The drosophila toll pathway controls but does not clear Candida glabrata infections

Journal of Immunology

Volumn 190, Issue 6, 2013, Pages 2818-2827

  Quintin, Jessica ^a,b   Asmar, Joelle ^a,c   Matskevich, Alexey A ^a,d   Lafarge, Marie Céline ^a   Ferrandon, Dominique ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Cegedim Strategic DataMedical Research ^*  (France)

^d TheraMAB   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; FUNGAL PROTEIN; GLYCEROL; MONOPHENOL MONOOXYGENASE; PATTERN RECOGNITION RECEPTOR; UNCLASSIFIED DRUG; YAPSIN;

ARTICLE; BLOOD CELL; CANDIDA ALBICANS; CANDIDA GLABRATA; CANDIDIASIS; COMPARATIVE STUDY; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME ACTIVATION; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE; GENE ACTIVATION; GNBP3 GENE; HOST PATHOGEN INTERACTION; IMMUNE DEFICIENCY; INFECTION CONTROL; INFECTION SENSITIVITY; NONHUMAN; OSMOLARITY; PERSEPHONE PROTEASE DEPENDENT DETECTION PATHWAY; PRIORITY JOURNAL; PSH GENE; SYSTEMIC DISEASE; SYSTEMS BIOLOGY; TOLL PATHWAY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, DIFFERENTIATION; CANDIDA GLABRATA; CANDIDIASIS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; PHAGOCYTOSIS; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; VIRULENCE;

EID: 84874875545     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201861     Document Type: Article

References (58)

1. Marriott, D. J., E. G. Playford, S. Chen, M. Slavin, Q. Nguyen, D. Ellis, and T. C. Sorrell; Australian Candidaemia Study. 2009. Determinants of mortality in non-neutropenic ICU patients with candidaemia. Crit. Care 13: R115
2. Sipsas, N. V., R. E. Lewis, J. Tarrand, R. Hachem, K. V. Rolston, I. I. Raad, and D. P. Kontoyiannis. 2009. Candidemia in patients with hematologic malignancies in the era of new antifungal agents (2001-2007): stable incidence but changing epidemiology of a still frequently lethal infection. Cancer 115: 4745-4752
3. Pfaller, M. A., G. J. Moet, S. A. Messer, R. N. Jones, and M. Castanheira. 2011. Geographic variations in species distribution and echinocandin and azole antifungal resistance rates among Candida bloodstream infection isolates: report from the SENTRY Antimicrobial Surveillance Program (2008 to 2009). J. Clin. Microbiol. 49: 396-399
4. Pfaller, M. A., S. A. Messer, G. J. Moet, R. N. Jones, and M. Castanheira. 2011. Candida bloodstream infections: comparison of species distribution and resistance to echinocandin and azole antifungal agents in Intensive Care Unit (ICU) and non-ICU settings in the SENTRY Antimicrobial Surveillance Program (2008-2009). Int. J. Antimicrob. Agents 38: 65-69
5. Pfaller, M. A., S. A. Messer, L. Boyken, C. Rice, S. Tendolkar, R. J. Hollis, and D. J. Diekema. 2003. Caspofungin activity against clinical isolates of fluconazole-resistant Candida. J. Clin. Microbiol. 41: 5729-5731
6. Barns, S. M., D. J. Lane, M. L. Sogin, C. Bibeau, and W. G. Weisburg. 1991. Evolutionary relationships among pathogenic Candida species and relatives. J. Bacteriol. 173: 2250-2255
7. Gow, N. A., F. L. van de Veerdonk, A. J. Brown, and M. G. Netea. 2012. Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat. Rev. Microbiol. 10: 112-122
8. Kaur, R., B.Ma, and B. P. Cormack. 2007. A family of glycosylphosphatidylinositollinked aspartyl proteases is required for virulence of Candida glabrata. Proc. Natl. Acad. Sci. USA 104: 7628-7633
9. Cormack, B. P., N. Ghori, and S. Falkow. 1999. An adhesin of the yeast pathogen Candida glabrata mediating adherence to human epithelial cells. Science 285: 578-582
10. Seider, K., S. Brunke, L. Schild, N. Jablonowski, D. Wilson, O. Majer, D. Barz, A. Haas, K. Kuchler, M. Schaller, and B. Hube. 2011. The facultative intracellular pathogen Candida glabrata subverts macrophage cytokine production and phagolysosome maturation. J. Immunol. 187: 3072-3086
11. Tsoni, S. V., A. M. Kerrigan, M. J. Marakalala, N. Srinivasan, M. Duffield, P. R. Taylor, M. Botto, C. Steele, and G. D. Brown. 2009. Complement C3 plays an essential role in the control of opportunistic fungal infections. Infect. Immun. 77: 3679-3685
12. Bourgeois, C., O. Majer, I. E. Frohner, I. Lesiak-Markowicz, K. S. Hildering, W. Glaser, S. Stockinger, T. Decker, S. Akira, M. Müller, and K. Kuchler. 2011. Conventional dendritic cells mount a type I IFN response against Candida spp. requiring novel phagosomal TLR7-mediated IFN-β signaling. J. Immunol. 186: 3104-3112
13. Jawhara, S., E. Mogensen, F. Maggiotto, C. Fradin, A. Sarazin, L. Dubuquoy, E. Maes, Y. Guérardel, G. Janbon, and D. Poulain. 2012. Murine model of dextran sulfate sodium-induced colitis reveals Candida glabrata virulence and contribution of b-mannosyltransferases. J. Biol. Chem. 287: 11313-11324
14. Chen, Y. L., J. H. Konieczka, D. J. Springer, S. E. Bowen, J. Zhang, F. G. Silao, A. A. Bungay, U. G. Bigol, M. G. Nicolas, S. N. Abraham, et al. 2012. Convergent evolution of calcineurin pathway roles in thermotolerance and virulence in Candida glabrata. G3 (Bethesda) 2: 675-691
15. Mylonakis, E., F. M. Ausubel, R. J. Tang, and S. B. Calderwood. 2003. The art of serendipity: killing of Caenorhabditis elegans by human pathogens as a model of bacterial and fungal pathogenesis. Expert Rev. Anti Infect. Ther. 1: 167-173
16. Pukkila-Worley, R., E. Holson, F. Wagner, and E. Mylonakis. 2009. Antifungal drug discovery through the study of invertebrate model hosts. Curr. Med. Chem. 16: 1588-1595
17. Limmer, S., J. Quintin, C. Hetru, and D. Ferrandon. 2011. Virulence on the fly: Drosophila melanogaster as a model genetic organism to decipher host-pathogen interactions. Curr. Drug Targets 12: 978-999
18. Alarco, A. M., A. Marcil, J. Chen, B. Suter, D. Thomas, and M. Whiteway. 2004. Immune-deficient Drosophila melanogaster: a model for the innate immune response to human fungal pathogens. J. Immunol. 172: 5622-5628
19. Chamilos, G., M. S. Lionakis, R. E. Lewis, J. L. Lopez-Ribot, S. P. Saville, N. D. Albert, G. Halder, and D. P. Kontoyiannis. 2006. Drosophila melanogaster as a facile model for large-scale studies of virulence mechanisms and antifungal drug efficacy in Candida species. J. Infect. Dis. 193: 1014-1022
20. Glittenberg, M. T., S. Silas, D. M. MacCallum, N. A. Gow, and P. Ligoxygakis. 2011. Wild-type Drosophila melanogaster as an alternative model system for investigating the pathogenicity of Candida albicans. Dis. Model. Mech. 4: 504-514
21. Lemaitre, B., E. Nicolas, L. Michaut, J. M. Reichhart, and J. A. Hoffmann. 1996. The dorsoventral regulatory gene cassette spätzle/Toll/ cactus controls the potent antifungal response in Drosophila adults. Cell 86: 973-983
22. Gottar, M., V. Gobert, A. A. Matskevich, J. M. Reichhart, C. Wang, T. M. Butt, M. Belvin, J. A. Hoffmann, and D. Ferrandon. 2006. Dual detection of fungal infections in Drosophila via recognition of glucans and sensing of virulence factors. Cell 127: 1425-1437
23. Jang, I. H., N. Chosa, S. H. Kim, H. J. Nam, B. Lemaitre, M. Ochiai, Z. Kambris, S. Brun, C. Hashimoto, M. Ashida, et al. 2006. A Spätzle- processing enzyme required for toll signaling activation in Drosophila innate immunity. Dev. Cell 10: 45-55
24. Mishima, Y., J. Quintin, V. Aimanianda, C. Kellenberger, F. Coste, C. Clavaud, C. Hetru, J. A. Hoffmann, J. P. Latgé, D. Ferrandon, and A. Roussel. 2009. The N-terminal domain of Drosophila Gram-negative binding protein 3 (GNBP3) defines a novel family of fungal pattern recognition receptors. J. Biol. Chem. 284: 28687-28697
25. Ligoxygakis, P., N. Pelte, J. A. Hoffmann, and J. M. Reichhart. 2002. Activation of Drosophila Toll during fungal infection by a blood serine protease. Science 297: 114-116
26. Chosa, N., T. Fukumitsu, K. Fujimoto, and E. Ohnishi. 1997. Activation of prophenoloxidase A1 by an activating enzyme in Drosophila melanogaster. Insect Biochem. Mol. Biol. 27: 61-68
27. De Gregorio, E., S. J. Han, W. J. Lee, M. J. Baek, T. Osaki, S. Kawabata, B. L. Lee, S. Iwanaga, B. Lemaitre, and P. T. Brey. 2002. An immune-responsive Serpin regulates the melanization cascade in Drosophila. Dev. Cell 3: 581-592
28. Ligoxygakis, P., N. Pelte, C. Ji, V. Leclerc, B. Duvic, M. Belvin, H. Jiang, J. A. Hoffmann, and J. M. Reichhart. 2002. A serpin mutant links Toll activation to melanization in the host defence of Drosophila. EMBO J. 21: 6330-6337
29. Tang, H., Z. Kambris, B. Lemaitre, and C. Hashimoto. 2006. Two proteases defining a melanization cascade in the immune system of Drosophila. J. Biol. Chem. 281: 28097-28104
30. Matskevich, A. A., J. Quintin, and D. Ferrandon. 2010. The Drosophila PRR GNBP3 assembles effector complexes involved in antifungal defenses independently of its Toll-pathway activation function. Eur. J. Immunol. 40: 1244-1254
31. Rutschmann, S., A. C. Jung, C. Hetru, J.-M. Reichhart, J. A. Hoffmann, and D. Ferrandon. 2000. The Rel protein DIF mediates the antifungal but not the antibacterial host defense in Drosophila. Immunity 12: 569-580
32. Rutschmann, S., A. Kilinc, and D. Ferrandon. 2002. Cutting edge: the Toll pathway is required for resistance to gram-positive bacterial infections in Drosophila. J. Immunol. 168: 1542-1546
33. Gobert, V., M. Gottar, A. A. Matskevich, S. Rutschmann, J. Royet, M. Belvin, J. A. Hoffmann, and D. Ferrandon. 2003. Dual activation of the Drosophila Toll pathway by two pattern recognition receptors. Science 302: 2126-2130
34. Gottar, M., V. Gobert, T. Michel, M. Belvin, G. Duyk, J. A. Hoffmann, D. Ferrandon, and J. Royet. 2002. The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature 416: 640-644
35. Leclerc, V., N. Pelte, L. El Chamy, C. Martinelli, P. Ligoxygakis, J. A. Hoffmann, and J. M. Reichhart. 2006. Prophenoloxidase activation is not required for survival to microbial infections in Drosophila. EMBO Rep. 7: 231-235
36. Tauszig-Delamasure, S., H. Bilak, M. Capovilla, J. A. Hoffmann, and J. L. Imler. 2002. Drosophila MyD88 is required for the response to fungal and Grampositive bacterial infections. Nat. Immunol. 3: 91-97
37. Elrod-Erickson, M., S. Mishra, and D. Schneider. 2000. Interactions between the cellular and humoral immune responses in Drosophila. Curr. Biol. 10: 781-784
38. Meng, X., B. S. Khanuja, and Y. T. Ip. 1999. Toll receptor-mediated Drosophila immune response requires Dif, an NF-kappaB factor. Genes Dev. 13: 792-797
39. Manfruelli, P., J. M. Reichhart, R. Steward, J. A. Hoffmann, and B. Lemaitre. 1999. A mosaic analysis in Drosophila fat body cells of the control of antimicrobial peptide genes by the Rel proteins Dorsal and DIF. EMBO J. 18: 3380-3391
40. Rutschmann, S., A. C. Jung, R. Zhou, N. Silverman, J. A. Hoffmann, and D. Ferrandon. 2000. Role of Drosophila IKK γ in a toll-independent antibacterial immune response. Nat. Immunol. 1: 342-347
41. Yáñez, A. M., C. Murciano, S. Llopis, T. Fernández-Espinar, M. L. Gil, and D. Gozalbo. 2009. In vivo and in vitro studies on virulence and host responses to Saccharomyces cerevisiae clinical and non-clinical isolates. Open Mycol. J. 3: 37-47
42. Lemaitre, B., J. M. Reichhart, and J. A. Hoffmann. 1997. Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc. Natl. Acad. Sci. USA 94: 14614-14619
43. Domergue, R., I. Castaño, A. De Las Peñas, M. Zupancic, V. Lockatell, J. R. Hebel, D. Johnson, and B. P. Cormack. 2005. Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 308: 866-870
44. Ma, B., S. J. Pan, M. L. Zupancic, and B. P. Cormack. 2007. Assimilation of NAD(+) precursors in Candida glabrata. Mol. Microbiol. 66: 14-25
45. Gregori, C., C. Schüller, A. Roetzer, T. Schwarzmüller, G. Ammerer, and K. Kuchler. 2007. The high-osmolarity glycerol response pathway in the human fungal pathogen Candida glabrata strain ATCC 2001 lacks a signaling branch that operates in baker's yeast. Eukaryot. Cell 6: 1635-1645
46. Apidianakis, Y., L. G. Rahme, J. Heitman, F. M. Ausubel, S. B. Calderwood, and E. Mylonakis. 2004. Challenge of Drosophila melanogaster with Cryptococcus neoformans and role of the innate immune response. Eukaryot. Cell 3: 413-419
47. Jacobsen, I. D., S. Brunke, K. Seider, T. Schwarzmüller, A. Firon, C. d'Enfért, K. Kuchler, and B. Hube. 2010. Candida glabrata persistence in mice does not depend on host immunosuppression and is unaffected by fungal amino acid auxotrophy. Infect. Immun. 78: 1066-1077
48. Fehlbaum, P., P. Bulet, L. Michaut, M. Lagueux, W. F. Broekaert, C. Hetru, and J. A. Hoffmann. 1994. Insect immunity. Septic injury of Drosophila induces the synthesis of a potent antifungal peptide with sequence homology to plant antifungal peptides. J. Biol. Chem. 269: 33159-33163
49. Levashina, E. A., S. Ohresser, P.Bulet, J.-M. Reichhart, C. Hétru, and J. A. Hoffmann. 1995. Metchnikowin, a novel immune-inducible proline-rich peptide from Drosophila with antibacterial and antifungal properties. Eur. J. Biochem. 233: 694-700
50. Lamberty, M., S. Ades, S. Uttenweiler-Joseph, G. Brookhart, D. Bushey, J. A. Hoffmann, and P. Bulet. 1999. Insect immunity. Isolation from the lepidopteran Heliothis virescens of a novel insect defensin with potent antifungal activity. J. Biol. Chem. 274: 9320-9326
51. Lamberty, M., D. Zachary, R. Lanot, C. Bordereau, A. Robert, J. A. Hoffmann, and P. Bulet. 2001. Insect immunity. Constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect. J. Biol. Chem. 276: 4085-4092
52. Ekengren, S., and D. Hultmark. 1999. Drosophila cecropin as an antifungal agent. Insect Biochem. Mol. Biol. 29: 965-972
53. Dolmetsch, R. E., R. S. Lewis, C. C. Goodnow, and J. I. Healy. 1997. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 386: 855-858
54. Shia, A. K., M. Glittenberg, G. Thompson, A. N. Weber, J. M. Reichhart, and P. Ligoxygakis. 2009. Toll-dependent antimicrobial responses in Drosophila larval fat body require Spätzle secreted by haemocytes. J. Cell Sci. 122: 4505-4515
55. Limmer, S., S. Haller, E. Drenkard, J. Lee, S. Yu, C. Kocks, F. M. Ausubel, and D. Ferrandon. 2011. Pseudomonas aeruginosa RhlR is required to neutralize the cellular immune response in a Drosophila melanogaster oral infection model. Proc. Natl. Acad. Sci. USA 108: 17378-17383
56. Cuéllar-Cruz, M., M. Briones-Martin-del-Campo, I. Cañas-Villamar, J. Montalvo- Arredondo, L. Riego-Ruiz, I. Castaño, and A. De Las Peñas. 2008. High resistance to oxidative stress in the fungal pathogen Candida glabrata is mediated by a single catalase, Cta1p, and is controlled by the transcription factors Yap1p, Skn7p, Msn2p, and Msn4p. Eukaryot. Cell 7: 814-825
57. Zhou, P., and D. J. Thiele. 1993. Rapid transcriptional autoregulation of a yeast metalloregulatory transcription factor is essential for high-level copper detoxification. Genes Dev. 7: 1824-1835
58. Bahn, Y. S., K. Kojima, G. M. Cox, and J. Heitman. 2005. Specialization of the HOG pathway and its impact on differentiation and virulence of Cryptococcus neoformans. Mol. Biol. Cell 16: 2285-2300