Wong-Baeza I., Serafin-Lopez J., Flores-Mejia R., Estrada-Parra S., Estrada-Garcia I., Chacon-Salinas R. Mast cells in lung homeostasis: beyond type I hypersensitivity. Curr. Respir. Med. Rev. 2014, 10:115.
6. Chacon-Salinas R., Chen L., Chavez-Blanco A.D., Limon-Flores A.Y., Ma Y., Ullrich S.E. An essential role for platelet-activating factor in activating mast cell migration following ultraviolet irradiation. J. Leukoc. Biol. 2014, 95:139.
7. Chacon-Salinas R., Limon-Flores A.Y., Chavez-Blanco A.D., Gonzalez-Estrada A., Ullrich S.E. Mast cell-derived IL-10 suppresses germinal center formation by affecting T follicular helper cell function. J. Immunol. 2011, 186:25.
8. Chan C.Y., St John A.L., Abraham S.N. Mast cell interleukin-10 drives localized tolerance in chronic bladder infection. Immunity 2013, 38:349.
9. Charo I.F., Ransohoff R.M. The many roles of chemokines and chemokine receptors in inflammation. N. Engl. J. Med. 2006, 354:610.
10. Cheng S.C., van de Veerdonk F.L., Lenardon M., Stoffels M., Plantinga T., Smeekens S., Rizzetto L., Mukaremera L., Preechasuth K., Cavalieri D., Kanneganti T.D., van der Meer J.W., Kullberg B.J., Joosten L.A., Gow N.A., Netea M.G. The dectin-1/inflammasome pathway is responsible for the induction of protective T-helper 17 responses that discriminate between yeasts and hyphae of Candida albicans. J. Leukoc. Biol. 2011, 90:357.
11. Dennehy K.M., Ferwerda G., Faro-Trindade I., Pyz E., Willment J.A., Taylor P.R., Kerrigan A., Tsoni S.V., Gordon S., Meyer-Wentrup F., Adema G.J., Kullberg B.J., Schweighoffer E., Tybulewicz V., Mora-Montes H.M., Gow N.A., Williams D.L., Netea M.G., Brown G.D. Syk kinase is required for collaborative cytokine production induced through Dectin-1 and Toll-like receptors. Eur. J. Immunol. 2008, 38:500.
12. Drummond R.A., Brown G.D. The role of Dectin-1 in the host defence against fungal infections. Curr. Opin. Microbiol. 2011, 14:392.
13. Ebert S., Becker M., Lemmermann N.A., Buttner J.K., Michel A., Taube C., Podlech J., Bohm V., Freitag K., Thomas D., Holtappels R., Reddehase M.J., Stassen M. Mast cells expedite control of pulmonary murine cytomegalovirus infection by enhancing the recruitment of protective CD8T cells to the lungs. PLoS Pathog. 2014, 10:e1004100.
14. Frohner I.E., Bourgeois C., Yatsyk K., Majer O., Kuchler K. Candida albicans cell surface superoxide dismutases degrade host-derived reactive oxygen species to escape innate immune surveillance. Mol. Microbiol. 2009, 71:240.
15. Furuta T., Kikuchi T., Iwakura Y., Watanabe N. Protective roles of mast cells and mast cell-derived TNF in murine malaria. J. Immunol. 2006, 177:3294.
16. Galli S.J., Tsai M. Mast cells: versatile regulators of inflammation, tissue remodeling, host defense and homeostasis. J. Dermatol. Sci. 2008, 49:7.
17. Gekara N.O., Weiss S. Mast cells initiate early anti-Listeria host defences. Cell Microbiol. 2008, 10:225.
18. Ghosh S., Hayden M.S. New regulators of NF-kappaB in inflammation. Nat. Rev. Immunol. 2008, 8:837.
19. Grimbaldeston M.A., Nakae S., Kalesnikoff J., Tsai M., Galli S.J. Mast cell-derived interleukin 10 limits skin pathology in contact dermatitis and chronic irradiation with ultraviolet B. Nat. Immunol. 2007, 8:1095.
20. Haidl I.D., McAlpine S.M., Marshall J.S. Enhancement of mast cell IL-6 production by combined toll-like and nucleotide-binding oligomerization domain-like receptor activation. Int. Arch. Allergy Immunol. 2011, 154:227.
21. Herre J., Marshall A.S., Caron E., Edwards A.D., Williams D.L., Schweighoffer E., Tybulewicz V., Reis e Sousa C., Gordon S., Brown G.D. Dectin-1 uses novel mechanisms for yeast phagocytosis in macrophages. Blood 2004, 104:4038.
22. Hise A.G., Tomalka J., Ganesan S., Patel K., Hall B.A., Brown G.D., Fitzgerald K.A. An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 2009, 5:487.
23. Joly S., Ma N., Sadler J.J., Soll D.R., Cassel S.L., Sutterwala F.S. Cutting edge: Candida albicans hyphae formation triggers activation of the Nlrp3 inflammasome. J. Immunol. 2009, 183:3578.
24. Kawakami T., Ando T., Kimura M., Wilson B.S., Kawakami Y. Mast cells in atopic dermatitis. Curr. Opin. Immunol. 2009, 21:666.
25. Ketavarapu J.M., Rodriguez A.R., Yu J.J., Cong Y., Murthy A.K., Forsthuber T.G., Guentzel M.N., Klose K.E., Berton M.T., Arulanandam B.P. Mast cells inhibit intramacrophage Francisella tularensis replication via contact and secreted products including IL-4. Proc. Natl Acad. Sci. U.S.A. 2008, 105:9313.
26. Knight P.A., Wright S.H., Lawrence C.E., Paterson Y.Y., Miller H.R. Delayed expulsion of the nematode Trichinella spiralis in mice lacking the mucosal mast cell-specific granule chymase, mouse mast cell protease-1. J. Exp. Med. 2000, 192:1849.
27. LeibundGut-Landmann S., Gross O., Robinson M.J., Osorio F., Slack E.C., Tsoni S.V., Schweighoffer E., Tybulewicz V., Brown G.D., Ruland J., Reis e Sousa C. Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 2007, 8:630.
28. Lin T.J., Garduno R., Boudreau R.T., Issekutz A.C. Pseudomonas aeruginosa activates human mast cells to induce neutrophil transendothelial migration via mast cell-derived IL-1 alpha and beta. J. Immunol. 2002, 169:4522.
29. Malaviya R., Ikeda T., Ross E., Abraham S.N. Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNF-alpha. Nature 1996, 381:77.
30. Maurer M., Lopez Kostka S., Siebenhaar F., Moelle K., Metz M., Knop J., von Stebut E. Skin mast cells control T cell-dependent host defense in Leishmania major infections. FASEB J. 2006, 20:2460.
31. Miramon P., Kasper L., Hube B. Thriving within the host: Candida spp. interactions with phagocytic cells. Med. Microbiol. Immunol. 2013, 202:183.
32. Nakamura Y., Kambe N., Saito M., Nishikomori R., Kim Y.G., Murakami M., Nunez G., Matsue H. Mast cells mediate neutrophil recruitment and vascular leakage through the NLRP3 inflammasome in histamine-independent urticaria. J. Exp. Med. 2009, 206:1037.
33. Netea M.G., Brown G.D., Kullberg B.J., Gow N.A. An integrated model of the recognition of Candida albicans by the innate immune system. Nat. Rev. Microbiol. 2008, 6:67.
34. Netea M.G., Sutmuller R., Hermann C., Van der Graaf C.A., Van der Meer J.W., van Krieken J.H., Hartung T., Adema G., Kullberg B.J. Toll-like receptor 2 suppresses immunity against Candida albicans through induction of IL-10 and regulatory T cells. J. Immunol. 2004, 172:3712.
35. Netea M.G., Van Der Graaf C.A., Vonk A.G., Verschueren I., Van Der Meer J.W., Kullberg B.J. The role of toll-like receptor (TLR) 2 and TLR4 in the host defense against disseminated candidiasis. J. Infect Dis. 2002, 185:1483.
36. Nosal R., Novotny J., Sikl D. The effect of glycoprotein from Candida albicans on isolated rat mast cells. Toxicon 1974, 12:103.
37. Olynych T.J., Jakeman D.L., Marshall J.S. Fungal zymosan induces leukotriene production by human mast cells through a dectin-1-dependent mechanism. J. Allergy Clin. Immunol. 2006, 118:837.
38. Palma A.S., Feizi T., Zhang Y., Stoll M.S., Lawson A.M., Diaz-Rodriguez E., Campanero-Rhodes M.A., Costa J., Gordon S., Brown G.D., Chai W. Ligands for the beta-glucan receptor, Dectin-1, assigned using designer microarrays of oligosaccharide probes (neoglycolipids) generated from glucan polysaccharides. J. Biol. Chem. 2006, 281:5771.
39. Rogers N.C., Slack E.C., Edwards A.D., Nolte M.A., Schulz O., Schweighoffer E., Williams D.L., Gordon S., Tybulewicz V.L., Brown G.D., Reis e Sousa C. Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 2005, 22:507.
40. Romo-Lozano Y., Hernandez-Hernandez F., Salinas E. Mast cell activation by conidia of Sporothrix schenckii: role in the severity of infection. Scand. J. Immunol. 2012, 76:11.
41. Romo-Lozano Y., Hernandez-Hernandez F., Salinas E. Sporothrix schenckii yeasts induce ERK pathway activation and secretion of IL-6 and TNF-alpha in rat mast cells, but no degranulation. Med. Mycol. 2014, 52:862.
42. Saluja R., Metz M., Maurer M. Role and relevance of mast cells in fungal infections. Front Immunol. 2012, 3:146.
43. Selander C., Engblom C., Nilsson G., Scheynius A., Andersson C.L. TLR2/MyD88-dependent and -independent activation of mast cell IgE responses by the skin commensal yeast Malassezia sympodialis. J. Immunol. 2009, 182:4208.
44. Shoham S., Levitz S.M. The immune response to fungal infections. Br. J. Haematol. 2005, 129:569.
45. Skrzypek F., Cenci E., Pietrella D., Rachini A., Bistoni F., Vecchiarelli A. Dectin-1 is required for human dendritic cells to initiate immune response to Candida albicans through Syk activation. Microbes Infect. 2009, 11:661.
46. St John A.L., Abraham S.N. Innate immunity and its regulation by mast cells. J. Immunol. 2013, 190:4458.
47. St John A.L., Rathore A.P., Yap H., Ng M.L., Metcalfe D.D., Vasudevan S.G., Abraham S.N. Immune surveillance by mast cells during dengue infection promotes natural killer (NK) and NKT-cell recruitment and viral clearance. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:9190.
48. St John A.L., Rathore A.P., Raghavan B., Ng M.L., Abraham S.N. Contributions of mast cells and vasoactive products, leukotrienes and chymase, to dengue virus-induced vascular leakage. Elife 2013, 2:e00481.
49. Sutherland R.E., Olsen J.S., McKinstry A., Villalta S.A., Wolters P.J. Mast cell IL-6 improves survival from Klebsiella pneumonia and sepsis by enhancing neutrophil killing. J. Immunol. 2008, 181:5598.
50. Taylor P.R., Tsoni S.V., Willment J.A., Dennehy K.M., Rosas M., Findon H., Haynes K., Steele C., Botto M., Gordon S., Brown G.D. Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat. Immunol. 2007, 8:31.
51. Trevisan E., Vita F., Medic N., Soranzo M.R., Zabucchi G., Borelli V. Mast cells kill Candida albicans in the extracellular environment but spare ingested fungi from death. Inflammation 2014, 37:2174.
52. Underhill D.M., Rossnagle E., Lowell C.A., Simmons R.M. Dectin-1 activates Syk tyrosine kinase in a dynamic subset of macrophages for reactive oxygen production. Blood 2005, 106:2543.
53. Urb M., Pouliot P., Gravelat F.N., Olivier M., Sheppard D.C. Aspergillus fumigatus induces immunoglobulin E-independent mast cell degranulation. J. Infect. Dis. 2009, 200:464.
54. Wellington M., Dolan K., Krysan D.J. Live Candida albicans suppresses production of reactive oxygen species in phagocytes. Infect. Immun. 2009, 77:405.
55. Woodbury R.G., Miller H.R., Huntley J.F., Newlands G.F., Palliser A.C., Wakelin D. Mucosal mast cells are functionally active during spontaneous expulsion of intestinal nematode infections in rat. Nature 1984, 312:450.
56. Yang Z., Marshall J.S. Zymosan treatment of mouse mast cells enhances dectin-1 expression and induces dectin-1-dependent reactive oxygen species (ROS) generation. Immunobiology 2009, 214:321.
57. Yepez-Mulia L., Montano-Escalona C., Fonseca-Linan R., Munoz-Cruz S., Arizmendi-Puga N., Boireau P., Ortega-Pierres G. Differential activation of mast cells by antigens from Trichinella spiralis muscle larvae, adults, and newborn larvae. Vet. Parasitol. 2009, 159:253.