The facultative intracellular pathogen Candida glabrata subverts macrophage cytokine production and phagolysosome maturation

Journal of Immunology

Volumn 187, Issue 6, 2011, Pages 3072-3086

  Seider, Katja ^a   Brunke, Sascha ^a,b   Schild, Lydia ^a   Jablonowski, Nadja ^a   Wilson, Duncan ^a   Majer, Olivia ^c   Barz, Dagmar ^b   Haas, Albert ^d   Kuchler, Karl ^c   Schaller, Martin ^e   Hube, Bernhard ^a,f  

^a HANS KNÖLL INSTITUTE   (Germany)

^b JENA UNIVERSITY HOSPITAL   (Germany)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

^d UNIVERSITY OF BONN   (Germany)

^e UNIVERSITY OF TÜBINGEN   (Germany)

^f FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN D; CYTOKINE; EARLY ENDOSOME ANTIGEN 1; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; REACTIVE OXYGEN METABOLITE;

ACIDIFICATION; ANTIMICROBIAL ACTIVITY; APOPTOSIS; ARTICLE; BIOGENESIS; CANDIDA GLABRATA; CELL ADHESION; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOSOME; FUNGAL VIABILITY; HEAT SENSITIVITY; HUMAN; HUMAN CELL; INTERNALIZATION; MACROPHAGE; MONOCYTE; NONHUMAN; PHAGOLYSOSOME; PHAGOSOME; PRIORITY JOURNAL; YEAST;

APOPTOSIS; CANDIDA GLABRATA; CANDIDIASIS; CYTOKINES; HUMANS; IMMUNE EVASION; MACROPHAGES; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHAGOSOMES; POLYMERASE CHAIN REACTION;

EID: 80053077071     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003730     Document Type: Article

References (78)

1. Kaur, R., R. Domergue, M. L. Zupancic, and B. P. Cormack. 2005. A yeast by any other name: Candida glabrata and its interaction with the host. Curr. Opin. Microbiol. 8: 378-384. (Pubitemid 41021896)
2. Pfaller, M. A., and D. J. Diekema. 2007. Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20: 133-163. (Pubitemid 46167771)
3. Pfaller, M. A., D. J. Diekema; International Fungal Surveillance Participant Group. 2004. Twelve years of fluconazole in clinical practice: global trends in species distribution and fluconazole susceptibility of bloodstream isolates of Candida. Clin. Microbiol. Infect. 10(Suppl. 1): 11-23. (Pubitemid 38386593)
4. Calderone, R. A., and W. A. Fonzi. 2001. Virulence factors of Candida albicans. Trends Microbiol. 9: 327-335. (Pubitemid 32575277)
5. Whiteway, M., and C. Bachewich. 2007. Morphogenesis in Candida albicans. Annu. Rev. Microbiol. 61: 529-553. (Pubitemid 350058220)
6. Zhu, W., and S. G. Filler. 2010. Interactions of Candida albicans with epithelial cells. Cell. Microbiol. 12: 273-282.
7. 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.
8. Brieland, J., D. Essig, C. Jackson, D. Frank, D. Loebenberg, F. Menzel, B. Arnold, B. DiDomenico, and R. Hare. 2001. Comparison of pathogenesis and host immune responses to Candida glabrata and Candida albicans in systemically infected immunocompetent mice. Infect. Immun. 69: 5046-5055. (Pubitemid 32674490)
9. Arendrup, M., T. Horn, and N. Frimodt-Møller. 2002. In vivo pathogenicity of eight medically relevant Candida species in an animal model. Infection 30: 286-291.
10. Otto, V., and D. H. Howard. 1976. Further studies on the intracellular behavior of Torulopsis glabrata. Infect. Immun. 14: 433-438.
11. Kaur, R., B. Ma, and B. P. Cormack. 2007. A family of glycosylphosphatidylinositol- linked aspartyl proteases is required for virulence of Candida glabrata. Proc. Natl. Acad. Sci. USA 104: 7628-7633. (Pubitemid 47185957)
12. Roetzer, A., N. Gratz, P. Kovarik, and C. Schüller. 2010. Autophagy supports Candida glabrata survival during phagocytosis. Cell. Microbiol. 12: 199-216.
13. Vieira, O. V., R. J. Botelho, and S. Grinstein. 2002. Phagosome maturation: aging gracefully. Biochem. J. 366: 689-704.
14. Haas, A. 2007. The phagosome: compartment with a license to kill. Traffic 8: 311-330. (Pubitemid 46421614)
15. Seider, K., A. Heyken, A. Lüttich, P. Miramón, and B. Hube. 2010. Interaction of pathogenic yeasts with phagocytes: survival, persistence and escape. Curr. Opin. Microbiol. 13: 392-400.
16. Webster, R. H., and A. Sil. 2008. Conserved factors Ryp2 and Ryp3 control cell morphology and infectious spore formation in the fungal pathogen Histoplasma capsulatum. Proc. Natl. Acad. Sci. USA 105: 14573-14578.
17. Eissenberg, L. G., W. E. Goldman, and P. H. Schlesinger. 1993. Histoplasma capsulatum modulates the acidification of phagolysosomes. J. Exp. Med. 177: 1605-1611. (Pubitemid 23146127)
18. Strasser, J. E., S. L. Newman, G. M. Ciraolo, R. E. Morris, M. L. Howell, and G. E. Dean. 1999. Regulation of the macrophage vacuolar ATPase and phagosome-lysosome fusion by Histoplasma capsulatum. J. Immunol. 162: 6148-6154. (Pubitemid 29314976)
19. Marcil, A., D. Harcus, D. Y. Thomas, and M. Whiteway. 2002. Candida albicans killing by RAW 264.7 mouse macrophage cells: effects of Candida genotype, infection ratios, and g interferon treatment. Infect. Immun. 70: 6319-6329. (Pubitemid 35192724)
20. Fernández-Arenas, E., C. K. Bleck, C. Nombela, C. Gil, G. Griffiths, and R. Diez-Orejas. 2009. Candida albicans actively modulates intracellular membrane trafficking in mouse macrophage phagosomes. Cell. Microbiol. 11: 560-589.
21. Wellington, M., K. Dolan, and D. J. Krysan. 2009. Live Candida albicans suppresses production of reactive oxygen species in phagocytes. Infect. Immun. 77: 405-413.
22. d'Ostiani, C. F., G. Del Sero, A. Bacci, C. Montagnoli, A. Spreca, A. Mencacci, P. Ricciardi-Castagnoli, and L. Romani. 2000. Dendritic cells discriminate between yeasts and hyphae of the fungus Candida albicans: implications for initiation of T helper cell immunity in vitro and in vivo. J. Exp. Med. 191: 1661-1674.
23. Van der Graaf, C. A., M. G. Netea, I. Verschueren, J. W. Van der Meer, and B. J. Kullberg. 2005. Differential cytokine production and Toll-like receptor signaling pathways by Candida albicans blastoconidia and hyphae. Infect. Immun. 73: 7458-7464. (Pubitemid 41587650)
24. Villena, S. N., R. O. Pinheiro, C. S. Pinheiro, M. P. Nunes, C. M. Takiya, G. A. DosReis, J. O. Previato, L. Mendonça-Previato, and C. G. Freire-de-Lima. 2008. Capsular polysaccharides galactoxylomannan and glucuronoxylomannan from Cryptococcus neoformans induce macrophage apoptosis mediated by Fas ligand. Cell. Microbiol. 10: 1274-1285. (Pubitemid 351663919)
25. Alvarez, M., and A. Casadevall. 2006. Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr. Biol. 16: 2161-2165. (Pubitemid 44692112)
26. Ma, H., J. E. Croudace, D. A. Lammas, and R. C. May. 2006. Expulsion of live pathogenic yeast by macrophages. Curr. Biol. 16: 2156-2160. (Pubitemid 44692099)
27. Dujon, B., D. Sherman, G. Fischer, P. Durrens, S. Casaregola, I. Lafontaine, J. De Montigny, C. Marck, C. Neuvéglise, E. Talla, et al. 2004. Genome evolution in yeasts. Nature 430: 35-44. (Pubitemid 38915217)
28. Gillum, A. M., E. Y. Tsay, and D. R. Kirsch. 1984. Isolation of the Candida albicans gene for orotidine-59-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol. Gen. Genet. 198: 179-182. (Pubitemid 15180998)
29. Haarer, B. K., A. H. Helfant, S. A. Nelson, J. A. Cooper, and D. C. Amberg. 2007. Stable preanaphase spindle positioning requires Bud6p and an apparent interaction between the spindle pole bodies and the neck. Eukaryot. Cell 6: 797-807. (Pubitemid 46835043)
30. Roetzer, A., C. Gregori, A. M. Jennings, J. Quintin, D. Ferrandon, G. Butler, K. Kuchler, G. Ammerer, and C. Schüller. 2008. Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors. Mol. Microbiol. 69: 603-620. (Pubitemid 351962559)
31. Ohkuma, S., and B. Poole. 1978. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc. Natl. Acad. Sci. USA 75: 3327-3331. (Pubitemid 8389720)
32. Brunke, S., K. Seider, R. S. Almeida, A. Heyken, C. B. Fleck, M. Brock, D. Barz, S. Rupp, and B. Hube. 2010. Candida glabrata tryptophan-based pigment production via the Ehrlich pathway. Mol. Microbiol. 76: 25-47.
33. Navarre, W. W., and A. Zychlinsky. 2000. Pathogen-induced apoptosis of macrophages: a common end for different pathogenic strategies. Cell. Microbiol. 2: 265-273. (Pubitemid 30612936)
34. Ibata-Ombetta, S., T. Idziorek, P. A. Trinel, D. Poulain, and T. Jouault. 2003. Role of phospholipomannan in Candida albicans escape from macrophages and induction of cell apoptosis through regulation of bad phosphorylation. Ann. N. Y. Acad. Sci. 1010: 573-576. (Pubitemid 38265048)
35. Chae, H. J., J. S. Kang, J. O. Byun, K. S. Han, D. U. Kim, S. M. Oh, H. M. Kim, S. W. Chae, and H. R. Kim. 2000. Molecular mechanism of staurosporine-induced apoptosis in osteoblasts. Pharmacol. Res. 42: 373-381.
36. Dongari-Bagtzoglou, A., and P. L. Fidel Jr. 2005. The host cytokine responses and protective immunity in oropharyngeal candidiasis. J. Dent. Res. 84: 966-977. (Pubitemid 43828140)
37. Villar, C. C., and A. Dongari-Bagtzoglou. 2008. Immune defence mechanisms and immunoenhancement strategies in oropharyngeal candidiasis. Expert Rev. Mol. Med. 10: e29.
38. Schaller, M., R. Mailhammer, G. Grassl, C. A. Sander, B. Hube, and H. C. Korting. 2002. Infection of human oral epithelia with Candida species induces cytokine expression correlated to the degree of virulence. J. Invest. Dermatol. 118: 652-657. (Pubitemid 34309985)
39. Li, L., H. Kashleva, and A. Dongari-Bagtzoglou. 2007. Cytotoxic and cytokine-inducing properties of Candida glabrata in single and mixed oral infection models. Microb. Pathog. 42: 138-147. (Pubitemid 46551640)
40. + T cells induced by a superantigen: roles of antigen-presenting cells and cytokines. Immunology 81: 513-520.
41. Dahlgren, C., A. Karlsson, and J. Bylund. 2007. Measurement of respiratory burst products generated by professional phagocytes. Methods Mol. Biol. 412: 349-363.
42. Bellaire, B. H., R. M. Roop, II, and J. A. Cardelli. 2005. Opsonized virulent Brucella abortus replicates within nonacidic, endoplasmic reticulum-negative, LAMP-1-positive phagosomes in human monocytes. Infect. Immun. 73: 3702-3713. (Pubitemid 40745915)
43. Von Bargen, K., and A. Haas. 2009. Molecular and infection biology of the horse pathogen Rhodococcus equi. FEMS Microbiol. Rev. 33: 870-891.
44. Newman, S. L., L. Gootee, J. Hilty, and R. E. Morris. 2006. Human macrophages do not require phagosome acidification to mediate fungistatic/fungicidal activity against Histoplasma capsulatum. J. Immunol. 176: 1806-1813. (Pubitemid 43134325)
45. Aboussekhra, A., and R. D. Wood. 1994. Repair of UV-damaged DNA by mammalian cells and Saccharomyces cerevisiae. Curr. Opin. Genet. Dev. 4: 212-220. (Pubitemid 24114852)
46. Dalle, F., B. Wachtler, C. L'Ollivier, G. Holland, N. Bannert, D. Wilson, C. Labruere, A. Bonnin, and B. Hube. 2010. Cellular interactions of Candida albicans with human oral epithelial cells and enterocytes. Cell. Microbiol. 12: 248-271.
47. Anaissie, E. J., J. H. Rex, O. Uzun, and S. Vartivarian. 1998. Predictors of adverse outcome in cancer patients with candidemia. Am. J. Med. 104: 238-245. (Pubitemid 28163168)
48. McNeil, M. M., S. L. Nash, R. A. Hajjeh, M. A. Phelan, L. A. Conn, B. D. Plikaytis, and D. W. Warnock. 2001. Trends in mortality due to invasive mycotic diseases in the United States, 1980-1997. Clin. Infect. Dis. 33: 641-647. (Pubitemid 32762937)
49. Haynes, K. 2001. Virulence in Candida species. Trends Microbiol. 9: 591-596. (Pubitemid 33135415)
50. Maró di, L., S. Schreiber, D. C. Anderson, R. P. MacDermott, H. M. Korchak, and R. B. Johnston Jr. 1993. Enhancement of macrophage candidacidal activity by interferon-g: increased phagocytosis, killing, and calcium signal mediated by a decreased number of mannose receptors. J. Clin. Invest. 91: 2596-2601.
51. Brummer, E., and D. A. Stevens. 1989. Candidacidal mechanisms of peritoneal macrophages activated with lymphokines or g-interferon. J. Med. Microbiol. 28: 173-181. (Pubitemid 19091524)
52. Ghosh, S., D. H. Navarathna, D. D. Roberts, J. T. Cooper, A. L. Atkin, T. M. Petro, and K. W. Nickerson. 2009. Arginine-induced germ tube formation in Candida albicans is essential for escape from murine macrophage line RAW 264.7. Infect. Immun. 77: 1596-1605.
53. Lorenz, M. C., J. A. Bender, and G. R. Fink. 2004. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot. Cell 3: 1076-1087. (Pubitemid 39385215)
54. Medeiros, A. I., V. L. Bonato, A. Malheiro, A. R. Dias, C. L. Silva, and L. H. Faccioli. 2002. Histoplasma capsulatum inhibits apoptosis and Mac-1 expression in leucocytes. Scand. J. Immunol. 56: 392-398.
55. Spellberg, B., A. S. Ibrahim, J. E. Edwards, Jr., and S. G. Filler. 2005. Mice with disseminated candidiasis die of progressive sepsis. J. Infect. Dis. 192: 336-343. (Pubitemid 40993405)
56. Aybay, C., and T. Imir. 1996. Tumor necrosis factor (TNF) induction from monocyte/macrophages by Candida species. Immunobiology 196: 363-374. (Pubitemid 27075953)
57. Li, L., and A. Dongari-Bagtzoglou. 2009. Epithelial GM-CSF induction by Candida glabrata. J. Dent. Res. 88: 746-751.
58. Fradin, C., P. De Groot, D. MacCallum, M. Schaller, F. Klis, F. C. Odds, and B. Hube. 2005. Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol. Microbiol. 56: 397-415. (Pubitemid 40516780)
59. Frohner, I. E., C. Bourgeois, K. Yatsyk, O. Majer, and K. Kuchler. 2009. Candida albicans cell surface superoxide dismutases degrade host-derived reactive oxygen species to escape innate immune surveillance. Mol. Microbiol. 71: 240-252.
60. 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. (Pubitemid 351968825)
61. Chen, K. H., T. Miyazaki, H. F. Tsai, and J. E. Bennett. 2007. The bZip transcription factor Cgap1p is involved in multidrug resistance and required for activation of multidrug transporter gene CgFLR1 in Candida glabrata. Gene 386: 63-72. (Pubitemid 44920447)
62. Cuéllar-Cruz, M., I. Castaño, O. Arroyo-Helguera, and A. De Las Peñas. 2009. Oxidative stress response to menadione and cumene hydroperoxide in the opportunistic fungal pathogen Candida glabrata. Mem. Inst. Oswaldo Cruz 104: 649-654.
63. Donini, M., E. Zenaro, N. Tamassia, and S. Dusi. 2007. NADPH oxidase of human dendritic cells: role in Candida albicans killing and regulation by interferons, dectin-1 and CD206. Eur. J. Immunol. 37: 1194-1203. (Pubitemid 46925304)
64. Goetz, M., A. Bubert, G. Wang, I. Chico-Calero, J. A. Vazquez-Boland, M. Beck, J. Slaghuis, A. A. Szalay, and W. Goebel. 2001. Microinjection and growth of bacteria in the cytosol of mammalian host cells. Proc. Natl. Acad. Sci. USA 98: 12221-12226. (Pubitemid 32959854)
65. Beck, M. R., G. T. Dekoster, D. P. Cistola, and W. E. Goldman. 2009. NMR structure of a fungal virulence factor reveals structural homology with mammalian saposin B. Mol. Microbiol. 72: 344-353.
66. Tucker, S. C., and A. Casadevall. 2002. Replication of Cryptococcus neoformans in macrophages is accompanied by phagosomal permeabilization and accumulation of vesicles containing polysaccharide in the cytoplasm. Proc. Natl. Acad. Sci. USA 99: 3165-3170. (Pubitemid 34240603)
67. Rodrigues, M. L., E. S. Nakayasu, D. L. Oliveira, L. Nimrichter, J. D. Nosanchuk, I. C. Almeida, and A. Casadevall. 2008. Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot. Cell 7: 58-67. (Pubitemid 351959594)
68. Jahn, B., K. Langfelder, U. Schneider, C. Schindel, and A. A. Brakhage. 2002. PKSP-dependent reduction of phagolysosome fusion and intracellular kill of Aspergillus fumigatus conidia by human monocyte-derived macrophages. Cell. Microbiol. 4: 793-803. (Pubitemid 35469667)
69. Spargo, B. J., L. M. Crowe, T. Ioneda, B. L. Beaman, and J. H. Crowe. 1991. Cord factor (a,a-trehalose 6,69-dimycolate) inhibits fusion between phospholipid vesicles. Proc. Natl. Acad. Sci. USA 88: 737-740. (Pubitemid 21916098)
70. Fratti, R. A., J. M. Backer, J. Gruenberg, S. Corvera, and V. Deretic. 2001. Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J. Cell Biol. 154: 631-644. (Pubitemid 34286167)
71. Vergne, I., R. A. Fratti, P. J. Hill, J. Chua, J. Belisle, and V. Deretic. 2004. Mycobacterium tuberculosis phagosome maturation arrest: mycobacterial phosphatidylinositol analog phosphatidylinositol mannoside stimulates early endosomal fusion. Mol. Biol. Cell 15: 751-760. (Pubitemid 38146490)
72. Hybiske, K., and R. S. Stephens. 2008. Exit strategies of intracellular pathogens. Nat. Rev. Microbiol. 6: 99-110.
73. Lo, H. J., J. R. Köhler, B. DiDomenico, D. Loebenberg, A. Cacciapuoti, and G. R. Fink. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939-949. (Pubitemid 27381632)
74. Monod, M., and Z. M. Borg-von. 2002. Secreted aspartic proteases as virulence factors of Candida species. Biol. Chem. 383: 1087-1093. (Pubitemid 35215053)
75. Kantarcioglu, A. S., and A. Yücel. 2002. Phospholipase and protease activities in clinical Candida isolates with reference to the sources of strains. Mycoses 45: 160-165. (Pubitemid 34743920)
76. Ghannoum, M. A. 2000. Potential role of phospholipases in virulence and fungal pathogenesis. Clin. Microbiol. Rev. 13: 122-143. (Pubitemid 30039346)
77. Hybiske, K., and R. S. Stephens. 2007. Mechanisms of host cell exit by the intracellular bacterium Chlamydia. Proc. Natl. Acad. Sci. USA 104: 11430-11435. (Pubitemid 47175157)
78. Horta, M. F. 1997. Pore-forming proteins in pathogenic protozoan parasites. Trends Microbiol. 5: 363-366. (Pubitemid 27374942)