Corticosteroids block autophagy protein recruitment in aspergillus fumigatus phagosomes via targeting dectin-1/Syk Kinase Signaling

Journal of Immunology

Volumn 191, Issue 3, 2013, Pages 1287-1299

  Kyrmizi, Irene ^a,b   Gresnigt, Mark S ^c   Akoumianaki, Tonia ^a   Samonis, George ^a   Sidiropoulos, Prodromos ^a   Boumpas, Dimitrios ^a,b   Netea, Mihai G ^c   Van De Veerdonk, Frank L ^c   Kontoyiannis, Dimitrios P ^d   Chamilos, Georgios ^a,b  

^a UNIVERSITY OF CRETE   (Greece)

^b INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLUCAN; CORTICOSTEROID; DECTIN 1; DECTIN 1 RECEPTOR; LC3 II PROTEIN; LECTIN RECEPTOR; PROTEIN KINASE; PROTEIN KINASE SYK; REACTIVE OXYGEN METABOLITE; REGULATOR PROTEIN; SRC PROTEIN; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; ASPERGILLUS FUMIGATUS; ATG5 GENE; AUTOPHAGY; CELL WALL; CELL WALL SWELLING; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EX VIVO STUDY; FEMALE; FUNGUS GROWTH; FUNGUS SPORE; GENE; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; IN VIVO STUDY; MONOCYTE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN TRANSPORT; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ADRENAL CORTEX HORMONES; AGED; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; AUTOPHAGY; CELLS, CULTURED; FEMALE; GRANULOMATOUS DISEASE, CHRONIC; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LECTINS, C-TYPE; LEUKOCYTES, MONONUCLEAR; MICROTUBULE-ASSOCIATED PROTEINS; MIDDLE AGED; PHAGOSOMES; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 84880668491     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300132     Document Type: Article

References (48)

1. Dagenais, T. R., and N. P. Keller. 2009. Pathogenesis of Aspergillus fumigatus in invasive aspergillosis. Clin. Microbiol. Rev. 22: 447-465.
2. Romani, L. 2011. Immunity to fungal infections. Nat. Rev. Immunol. 11: 275-288.
3. Lionakis, M. S., and D. P. Kontoyiannis. 2003. Glucocorticoids and invasive fungal infections. Lancet 362: 1828-1838.
4. Cornillet, A., C. Camus, S. Nimubona, V. Gandemer, P. Tattevin, C. Belleguic, S. Chevrier, C. Meunier, C. Lebert, M. Aupée, et al. 2006. Comparison of epidemiological, clinical, and biological features of invasive aspergillosis in neutropenic and nonneutropenic patients: a 6-year survey. Clin. Infect. Dis. 43: 577-584.
5. Ader, F., S. Nseir, R. Le Berre, S. Leroy, I. Tillie-Leblond, C. H. Marquette, and A. Durocher. 2005. Invasive pulmonary aspergillosis in chronic obstructive pulmonary disease: an emerging fungal pathogen. Clin. Microbiol. Infect. 11: 427-429.
6. Meersseman, W., K. Lagrou, J. Maertens, and E. Van Wijngaerden. 2007. Invasive aspergillosis in the intensive care unit. Clin. Infect. Dis. 45: 205-216.
7. Schaffner, A., H. Douglas, and A. Braude. 1982. Selective protection against conidia by mononuclear and against mycelia by polymorphonuclear phagocytes in resistance to Aspergillus. Observations on these two lines of defense in vivo and in vitro with human and mouse phagocytes. J. Clin. Invest. 69: 617-631.
8. Waldorf, A. R., S. M. Levitz, and R. D. Diamond. 1984. In vivo bronchoalveolar macrophage defense against Rhizopus oryzae and Aspergillus fumigatus. J. Infect. Dis. 150: 752-760.
9. Ibrahim-Granet, O., B. Philippe, H. Boleti, E. Boisvieux-Ulrich, D. Grenet, M. Stern, and J. P. Latgé. 2003. Phagocytosis and intracellular fate of Aspergillus fumigatus conidia in alveolar macrophages. Infect. Immun. 71: 891-903.
10. Philippe, B., O. Ibrahim-Granet, M. C. Prévost, M. A. Gougerot-Pocidalo, M. Sanchez Perez, A. Van Der Meeren, and J. P. Latgé. 2003. Killing of Aspergillus fumigatus by alveolar macrophages is mediated by reactive oxidant intermediates. Infect. Immun. 71: 3034-3042.
11. Morgenstern, D. E., M. A. Gifford, L. L. Li, C. M. Doerschuk, and M. C. Dinauer. 1997. Absence of respiratory burst in X-linked chronic granulomatous disease mice leads to abnormalities in both host defense and inflammatory response to Aspergillus fumigatus. J. Exp. Med. 185: 207-218.
12. Merkow, L., M. Pardo, S. M. Epstein, E. Verney, and H. Sidransky. 1968. Lysosomal stability during phagocytosis of Aspergillus flavus spores by alveolar macrophages of cortisone-treated mice. Science 160: 79-81.
13. Schaffner, A. 1985. Therapeutic concentrations of glucocorticoids suppress the antimicrobial activity of human macrophages without impairing their responsiveness to gamma interferon. J. Clin. Invest. 76: 1755-1764.
14. Mambula, S. S., K. Sau, P. Henneke, D. T. Golenbock, and S. M. Levitz. 2002. Toll-like receptor (TLR) signaling in response to Aspergillus fumigatus. J. Biol. Chem. 277: 39320-39326.
15. Bellocchio, S., C. Montagnoli, S. Bozza, R. Gaziano, G. Rossi, S. S. Mambula, A. Vecchi, A. Mantovani, S. M. Levitz, and L. Romani. 2004. The contribution of the Toll-like/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J. Immunol. 172: 3059-3069.
16. Drummond, R. A., and G. D. Brown. 2011. The role of Dectin-1 in the host defence against fungal infections. Curr. Opin. Microbiol. 14: 392-399.
17. Goodridge, H. S., A. J. Wolf, and D. M. Underhill. 2009. Beta-glucan recognition by the innate immune system. Immunol. Rev. 230: 38-50.
18. Gringhuis, S. I., B. A. Wevers, T. M. Kaptein, T. M. van Capel, B. Theelen, T. Boekhout, E. C. de Jong, and T. B. Geijtenbeek. 2011. Selective C-Rel activation via Malt1 controls anti-fungal T(H)-17 immunity by dectin-1 and dectin-2. PLoS Pathog. 7: e1001259.
19. Werner, J. L., A. E. Metz, D. Horn, T. R. Schoeb, M. M. Hewitt, L. M. Schwiebert, I. Faro-Trindade, G. D. Brown, and C. Steele. 2009. Requisite role for the dectin-1 beta-glucan receptor in pulmonary defense against Aspergillus fumigatus. J. Immunol. 182: 4938-4946.
20. Ferwerda, B., G. Ferwerda, T. S. Plantinga, J. A. Willment, A. B. van Spriel, H. Venselaar, C. C. Elbers, M. D. Johnson, A. Cambi, C. Huysamen, et al. 2009. Human dectin-1 deficiency and mucocutaneous fungal infections. N. Engl. J. Med. 361: 1760-1767.
21. Cunha, C., M. Di Ianni, S. Bozza, G. Giovannini, S. Zagarella, T. Zelante, C. D'Angelo, A. Pierini, L. Pitzurra, F. Falzetti, et al. 2010. Dectin-1 Y238X polymorphism associates with susceptibility to invasive aspergillosis in hematopoietic transplantation through impairment of both recipient-And donordependent mechanisms of antifungal immunity. Blood 116: 5394-5402.
22. Gringhuis, S. I., J. den Dunnen, M. Litjens, M. van der Vlist, B. Wevers, S. C. Bruijns, and T. B. Geijtenbeek. 2009. Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-kappaB activation through Raf-1 and Syk. Nat. Immunol. 10: 203-213.
23. Sanjuan, M. A., C. P. Dillon, S. W. Tait, S. Moshiach, F. Dorsey, S. Connell, M. Komatsu, K. Tanaka, J. L. Cleveland, S. Withoff, and D. R. Green. 2007. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450: 1253-1257.
24. Huang, J., V. Canadien, G. Y. Lam, B. E. Steinberg, M. C. Dinauer, M. A. Magalhaes, M. Glogauer, S. Grinstein, and J. H. Brumell. 2009. Activation of antibacterial autophagy by NADPH oxidases. Proc. Natl. Acad. Sci. USA 106: 6226-6231.
25. Luo, H., F. Nakatsu, A. Furuno, H. Kato, A. Yamamoto, and H. Ohno. 2006. Visualization of the post-Golgi trafficking of multiphoton photoactivated transferrin receptors. Cell Struct. Funct. 31: 63-75.
26. Wang, H., and J. A. Joseph. 1999. Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic. Biol. Med. 27: 612-616.
27. Aimanianda, V., J. Bayry, S. Bozza, O. Kniemeyer, K. Perruccio, S. R. Elluru, C. Clavaud, S. Paris, A. A. Brakhage, S. V. Kaveri, et al. 2009. Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460: 1117-1121.
28. Hohl, T. M., H. L. Van Epps, A. Rivera, L. A. Morgan, P. L. Chen, M. Feldmesser, and E. G. Pamer. 2005. Aspergillus fumigatus triggers inflammatory responses by stage-specific beta-glucan display. PLoS Pathog. 1: e30.
29. Fontaine, T., C. Simenel, G. Dubreucq, O. Adam, M. Delepierre, J. Lemoine, C. E. Vorgias, M. Diaquin, and J. P. Latgé. 2000. Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J. Biol. Chem. 275: 27594-27607.
30. Persat, F., N. Noirey, J. Diana, M. J. Gariazzo, D. Schmitt, S. Picot, and C. Vincent. 2003. Binding of live conidia of Aspergillus fumigatus activates in vitro-generated human Langerhans cells via a lectin of galactomannan specificity. Clin. Exp. Immunol. 133: 370-377.
31. Serrano-Gómez, D., A. Domínguez-Soto, J. Ancochea, J. A. Jimenez-Heffernan, J. A. Leal, and A. L. Corbí. 2004. Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin mediates binding and internalization of Aspergillus fumigatus conidia by dendritic cells and macrophages. J. Immunol. 173: 5635-5643.
32. Thornton, B. P., V. Vetvicka, M. Pitman, R. C. Goldman, and G. D. Ross. 1996. Analysis of the sugar specificity and molecular location of the beta-glucanbinding lectin site of complement receptor type 3 (CD11b/CD18). J. Immunol. 156: 1235-1246.
33. Ross, G. D., J. A. Cain, and P. J. Lachmann. 1985. Membrane complement receptor type three (CR3) has lectin-like properties analogous to bovine conglutinin as functions as a receptor for zymosan and rabbit erythrocytes as well as a receptor for iC3b. J. Immunol. 134: 3307-3315.
34. Mócsai, A., J. Ruland, and V. L. Tybulewicz. 2010. The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat. Rev. Immunol. 10: 387-402.
35. Underhill, D. M., E. Rossnagle, C. A. Lowell, and R. M. Simmons. 2005. Dectin-1 activates Syk tyrosine kinase in a dynamic subset of macrophages for reactive oxygen production. Blood 106: 2543-2550.
36. Nicola, A. M., P. Albuquerque, L. R. Martinez, R. A. Dal-Rosso, C. Saylor, M. De Jesus, J. D. Nosanchuk, and A. Casadevall. 2012. Macrophage autophagy in immunity to Cryptococcus neoformans and Candida albicans. Infect. Immun. 80: 3065-3076.
37. Marr, K. A., M. Koudadoust, M. Black, and S. A. Balajee. 2001. Early events in macrophage killing of Aspergillus fumigatus conidia: new flow cytometric viability assay. Clin. Diagn. Lab. Immunol. 8: 1240-1247.
38. Löwenberg, M., J. Tuynman, J. Bilderbeek, T. Gaber, F. Buttgereit, S. van Deventer, M. Peppelenbosch, and D. Hommes. 2005. Rapid immunosuppressive effects of glucocorticoids mediated through Lck and Fyn. Blood 106: 1703-1710.
39. Löwenberg, M., A. P. Verhaar, J. Bilderbeek, Jv. Marle, F. Buttgereit, M. P. Peppelenbosch, S. J. van Deventer, and D. W. Hommes. 2006. Glucocorticoids cause rapid dissociation of a T-cell-receptor-Associated protein complex containing LCK and FYN. EMBO Rep. 7: 1023-1029.
40. Kuballa, P., W. M. Nolte, A. B. Castoreno, and R. J. Xavier. 2012. Autophagy and the immune system. Annu. Rev. Immunol. 30: 611-646.
41. Brown, G. D., J. Herre, D. L. Williams, J. A. Willment, A. S. Marshall, and S. Gordon. 2003. Dectin-1 mediates the biological effects of beta-glucans. J. Exp. Med. 197: 1119-1124.
42. Ma, J., C. Becker, C. A. Lowell, and D. M. Underhill. 2012. Dectin-1-triggered recruitment of light chain 3 protein to phagosomes facilitates major histocom-patibility complex class II presentation of fungal-derived antigens. J. Biol. Chem. 287: 34149-34156.
43. Jhingran, A., K. B. Mar, D. K. Kumasaka, S. E. Knoblaugh, L. Y. Ngo, B. H. Segal, Y. Iwakura, C. A. Lowell, J. A. Hamerman, X. Lin, and T. M. Hohl. 2012. Tracing conidial fate and measuring host cell antifungal activity using a reporter of microbial viability in the lung. Cell Rep. 2: 1762-1773.
44. Artavanis-Tsakonas, K., J. C. Love, H. L. Ploegh, and J. M. Vyas. 2006. Recruitment of CD63 to Cryptococcus neoformans phagosomes requires acidification. Proc. Natl. Acad. Sci. USA 103: 15945-15950.
45. Mansour, M. K., J. M. Tam, N. S. Khan, M. Seward, P. J. Davids, S. Puranam, A. Sokolovska, D. B. Sykes, Z. Dagher, C. Becker, et al. 2013. Dectin-1 activation controls maturation of b-1,3-glucan-containing phagosomes. J. Biol. Chem. 288: 16043-16054.
46. Kuma, A., M. Hatano, M. Matsui, A. Yamamoto, H. Nakaya, T. Yoshimori, Y. Ohsumi, T. Tokuhisa, and N. Mizushima. 2004. The role of autophagy during the early neonatal starvation period. Nature 432: 1032-1036.
47. Boelens, J., S. Lust, F. Van Bockstaele, M. Van Gele, A. Janssens, L. Derycke, B. Vanhoecke, J. Philippé, M. Bracke, and F. Offner. 2009. Steroid effects on ZAP-70 and SYK in relation to apoptosis in poor prognosis chronic lymphocytic leukemia. Leuk. Res. 33: 1335-1343.
48. Harr, M. W., K. S. McColl, F. Zhong, J. K. Molitoris, and C. W. Distelhorst. 2010. Glucocorticoids downregulate Fyn and inhibit IP(3)-mediated calcium signaling to promote autophagy in T lymphocytes. Autophagy 6: 912-921.