Chapter 17 : Encounters with Mammalian Cells: Survival Strategies of Species

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This chapter reviews the changes in cellular physiology that follow contact with host cells and the impact of these changes on the host-pathogen interaction. The focus is on , for the simple reason that the vast majority of the published research is on this species. The chapter focuses on the interaction between cells and the most important and relevant mammalian cell types. Reflecting the scope of available literature, the chapter concentrates on interactions with neutrophils and macrophages. Stress responses include reactive oxygen species (ROS), reactive nitrogen species (RNS) and superoxide dismutases (SODs). The chapter focuses on the effectors and their roles in mediating the interaction with host cells. Invasion and endocytosis are terms primarily used to describe the internalization of into normally nonphagocytic cells, mostly endothelial and epithelial cells. A surprising finding from the analysis of macrophagephagocytosed cells was the role of carbon starvation, which represented nearly two-thirds of the genes whose expression changed. The adhesion between cells and phagocytes is primarily driven by receptors on the mammalian cell that recognize carbohydrate moieties on the cell wall, though there are some fungal proteins that mediate adhesion as well.

Citation: Vylkova S, Lorenz M. 2012. Encounters with Mammalian Cells: Survival Strategies of Species, p 261-282. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch17
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Extracellular detoxification of ROS. Depicted are a generic phagocyte producing superoxide, hydrogen peroxide, and NO, opposed with a cell elaborating cell surface and intracellular antioxidant mechanisms (see symbol key). doi:10.1128/9781555817176.ch17.f1

Citation: Vylkova S, Lorenz M. 2012. Encounters with Mammalian Cells: Survival Strategies of Species, p 261-282. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch17
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Mechanisms by which can cross endothelial layers. (A) Endocytosis can be triggered by specific interactions between ALS3 (triangles) and N-cadherin (“Y”), which leads to pseudopod formation and internalization. Hyphal morphogenesis inside the endothelial cell can lead to rupture and escape. (B) Passage between cells by degrading extracellular matrix and tight junctions. Scissors represent secreted proteases. (C) Passage through the host cell. Scissors represent secreted proteases and/or lipases. (D) Transit within phagocytes. A phagocytosed cell crosses the endothelial layer within a migrating phagocyte. Many of these mechanisms are also applicable to interactions with epithelial cells; see reference for greater detail on host epithelial interactions. doi:10.1128/9781555817176.ch17.f2

Citation: Vylkova S, Lorenz M. 2012. Encounters with Mammalian Cells: Survival Strategies of Species, p 261-282. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch17
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morphogenesis and escape following macrophage phagocytosis. A wild-type strain expressing a constitutive ACT1 promoter-GFP construct was incubated with J774A.1 macrophages for the indicated times. Fluorescent images are overlaid onto the phase image to highlight the fungal cells. doi:10.1128/9781555817176.ch17.f3

Citation: Vylkova S, Lorenz M. 2012. Encounters with Mammalian Cells: Survival Strategies of Species, p 261-282. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch17
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1. Abe, S.,, R. Tsunashima,, R. Iijima,, T. Yamada,, N. Maruyama,, T. Hisajima,, Y. Abe,, H. Oshima, and, M. Yamazaki. 2009. Suppression of anti- Candida activity of macrophages by a quorum-sensing molecule, farnesol, through induction of oxidative stress. Microbiol. Immunol. 53: 323330.
2. Alarco, A. M., and, M. Raymond. 1999. The bZip transcription factor Cap1p is involved in multidrug resistance and oxidative stress response in Candida albicans. J. Bacteriol. 181: 700708.
3. Alberti-Segui, C.,, A. J. Morales,, H. Xing,, M. M. Kessler,, D. A. Willins,, K. G. Weinstock,, G. Cottarel,, K. Fechtel, and, B. Rogers. 2004. Identification of potential cell-surface proteins in Candida albicans and investigation of the role of a putative cell-surface glycosidase in adhesion and virulence. Yeast 21: 285302.
4. Albrecht, A.,, A. Felk,, I. Pichova,, J. R. Naglik,, M. Schaller,, P. de Groot,, D. Maccallum,, F. C. Odds,, W. Schafer,, F. Klis,, M. Monod, and, B. Hube. 2006. Glycosylphosphatidylinositol-anchored proteases of Candida albicans target proteins necessary for both cellular processes and host-pathogen interactions. J. Biol. Chem. 281: 688694.
5. Almeida, R. S.,, S. Brunke,, A. Albrecht,, S. Thewes,, M. Laue,, J. E. Edwards,, S. G. Filler, and, B. Hube. 2008. The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog. 4: e1000217.
6. Alonso-Monge, R.,, F. Navarro-Garcia,, G. Molero,, R. Diez-Orejas,, M. Gustin,, J. Pla,, M. Sanchez, and, C. Nom-bela. 1999. Role of the mitogenactivated protein kinase Hog1p in morphogenesis and virulence of Candida albicans. J. Bacteriol. 181: 30583068.
7. Alonso-Monge, R.,, F. Navarro-Garcia,, E. Roman,, A. I. Negredo,, B. Eisman,, C. Nombela, and, J. Pla. 2003. The Hog1 mitogen-activated protein kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans. Eukaryot. Cell 2: 351361.
8. Alvarez-Peral, F. J.,, O. Zaragoza,, Y. Pedreno, and, J. C. Arguelles. 2002. Protective role of trehalose during severe oxidative stress caused by hydrogen peroxide and the adaptive oxidative stress response in Candida albicans. Microbiology 148: 25992606.
9. Andes, D.,, A. Lepak,, A. Pitula,, K. Marchillo, and, J. Clark. 2005. A simple approach for estimating gene expression in Candida albicans directly from a systemic infection site. J. Infect. Dis. 192: 893900.
10. Arguelles, J. C. 2000. Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Arch. Microbiol. 174: 217224.
11. Bailey, D. A.,, P. J. Feldmann,, M. Bovey,, N. A. Gow, and, A. J. Brown. 1996. The Candida albicans HYR1 gene, which is activated in response to hyphal development, belongs to a gene family encoding yeast cell wall proteins. J. Bacteriol. 178: 53535360.
12. Barelle, C. J.,, C. L. Priest,, D. M. Maccallum,, N. A. Gow,, F. C. Odds, and, A. J. Brown. 2006. Niche-specific regulation of central metabolic pathways in a fungal pathogen. Cell. Microbiol. 8: 961971.
13. Barker, K. S.,, H. Park,, Q. T. Phan,, L. Xu,, R. Homayouni,, P. D. Rogers, and, S. G. Filler. 2008. Transcriptome profile of the vascular endothelial cell response to Candida albicans. J. Infect. Dis. 198: 193202.
14. Bates, S.,, J. M. de la Rosa,, D. M. MacCallum,, A. J. Brown,, N. A. Gow, and, F. C. Odds. 2007. Candida albicans Iff11, a secreted protein required for cell wall structure and virulence. Infect. Immun. 75: 29222928.
15. Bensen, E. S.,, S. J. Martin,, M. Li,, J. Berman, and, D. A. Davis. 2004. Transcriptional profiling in Candida albicans reveals new adaptive responses to extracellular pH and functions for Rim101p. Mol. Microbiol. 54: 13351351.
16. Bernhardt, J.,, D. Herman,, M. Sheridan, and, R. Calderone. 2001. Adherence and invasion studies of Candida albicans strains, using in vitro models of esophageal candidiasis. J. Infect. Dis. 184: 11701175.
17. Bethea, E. K.,, B. J. Carver,, A. E. Montedonico, and, T. B. Reynolds. 2010. The inositol regulon controls viability in Candida glabrata. Microbiology 156: 452462.
18. Borg, M., and, R. Ruchel. 1990. Demonstration of fungal proteinase during phagocytosis of Candida albicans and Candida tropicalis. J. Med. Vet. Mycol. 28: 314.
19. Borg-von Zepelin, M.,, S. Beggah,, K. Boggian,, D. Sanglard, and, M. Monod. 1998. The expression of the secreted aspartyl proteinases Sap4 to Sap6 from Candida albicans in murine macrophages. Mol. Microbiol. 28: 543554.
20. Brand, A.,, D. M. MacCallum,, A. J. Brown,, N. A. Gow, and, F. C. Odds. 2004. Ectopic expression of URA3 can influence the virulence phenotypes and proteome of Candida albicans but can be overcome by targeted reintegration of URA3 at the RPS10 locus. Eukaryot. Cell 3: 900909.
21. Brasch, J.,, J. M. Schroder, and, E. Christophers. 1992. Candida albicans grown in glucose-free media contains serum-independent chemotactic activity. Acta Derm. Venereol. 72: 13.
22. Braun, B. R.,, D. Kadosh, and, A. D. Johnson. 2001. NRG1, a repressor of filamentous growth in C. albicans, is down-regulated during filament induction. EMBO J. 20: 47534761.
23. Brown, A. J. 2002. Expression of growth form-specific factors during morphogenesis in Candida albicans, p. 8794. In R. Calderone (ed.), Candida and Candidiasis. ASM Press, Washington, DC.
24. Brown, A. J. 2002. Morphogenetic signaling pathways in Candida albicans, p. 95–106. In R. Calderone (ed.), Candida and Candidiasis. ASM Press, Washington, DC.
25. Butler, G.,, M. D. Rasmussen,, M. F. Lin,, M. A. Santos,, S. Sakthikumar,, C. A. Munro,, E. Rheinbay,, M. Grabherr,, A. Forche,, J. L. Reedy,, I. Agrafioti,, M. B. Arnaud,, S. Bates,, A. J. Brown,, S. Brunke,, M. C. Costanzo,, D. A. Fitzpatrick,, P. W. de Groot,, D. Harris,, L. L. Hoyer,, B. Hube,, F. M. Klis,, C. Kodira,, N. Lennard,, M. E. Logue,, R. Martin,, A. M. Neiman,, E. Nikolaou,, M. A. Quail,, J. Quinn,, M. C. Santos,, F. F. Schmitzberger,, G. Sherlock,, P. Shah,, K. A. Silverstein,, M. S. Skrzypek,, D. Soll,, R. Staggs,, I. Stansfield,, M. P. Stumpf,, P. E. Sudbery,, T. Srikantha,, Q. Zeng,, J. Berman,, M. Berriman,, J. Heitman,, N. A. Gow,, M. C. Lorenz,, B. W. Birren,, M. Kellis, and, C. A. Cuomo. 2009. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459: 657662.
26. Calcagno, A. M.,, E. Bignell,, P. Warn,, M. D. Jones,, D. W. Denning,, F. A. Muhlschlegel,, T. R. Rogers, and, K. Haynes. 2003. Candida glabrata STE12 is required for wild-type levels of virulence and nitrogen starvation induced filamentation. Mol. Microbiol. 50: 13091318.
27. Cao, Y.,, Y. Wang,, B. Dai,, B. Wang,, H. Zhang,, Z. Zhu,, Y. Xu,, Y. Jiang, and, G. Zhang. 2008. Trehalose is an important mediator of Cap1p oxidative stress response in Candida albicans. Biol. Pharm. Bull. 31: 421425.
28. Carman, A. J.,, S. Vylkova, and, M. C. Lorenz. 2008. Role of acetyl coenzyme a synthesis and breakdown in alternative carbon source utilization in Candida albicans. Eukaryot. Cell 7: 17331741.
29. Caro, L. H.,, H. Tettelin,, J. H. Vossen,, A. F. Ram,, H. van den Ende, and, F. M. Klis. 1997. In silicio identification of glycosyl-phosphatidylinositol-anchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast 13: 14771489.
30. Casanova, M.,, J. L. Lopez-Ribot,, J. P. Martinez, and, R. Sentandreu. 1992. Characterization of cell wall proteins from yeast and mycelial cells of Candida albicans by labelling with biotin: comparison with other techniques. Infect. Immun. 60: 48984906.
31. Castano, I.,, S. J. Pan,, M. Zupancic,, C. Hennequin,, B. Dujon, and, B. P. Cormack. 2005. Telomere length control and transcriptional regulation of subtelomeric adhesins in Candida glabrata. Mol. Microbiol. 55: 12461258.
32. Chauhan, N.,, D. Inglis,, E. Roman,, J. Pla,, D. Li,, J. A. Calera, and, R. Calderone. 2003. Candida albicans response regulator gene SSK1 regulates a subset of genes whose functions are associated with cell wall biosynthesis and adaptation to oxidative stress. Eukaryot. Cell 2: 10181024.
33. Chauhan, N.,, J. P. Latge, and, R. Calderone. 2006. Signalling and oxidant adaptation in Candida albicans and Aspergillus fumigatus. Nat. Rev. 4: 435444.
34. Chaves, G. M.,, S. Bates,, D. M. Maccallum, and, F. C. Odds. 2007. Candida albicans GRX2, encoding a putative glutaredoxin, is required for virulence in a murine model. Genet. Mol. Res. 6: 10511063.
35. Chen, Y. L.,, S. Kauffman, and, T. B. Reynolds. 2008. Candida albicans uses multiple mechanisms to acquire the essential metabolite inositol during infection. Infect. Immun. 76: 27932801.
36. Cheng, G.,, K. Wozniak,, M. A. Wallig,, P. L. Fidel,, Jr., S. R. Trupin, and, L. L. Hoyer. 2005. Comparison between Candida albicans agglutinin-like sequence gene expression patterns in human clinical specimens and models of vaginal candidiasis. Infect. Immun. 73: 16561663.
37. Cheng, G.,, K. M. Yeater, and, L. L. Hoyer. 2006. Cellular and molecular biology of Candida albicans estrogen response. Eukaryot. Cell 5: 180191.
38. Chinen, T.,, M. H. Qureshi,, Y. Koguchi, and, K. Kawakami. 1999. Candida albicans suppresses nitric oxide (NO) production by interferon-gamma (IFN-gamma) and lipopolysaccharide (LPS)-stimulated murine peritoneal macrophages. Clin. Exp. Immunol. 115: 491497.
39. Chiranand, W.,, I. McLeod,, H. Zhou,, J. J. Lynn,, L. A. Vega,, H. Myers,, J. R. Yates III,, M. C. Lorenz, and, M. C. Gustin. 2008. CTA4 transcription factor mediates induction of nitrosative stress response in Candida albicans. Eukaryot. Cell 7: 268278.
40. Cole, M. F.,, W. H. Bowen,, X. J. Zhao, and, R. L. Cihlar. 1995. Avirulence of Candida albicans auxotrophic mutants in a rat model of oropharyngeal candidiasis. FEMS Microbiol. Lett. 126: 177180.
41. Coleman, D. A.,, S. H. Oh,, X. Zhao,, H. Zhao,, J. T. Hutchins,, J. H. Vernachio,, J. M. Patti, and, L. L. Hoyer. 2009. Monoclonal antibodies specific for Candida albicans Als3 that immunolabel fungal cells in vitro and in vivo and block adhesion to host surfaces. J. Microbiol. Methods 78: 7178.
42. 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: 578582.
43. Crowe, J. D.,, I. K. Sievwright,, G. C. Auld,, N. R. Moore,, N. A. Gow, and, N. A. Booth. 2003. Candida albicans binds human plasminogen: identification of eight plasminogen-binding proteins. Mol. Microbiol. 47: 16371651.
44. Cuellar-Cruz, M.,, M. Briones-Martin-del-Campo,, I. Canas-Villamar,, J. Montalvo-Arredondo,, L. Riego-Ruiz,, I. Castano, and, A. De Las Penas. 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: 814825.
45. Cutler, J. E. 1977. Chemotactic factor produced by Candida albicans. Infect. Immun. 18: 568573.
46. de Groot, P. W.,, A. D. de Boer,, J. Cunningham,, H. L. Dekker,, L. de Jong,, K. J. Hellingwerf,, C. de Koster, and, F. M. Klis. 2004. Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryot. Cell 3: 955965.
47. De Groot, P. W.,, K. J. Hellingwerf, and, F. M. Klis. 2003. Genome-wide identification of fungal GPI proteins. Yeast 20: 781796.
48. De Las Penas, A.,, S. J. Pan,, I. Castaäno,, J. Alder,, R. Cregg, and, B. P. Cormack. 2003. Virulence-related surface glycoproteins in the yeast pathogen Candida glabrata are encoded in subtelomeric clusters and subject to RAP1-and SIR-dependent transcriptional silencing. Genes Dev. 17: 22452258.
49. Dieterich, C.,, M. Schandar,, M. Noll,, F. J. Johannes,, H. Brunner,, T. Graeve, and, S. Rupp. 2002. In vitro reconstructed human epithelia reveal contributions of Candida albicans EFG1 and CPH1 to adhesion and invasion. Microbiology 148: 497506.
50. do Carmo-Sousa, L. 1969. Distribution of yeasts in nature, p. 79–105. In A. H. Rose and, J. S. Harrison (ed.), The Yeasts, vol. 1. Academic Press, London, United Kingdom.
51. Dolan, J. W.,, A. C. Bell,, B. Hube,, M. Schaller,, T. F. Warner, and, E. Balish. 2004. Candida albicans PLD I activity is required for full virulence. Med. Mycol. 42: 439447.
52. Domergue, R.,, I. Castano,, A. De Las Penas,, 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: 866870.
53. Donovan, M.,, J. J. Schumuke,, W. A. Fonzi,, S. L. Bonar,, K. Gheesling-Mullis,, G. S. Jacob,, V. J. Davisson, and, S. B. Dotson. 2001. Virulence of a phosphoribosylaminoimidazole carboxylase-deficient Candida albicans strain in an immunosuppressed murine model of systemic candidiasis. Infect. Immun. 69: 25422548.
54. Draculic, T.,, I. W. Dawes, and, C. M. Grant. 2000. A single glutaredoxin or thioredoxin gene is essential for viability in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 36: 11671174.
55. Du, C.,, R. Calderone,, J. Richert, and, D. Li. 2005. Deletion of the SSK1 response regulator gene in Candida albicans contributes to enhanced killing by human polymorphonuclear neutrophils. Infect. Immun. 73: 865871.
56. Dujon, B.,, D. Sherman,, G. Fischer,, P. Durrens,, S. Casaregola,, I. Lafontaine,, J. De Montigny,, C. Marck,, C. Neuveglise,, E. Talla,, N. Goffard,, L. Frangeul,, M. Aigle,, V. Anthouard,, A. Babour,, V. Barbe,, S. Barnay,, S. Blanchin,, J. M. Beckerich,, E. Beyne,, C. Bleykasten,, A. Boisrame,, J. Boyer,, L. Cattolico,, F. Confanioleri,, A. De Daruvar,, L. Despons,, E. Fabre,, C. Fairhead,, H. Ferry-Dumazet,, A. Groppi,, F. Hantraye,, C. Hennequin,, N. Jauniaux,, P. Joyet,, R. Kachouri,, A. Kerrest,, R. Koszul,, M. Lemaire,, I. Lesur,, L. Ma,, H. Muller,, J. M. Nicaud,, M. Nikolski,, S. Oztas,, O. Ozier-Kalogeropoulos,, S. Pellenz,, S. Potier,, G. F. Richard,, M. L. Straub,, A. Suleau,, D. Swennen,, F. Tekaia,, M. Wesolowski-Louvel,, E. Westhof,, B. Wirth,, M. Zeniou-Meyer,, I. Zivanovic,, M. Bolotin-Fukuhara,, A. Thierry,, C. Bouchier,, B. Caudron,, C. Scarpelli,, C. Gaillardin,, J. Weissenbach,, P. Wincker, and, J. L. Souciet. 2004. Genome evolution in yeasts. Nature 430: 3544.
57. Edens, H. A.,, C. A. Parkos,, T. W. Liang,, A. J. Jesaitis,, J. E. Cutler, and, H. M. Miettinen. 1999. Non-serum-dependent chemotactic factors produced by Candida albicans stimulate chemotaxis by binding to the formyl peptide receptor on neutrophils and to an unknown receptor on macrophages. Infect. Immun. 67: 10631071.
58. Eisenhaber, B.,, G. Schneider,, M. Wildpaner, and, F. Eisenhaber. 2004. A sensitive predictor for potential GPI lipid modification sites in fungal protein sequences and its application to genome-wide studies for Aspergillus nidulans, Candida albicans, Neurospora crassa, Saccharomyces cerevisiae and Schizosaccharomyces pombe. J. Mol. Biol. 337: 243253.
59. Elson, S. L.,, S. M. Noble,, N. V. Solis,, S. G. Filler, and, A. D. Johnson. 2009. An RNA transport system in Candida albicans regulates hyphal morphology and invasive growth. PLoS Genet. 5: e1000664.
60. Ene, I. V., and, R. J. Bennett. 2009. Hwp1 and related adhesins contribute to both mating and biofilm formation in Candida albicans. Eukaryot. Cell 8: 19091913.
61. Enjalbert, B.,, D. M. MacCallum,, F. C. Odds, and, A. J. Brown. 2007. Niche-specific activation of the oxidative stress response by the pathogenic fungus Candida albicans. Infect. Immun. 75: 21432151.
62. Enjalbert, B.,, A. Nantel, and, M. Whiteway. 2003. Stress-induced gene expression in Candida albicans: absence of a general stress response. Mol. Biol. Cell 14: 14601467.
63. Enjalbert, B.,, D. A. Smith,, M. J. Cornell,, I. Alam,, S. Nicholls,, A. J. Brown, and, J. Quinn. 2006. Role of the Hog1 stress-activated protein kinase in the global transcriptional response to stress in the fungal pathogen Candida albicans. Mol. Biol. Cell 17: 10181032.
64. Fernandez-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: 560589.
65. Fernandez-Arenas, E.,, V. Cabezon,, C. Bermejo,, J. Arroyo,, C. Nombela,, R. Diez-Orejas, and, C. Gil. 2007. Integrated proteomics and genomics strategies bring new insight into Candida albicans response upon macrophage interaction. Mol. Cell. Proteomics 6: 460478.
66. Filler, S. G., and, D. C. Sheppard. 2006. Fungal invasion of normally non-phagocytic host cells. PLoS Pathog. 2: e129.
67. Filler, S. G.,, J. N. Swerdloff,, C. Hobbs, and, P. M. Luckett. 1995. Penetration and damage of endothelial cells by Candida albicans. Infect. Immun. 63: 976983.
68. Forsyth, C. B., and, H. L. Mathews. 1996. Lymphocytes utilize CD11b/CD18 for adhesion to Candida albicans. Cell. Immunol. 170: 91100.
69. Forsyth, C. B.,, E. F. Plow, and, L. Zhang. 1998. Interaction of the fungal pathogen Candida albicans with integrin CD11b/CD18: recognition by the I domain is modulated by the lectin-like domain and the CD18 subunit. J. Immunol. 161: 61986205.
70. 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: 397415.
71. Fradin, C.,, M. Kretschmar,, T. Nichterlein,, C. Gaillardin,, C. d’Enfert, and, B. Hube. 2003. Stage-specific gene expression of Candida albicans in human blood. Mol. Microbiol. 47: 15231543.
72. Frank, A. T.,, C. Ramsook,, H. N. Otoo,, C. Tan,, G. Soybelman,, J. M. Rauceo,, N. K. Gaur,, S. A. Klotz, and, P. N. Lipke. 2010. Structure and function of glycosylated tandem repeats from Candida albicans Als adhesins. Eukaryot. Cell 9: 405414.
73. Frealle, E.,, C. Noel,, E. Viscogliosi,, D. Camus,, E. Dei-Cas, and, L. Delhaes. 2005. Manganese superoxide dismutase in pathogenic fungi: an issue with pathophysiological and phylogenetic involvements. FEMS Immunol. Med. Microbiol. 45: 411422.
74. 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: 240252.
75. Fu, Y.,, A. S. Ibrahim,, W. Fonzi,, X. Zhou,, C. F. Ramos, and, M. A. Ghannoum. 1997. Cloning and characterization of a gene (LIP1) which encodes a lipase from the pathogenic yeast Candida albicans. Microbiology 143 (Pt. 2): 331340.
76. Fu, Y.,, A. S. Ibrahim,, D. C. Sheppard,, Y. C. Chen,, S. W. French,, J. E. Cutler,, S. G. Filler, and, J. E. Edwards, Jr. 2002. Candida albicans Als1p: an adhesin that is a downstream effector of the EFG1 filamentation pathway. Mol. Microbiol. 44: 6172.
77. Fu, Y.,, G. Luo,, B. J. Spellberg,, J. E. Edwards, Jr., and, A. S. Ibrahim. 2008. Gene overexpression/suppression analysis of candidate virulence factors of Candida albicans. Eukaryot. Cell 7: 483492.
78. Fu, Y.,, G. Rieg,, W. A. Fonzi,, P. H. Belanger,, J. E. Edwards, Jr., and, S. G. Filler. 1998. Expression of the Candida albicans gene ALS1 in Saccharomyces cerevisiae induces adherence to endothelial and epithelial cells. Infect. Immun. 66: 17831786.
79. Gacser, A.,, F. Stehr,, C. Kroger,, L. Kredics,, W. Schafer, and, J. D. Nosanchuk. 2007. Lipase 8 affects the pathogenesis of Candida albicans. Infect. Immun. 75: 47104718.
80. Gacser, A.,, D. Trofa,, W. Schafer, and, J. D. Nosanchuk. 2007. Targeted gene deletion in Candida parapsilosis demonstrates the role of secreted lipase in virulence. J. Clin. Investig. 117: 30493058.
81. Gasch, A. P.,, P. T. Spellman,, C. M. Kao,, O. Carmel-Harel,, M. B. Eisen,, G. Storz,, D. Botstein, and, P. O. Brown. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11: 42414257.
82. Gaur, N. K., and, S. A. Klotz. 1997. Expression, cloning, and characterization of a Candida albicans gene, ALA1, that confers adherence properties upon Saccharomyces cerevisiae for extracellular matrix proteins. Infect. Immun. 65: 52895294.
83. Geiger, J.,, D. Wessels,, S. R. Lockhart, and, D. R. Soll. 2004. Release of a potent polymorphonuclear leukocyte chemoattractant is regulated by white-opaque switching in Candida albicans. Infect. Immun. 72: 667677.
84. 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: 15961605.
85. Gonzalez, M. I.,, R. Stucka,, M. A. Blazquez,, H. Feld-mann, and, C. Gancedo. 1992. Molecular cloning of CIF1, a yeast gene necessary for growth on glucose. Yeast 8: 183192.
86. Hajjeh, R. A.,, A. N. Sofair,, L. H. Harrison,, G. M. Lyon,, B. A. Arthington-Skaggs,, S. A. Mirza,, M. Phelan,, J. Morgan,, W. Lee-Yang,, M. A. Ciblak,, L. E. Benjamin,, L. T. Sanza,, S. Huie,, S. F. Yeo,, M. E. Brandt, and, D. W. Warnock. 2004. Incidence of bloodstream infections due to Candida species and in vitro susceptibilities of isolates collected from 1998 to 2000 in a population-based active surveillance program. J. Clin. Microbiol. 42: 15191527.
87. Heidenreich, S.,, B. Otte,, D. Lang, and, M. Schmidt. 1996. Infection by Candida albicans inhibits apoptosis of human monocytes and monocytic U937 cells. J. Leukoc. Biol. 60: 737743.
88. Herrero, E.,, J. Ros,, G. Belli, and, E. Cabiscol. 2008. Redox control and oxidative stress in yeast cells. Biochim. Biophys. Acta 1780: 12171235.
89. Hornbach, A.,, A. Heyken,, L. Schild,, B. Hube,, J. Loffler, and, O. Kurzai. 2009. The glycosylphosphatidylinositol-anchored protease Sap9 modulates the interaction of Candida albicans with human neutrophils. Infect. Immun. 77: 52165224.
90. Hoyer, L. L. 2001. The ALS gene family of Candida albicans. Trends Microbiol. 9: 176180.
91. Hoyer, L. L.,, C. B. Green,, S. H. Oh, and, X. Zhao. 2008. Discovering the secrets of the Candida albicans agglutinin-like sequence (ALS) gene family—a sticky pursuit. Med. Mycol. 46: 115.
92. Hoyer, L. L., and, J. E. Hecht. 2001. The ALS5 gene of Candida albicans and analysis of the Als5p N-terminal domain. Yeast 18: 4960.
93. Hoyer, L. L.,, S. Scherer,, A. R. Shatzman, and, G. P. Livi. 1995. Candida albicans ALS1: domains related to a Saccharomyces cerevisiae sexual agglutinin separated by a repeating motif. Mol. Microbiol. 15: 3954.
94. Hromatka, B. S.,, S. M. Noble, and, A. D. Johnson. 2005. Transcriptional response of Candida albicans to nitric oxide and the role of the YHB1 gene in nitrosative stress and virulence. Mol. Biol. Cell 16: 48144826.
95. Hube, B.,, D. Sanglard,, F. C. Odds,, D. Hess,, M. Monod,, W. Schafer,, A. J. Brown, and, N. A. Gow. 1997. Disruption of each of the secreted aspartyl proteinase genes SAP1, SAP2, and SAP3 of Candida albicans attenuates virulence. Infect. Immun. 65: 35293538.
96. Hube, B.,, F. Stehr,, M. Bossenz,, A. Mazur,, M. Kretschmar, and, W. Schafer. 2000. Secreted lipases of Candida albicans: cloning, characterisation and expression analysis of a new gene family with at least ten members. Arch. Microbiol. 174: 362374.
97. Hwang, C. S.,, Y. U. Baek,, H. S. Yim, and, S. O. Kang. 2003. Protective roles of mitochondrial manganese-containing superoxide dismutase against various stresses in Candida albicans. Yeast 20: 929941.
98. Hwang, C. S.,, G. Rhie,, S. T. Kim,, Y. R. Kim,, W. K. Huh,, Y. U. Baek, and, S. O. Kang. 1999. Copper- and zinc-containing superoxide dismutase and its gene from Candida albicans. Biochim. Biophys. Acta 1427: 245255.
99. Hwang, C. S.,, G. E. Rhie,, J. H. Oh,, W. K. Huh,, H. S. Yim, and, S. O. Kang. 2002. Copper- and zinc-containing superoxide dismutase (Cu/ZnSOD) is required for the protection of Candida albicans against oxidative stresses and the expression of its full virulence. Microbiology 148: 37053713.
100. Ibata-Ombetta, S.,, T. Idziorek,, P. A. Trinel,, D. Poulain, and, T. Jouault. 2003. Candida albicans phospholipomannan promotes survival of phagocytosed yeasts through modulation of bad phosphorylation and macrophage apoptosis. J. Biol. Chem. 278: 1308613093.
101. Iraqui, I.,, S. Garcia-Sanchez,, S. Aubert,, F. Dromer,, J. M. Ghigo,, C. d’Enfert, and, G. Janbon. 2005. The Yak1p kinase controls expression of adhesins and biofilm formation in Candida glabrata in a Sir4p-dependent pathway. Mol. Microbiol. 55: 12591271.
102. Jackson, A. P.,, J. A. Gamble,, T. Yeomans,, G. P. Moran,, D. Saunders,, D. Harris,, M. Aslett,, J. F. Barrell,, G. Butler,, F. Citiulo,, D. C. Coleman,, P. W. de Groot,, T. J. Goodwin,, M. A. Quail,, J. McQuillan,, C. A. Munro,, A. Pain,, R. T. Poulter,, M. A. Rajandream,, H. Renauld,, M. J. Spiering,, A. Tivey,, N. A. Gow,, B. Barrell,, D. J. Sullivan, and, M. Berriman. 2009. Comparative genomics of the fungal pathogens Candida dubliniensis and Candida albicans. Genome Res. 19: 22312244.
103. Jacobsen, I. D.,, S. Brunke,, K. Seider,, T. Schwarzmuller,, A. Firon,, C. d’Enfert,, 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: 10661077.
104. Jong, A. Y.,, M. F. Stins,, S. H. Huang,, S. H. Chen, and, K. S. Kim. 2001. Traversal of Candida albicans across human blood-brain barrier in vitro. Infect. Immun. 69: 45364544.
105. Kaposzta, R.,, L. Marodi,, M. Hollinshead,, S. Gordon, and, R. P. da Silva. 1999. Rapid recruitment of late endosomes and lysosomes in mouse macrophages ingesting Candida albicans. J. Cell Sci. 112 (Pt. 19): 32373248.
106. 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: 76287633.
107. Kempf, M.,, J. Cottin,, P. Licznar,, C. Lefrancois,, R. Robert, and, V. Apaire-Marchais. 2009. Disruption of the GPI protein-encoding gene IFF4 of Candida albicans results in decreased adherence and virulence. Mycopathologia 168: 7377.
108. Kingsbury, J. M., and, J. H. McCusker. 2008. Threonine biosynthetic genes are essential in Cryptococcus neoformans. Microbiology 154: 27672775.
109. Kingsbury, J. M., and, J. H. McCusker. 2010. Cytocidal amino acid starvation of Saccharomyces cerevisiae and Candida albicans acetolactate synthase ( ilv2Δ) mutants is influenced by the carbon source and rapamycin. Microbiology 156: 929939.
110. Kingsbury, J. M.,, Z. Yang,, T. M. Ganous,, G. M. Cox, and, J. H. McCusker. 2004. Cryptococcus neoformans Ilv2p confers resistance to sulfometuron methyl and is required for survival at 37°C and in vivo. Microbiology 150: 15471558.
111. Kingsbury, J. M.,, Z. Yang,, T. M. Ganous,, G. M. Cox, and, J. H. McCusker. 2004. Novel chimeric spermidine synthase-saccharopine dehydrogenase gene (SPE3-LYS9) in the human pathogen Cryptococcus neoformans. Eukaryot. Cell 3: 752763.
112. Kirsch, D. R., and, R. R. Whitney. 1991. Pathogenicity of Candida albicans auxotrophic mutants in experimental infections. Infect. Immun. 59: 32973300.
113. Klengel, T.,, W. J. Liang,, J. Chaloupka,, C. Ruoff,, K. Schroppel,, J. R. Naglik,, S. E. Eckert,, E. G. Mogensen,, K. Haynes,, M. F. Tuite,, L. R. Levin,, J. Buck, and, F. A. Muhlschlegel. 2005. Fungal adenylyl cyclase integrates CO 2 sensing with cAMP signaling and virulence. Curr. Biol. 15: 20212026.
114. Klotz, S. A.,, D. J. Drutz,, J. L. Harrison, and, M. Huppert. 1983. Adherence and penetration of vascular endothelium by Candida yeasts. Infect. Immun. 42: 374384.
115. Knechtle, P.,, S. Goyard,, S. Brachat,, O. Ibrahim-Granet, and, C. d’Enfert. 2005. Phosphatidylinositol-dependent phospholipases C Plc2 and Plc3 of Candida albicans are dispensable for morphogenesis and host-pathogen interaction. Res. Microbiol. 156: 822829.
116. Kunze, D.,, I. Melzer,, D. Bennett,, D. Sanglard,, D. MacCallum,, J. Norskau,, D. C. Coleman,, F. C. Odds,, W. Schafer, and, B. Hube. 2005. Functional analysis of the phospholipase C gene CaPLC1 and two unusual phospholipase C genes, CaPLC2 and CaPLC3, of Candida albicans. Microbiology 151: 33813394.
117. Kusch, H.,, S. Engelmann,, D. Albrecht,, J. Morschhauser, and, M. Hecker. 2007. Proteomic analysis of the oxidative stress response in Candida albicans. Proteomics 7: 686697.
118. Laforce-Nesbitt, S. S.,, M. A. Sullivan,, L. L. Hoyer, and, J. M. Bliss. 2008. Inhibition of Candida albicans adhesion by recombinant human antibody single-chain variable fragment specific for Als3p. FEMS Immunol. Med. Microbiol. 54: 195202.
119. Lamarre, C.,, J. D. LeMay,, N. Deslauriers, and, Y. Bourbonnais. 2001. Candida albicans expresses an unusual cytoplasmic manganese-containing superoxide dismutase (SOD3 gene product) upon the entry and during the stationary phase. J. Biol. Chem. 276: 4378443791.
120. Lay, J.,, L. K. Henry,, J. Clifford,, Y. Koltin,, C. E. Bulawa, and, J. M. Becker. 1998. Altered expression of selectable marker URA3 in gene-disrupted Candida albicans strains complicates interpretation of virulence studies. Infect. Immun. 66: 53015306.
121. Leidich, S. D.,, A. S. Ibrahim,, Y. Fu,, A. Koul,, C. Jessup,, J. Vitullo,, W. Fonzi,, F. Mirbod,, S. Nakashima,, Y. Nozawa, and, M. A. Ghannoum. 1998. Cloning and disruption of caPLB1, a phospholipase B gene involved in the pathogenicity of Candida albicans. J. Biol. Chem. 273: 2607826086.
122. Lermann, U., and, J. Morschhauser. 2008. Secreted aspartic proteases are not required for invasion of reconstituted human epithelia by Candida albicans. Microbiology 154: 32813295.
123. Levitin, A., and, M. Whiteway. 2007. The effect of pros-taglandin E2 on transcriptional responses of Candida albicans. Microbiol. Res. 162: 201210.
124. Liu, X. F.,, I. Elashvili,, E. B. Gralla,, J. S. Valentine,, P. Lapinskas, and, V. C. Culotta. 1992. Yeast lacking super-oxide dismutase. Isolation of genetic suppressors. J. Biol. Chem. 267: 1829818302.
125. Lo, H. J.,, J. R. Kohler,, B. DiDomenico,, D. Loebenberg,, A. Cacciapuoti, and, G. R. Fink. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939949.
126. Loaiza-Loeza, S.,, B. Parra-Ortega,, J. C. Cancino-Diaz,, B. Illades-Aguiar,, C. H. Hernandez-Rodriguez, and, L. Villa-Tanaca. 2009. Differential expression of Candida dubliniensis-secreted aspartyl proteinase genes (CdSAP1-4) under different physiological conditions and during infection of a keratinocyte culture. FEMS Immunol. Med. Microbiol. 56: 212222.
127. Lohse, M. B., and, A. D. Johnson. 2008. Differential phagocytosis of white versus opaque Candida albicans by Drosophila and mouse phagocytes. PLoS One 3: e1473.
128. Longo, V. D.,, E. B. Gralla, and, J. S. Valentine. 1996. Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae. Mitochondrial production of toxic oxygen species in vivo. J. Biol. Chem. 271: 1227512280.
129. Longo, V. D.,, L. L. Liou,, J. S. Valentine, and, E. B. Gralla. 1999. Mitochondrial superoxide decreases yeast survival in stationary phase. Arch. Biochem. Biophys. 365: 131142.
130. Lorenz, M. C.,, J. A. Bender, and, G. R. Fink. 2004. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot. Cell 3: 10761087.
131. Lorenz, M. C., and, G. R. Fink. 2001. The glyoxylate cycle is required for fungal virulence. Nature 412: 8386.
132. Loza, L.,, Y. Fu,, A. S. Ibrahim,, D. C. Sheppard,, S. G. Filler, and, J. E. Edwards, Jr. 2004. Functional analysis of the Candida albicans ALS1 gene product. Yeast 21: 473482.
133. Luo, S.,, S. Poltermann,, A. Kunert,, S. Rupp, and, P. F. Zipfel. 2009. Immune evasion of the human pathogenic yeast Candida albicans: Pra1 is a factor H, FHL-1 and plasminogen binding surface protein. Mol. Immunol. 47: 541550.
134. Maidan, M. M.,, L. De Rop,, M. Relloso,, R. Diez-Orejas,, J. M. Thevelein, and, P. Van Dijck. 2008. Combined inactivation of the Candida albicans GPR1 and TPS2 genes results in avirulence in a mouse model for systemic infection. Infect. Immun. 76: 16861694.
135. Marcil, A.,, C. Gadoury,, J. Ash,, J. Zhang,, A. Nantel, and, M. Whiteway. 2008. Analysis of PRA1 and its relationship to Candida albicans-macrophage interactions. Infect. Immun. 76: 43454358.
136. Martchenko, M.,, A. M. Alarco,, D. Harcus, and, M. Whiteway. 2004. Superoxide dismutases in Candida albicans: transcriptional regulation and functional characterization of the hyphal-induced SOD5 gene. Mol. Biol. Cell 15: 456467.
137. Martinez-Esparza, M.,, A. Aguinaga,, P. Gonzalez- Parraga,, P. Garcia-Penarrubia,, T. Jouault, and, J. C. Arguelles. 2007. Role of trehalose in resistance to macrophage killing: study with a tps1/ tps1 trehalose-deficient mutant of Candida albicans. Clin. Microbiol. Infect. 13: 384394.
138. Martinez-Esparza, M.,, E. Martinez-Vicente,, P. Gonzalez-Parraga,, J. M. Ros,, P. Garcia-Penarrubia, and, J. C. Arguelles. 2009. Role of trehalose-6P phosphatase (TPS2) in stress tolerance and resistance to macrophage killing in Candida albicans. Int. J. Med. Microbiol. 299: 453464.
139. Mor, N., and, M. B. Goren. 1987. Discrepancy in assessment of phagosome-lysosome fusion with two lysosomal markers in murine macrophages infected with Candida albicans. Infect. Immun. 55: 16631667.
140. Moran, G. P.,, D. M. MacCallum,, M. J. Spiering,, D. C. Coleman, and, D. J. Sullivan. 2007. Differential regulation of the transcriptional repressor NRG1 accounts for altered host-cell interactions in Candida albicans and Candida dubliniensis. Mol. Microbiol. 66: 915929.
141. Moreno-Ruiz, E.,, M. Galan-Diez,, W. Zhu,, E. Fernandez-Ruiz,, C. d’Enfert,, S. G. Filler,, P. Cossart, and, E. Veiga. 2009. Candida albicans internalization by host cells is mediated by a clathrin-dependent mechanism. Cell. Microbiol. 11: 11791189.
142. Murad, A. M.,, P. Leng,, M. Straffon,, J. Wishart,, S. Macaskill,, D. MacCallum,, N. Schnell,, D. Talibi,, D. Marechal,, F. Tekaia,, C. d’Enfert,, C. Gaillardin,, F. C. Odds, and, A. J. Brown. 2001. NRG1 represses yeasthypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J. 20: 47424752.
143. Nadir, E., and, M. Kaufshtein. 2005. Images in clinical medicine. Candida albicans in a peripheral-blood smear. N. Engl. J. Med. 353: e9.
144. Nagahashi, S.,, T. Mio,, N. Ono,, T. Yamada-Okabe,, M. Arisawa,, H. Bussey, and, H. Yamada-Okabe. 1998. Isolation of CaSLN1 and CaNIK1, the genes for osmosensing histidine kinase homologues, from the pathogenic fungus Candida albicans. Microbiology 144 (Pt. 2): 425432.
145. Naglik, J. R.,, S. J. Challacombe, and, B. Hube. 2003. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol. Mol. Biol. Rev. 67: 400428.
146. Naglik, J. R.,, C. A. Rodgers,, P. J. Shirlaw,, J. L. Dobbie,, L. L. Fernandes-Naglik,, D. Greenspan,, N. Agabian, and, S. J. Challacombe. 2003. Differential expression of Candida albicans secreted aspartyl proteinase and phospholipase B genes in humans correlates with active oral and vaginal infections. J. Infect. Dis. 188: 469479.
147. Nakagawa, Y. 2008. Catalase gene disruptant of the human pathogenic yeast Candida albicans is defective in hyphal growth, and a catalase-specific inhibitor can suppress hyphal growth of wild-type cells. Microbiol. Immunol. 52: 1624.
148. Nakagawa, Y.,, T. Kanbe, and, I. Mizuguchi. 2003. Disruption of the human pathogenic yeast Candida albicans catalase gene decreases survival in mouse-model infection and elevates susceptibility to higher temperature and to detergents. Microbiol. Immunol. 47: 395403.
149. Nantel, A.,, D. Dignard,, C. Bachewich,, D. Harcus,, A. Marcil,, A. P. Bouin,, C. W. Sensen,, H. Hogues,, M. van het Hoog,, P. Gordon,, T. Rigby,, F. Benoit,, D. C. Tessier,, D. Y. Thomas, and, M. Whiteway. 2002. Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol. Biol. Cell 13: 34523465.
150. Nasution, O.,, K. Srinivasa,, M. Kim,, Y. J. Kim,, W. Kim,, W. Jeong, and, W. Choi. 2008. Hydrogen peroxide induces hyphal differentiation in Candida albicans. Eukaryot. Cell 7: 20082011.
151. Navarathna, D. H.,, K. W. Nickerson,, G. E. Duhamel,, T. R. Jerrels, and, T. M. Petro. 2007. Exogenous farnesol interferes with the normal progression of cytokine expression during candidiasis in a mouse model. Infect. Immun. 75: 40064011.
152. Nazi, I.,, A. Scott,, A. Sham,, L. Rossi,, P. R. Williamson,, J. W. Kronstad, and, G. D. Wright. 2007. Role of homo-serine transacetylase as a new target for antifungal agents. Antimicrob. Agents Chemother. 51: 17311736.
153. Netea, M. G.,, K. Gijzen,, N. Coolen,, I. Verschueren,, C. Figdor,, J. W. Van der Meer,, R. Torensma, and, B. J. Kullberg. 2004. Human dendritic cells are less potent at killing Candida albicans than both monocytes and macrophages. Microbes Infect. 6: 985989.
154. Nett, J. E.,, A. J. Lepak,, K. Marchillo, and, D. R. Andes. 2009. Time course global gene expression analysis of an in vivo Candida biofilm. J. Infect. Dis. 200: 307313.
155. Newman, S. L.,, B. Bhugra,, A. Holly, and, R. E. Morris. 2005. Enhanced killing of Candida albicans by human macrophages adherent to type 1 collagen matrices via induction of phagolysosomal fusion. Infect. Immun. 73 : 770–777.
156. Nobile, C. J.,, D. R. Andes,, J. E. Nett,, F. J. Smith,, F. Yue,, Q. T. Phan,, J. E. Edwards,, S. G. Filler, and, A. P. Mitchell. 2006. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog. 2: e63.
157. Nobile, C. J., and, A. P. Mitchell. 2006. Genetics and genomics of Candida albicans biofilm formation. Cell. Microbiol. 8: 13821391.
158. Noble, S. M., and, A. D. Johnson. 2005. Strains and strategies for large-scale gene deletion studies of the diploid human fungal pathogen Candida albicans. Eukaryot. Cell 4: 298309.
159. Oh, S. H.,, G. Cheng,, J. A. Nuessen,, R. Jajko,, K. M. Yeater,, X. Zhao,, C. Pujol,, D. R. Soll, and, L. L. Hoyer. 2005. Functional specificity of Candida albicans Als3p proteins and clade specificity of ALS3 alleles discriminated by the number of copies of the tandem repeat sequence in the central domain. Microbiology 151: 673681.
160. Otoo, H. N.,, K. G. Lee,, W. Qiu, and, P. N. Lipke. 2008. Candida albicans Als adhesins have conserved amyloid-forming sequences. Eukaryot. Cell 7: 776782.
161. Palmer, G. E.,, D. S. Askew, and, P. R. Williamson. 2008. The diverse roles of autophagy in medically important fungi. Autophagy 4: 982988.
162. Palmer, G. E.,, M. N. Kelly, and, J. E. Sturtevant. 2007. Autophagy in the pathogen Candida albicans. Microbiology 153: 5158.
163. Park, H.,, Y. Liu,, N. Solis,, J. Spotkov,, J. Hamaker,, J. R. Blankenship,, M. R. Yeaman,, A. P. Mitchell,, H. Liu, and, S. G. Filler. 2009. Transcriptional responses of Candida albicans to epithelial and endothelial cells. Eukaryot. Cell 8: 14981510.
164. Park, H.,, C. L. Myers,, D. C. Sheppard,, Q. T. Phan,, A. A. Sanchez,, J. E. Edwards, and, S. G. Filler. 2005. Role of the fungal Ras-protein kinase A pathway in governing epithelial cell interactions during oropharyngeal candidiasis. Cell. Microbiol. 7: 499510.
165. Pascon, R. C.,, T. M. Ganous,, J. M. Kingsbury,, G. M. Cox, and, J. H. McCusker. 2004. Cryptococcus neoformans methionine synthase: expression analysis and requirement for virulence. Microbiology 150: 30133023.
166. Phan, Q. T.,, P. H. Belanger, and, S. G. Filler. 2000. Role of hyphal formation in interactions of Candida albicans with endothelial cells. Infect. Immun. 68: 34853490.
167. Phan, Q. T.,, R. A. Fratti,, N. V. Prasadarao,, J. E. Edwards, Jr., and, S. G. Filler. 2005. N-cadherin mediates endocytosis of Candida albicans by endothelial cells. J. Biol. Chem. 280: 1045510461.
168. Phan, Q. T.,, C. L. Myers,, Y. Fu,, D. C. Sheppard,, M. R. Yeaman,, W. H. Welch,, A. S. Ibrahim,, J. E. Edwards, Jr., and, S. G. Filler. 2007. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol. 5: e64.
169. Piekarska, K.,, G. Hardy,, E. Mol,, J. van den Burg,, K. Strijbis,, C. van Roermund,, M. van den Berg, and, B. Distel. 2008. The activity of the glyoxylate cycle in peroxisomes of Candida albicans depends on a functional beta-oxidation pathway: evidence for reduced metabolite transport across the peroxisomal membrane. Microbiology 154: 30613072.
170. Piekarska, K.,, E. Mol,, M. van den Berg,, G. Hardy,, J. van den Burg,, C. van Roermund,, D. Maccallum,, F. Odds, and, B. Distel. 2006. Peroxisomal fatty acid β-oxidation is not essential for virulence of Candida albicans. Eukaryot. Cell 5: 18471856.
171. Poltermann, S.,, A. Kunert,, M. von der Heide,, R. Eck,, A. Hartmann, and, P. F. Zipfel. 2007. Gpm1p is a factor H-, FHL-1-, and plasminogen-binding surface protein of Candida albicans. J. Biol. Chem. 282: 3753737544.
172. Ponniah, G.,, C. Rollenhagen,, Y. S. Bahn,, J. F. Staab, and, P. Sundstrom. 2007. State of differentiation defines buccal epithelial cell affinity for cross-linking to Candida albicans Hwp1. J. Oral Pathol. Med. 36: 456467.
173. Prigneau, O.,, A. Porta,, J. A. Poudrier,, S. Colonna-Romano,, T. Noel, and, B. Maresca. 2003. Genes involved in beta-oxidation, energy metabolism and glyoxylate cycle are induced by Candida albicans during macrophage infection. Yeast 20: 723730.
174. Ramirez, M. A., and, M. C. Lorenz. 2007. Mutations in alternative carbon utilization pathways in Candida albicans attenuate virulence and confer pleiotropic pheno-types. Eukaryot. Cell 6: 280290.
175. Rauceo, J. M.,, R. De Armond,, H. Otoo,, P. C. Kahn,, S. A. Klotz,, N. K. Gaur, and, P. N. Lipke. 2006. Threonine-rich repeats increase fibronectin binding in the Candida albicans adhesin Als5p. Eukaryot. Cell 5: 16641673.
176. Ray, T. L., and, C. D. Payne. 1988. Scanning electron microscopy of epidermal adherence and cavitation in murine candidiasis: a role for Candida acid proteinase. Infect. Immun. 56: 19421949.
177. Reggiori, F., and, D. J. Klionsky. 2002. Autophagy in the eukaryotic cell. Eukaryot. Cell 1: 1121.
178. Renna, M. S.,, S. G. Correa,, C. Porporatto,, C. M. Figueredo,, M. P. Aoki,, M. G. Paraje, and, C. E. Soto-mayor. 2006. Hepatocellular apoptosis during Candida albicans colonization: involvement of TNF-alpha and infiltrating Fas-L positive lymphocytes. Int. Immunol. 18: 17191728.
179. Rennemeier, C.,, T. Frambach,, F. Hennicke,, J. Dietl, and, P. Staib. 2009. Microbial quorum-sensing molecules induce acrosome loss and cell death in human spermatozoa. Infect. Immun. 77: 49904997.
180. Rhie, G. E.,, C. S. Hwang,, M. J. Brady,, S. T. Kim,, Y. R. Kim,, W. K. Huh,, Y. U. Baek,, B. H. Lee,, J. S. Lee, and, S. O. Kang. 1999. Manganese-containing superoxide dismutase and its gene from Candida albicans. Biochim. Biophys. Acta 1426: 409419.
181. Richard, M. L., and, A. Plaine. 2007. Comprehensive analysis of glycosylphosphatidylinositol-anchored proteins in Candida albicans. Eukaryot. Cell 6: 119133.
182. Rivas, V., and, T. J. Rogers. 1983. Studies on the cellular nature of Candida albicans-induced suppression. J. Immunol. 130: 376379.
183. Roetzer, A.,, N. Gratz,, P. Kovarik, and, C. Schuller. 2010. Autophagy supports Candida glabrata survival during phagocytosis. Cell. Microbiol. 12: 199216.
184. Rogers, T. J., and, E. Balish. 1978. Effect of systemic candidiasis on blastogenesis of lymphocytes from germfree and conventional rats. Infect. Immun. 20: 142150.
185. Rogers, T. J., and, E. Balish. 1978. Suppression of lymphocyte blastogenesis by Candida albicans. Clin. Immunol. Immunopathol. 10: 298305.
186. Rotrosen, D.,, J. E. Edwards, Jr.,, T. R. Gibson,, J. C. Moore,, A. H. Cohen, and, I. Green. 1985. Adherence of Candida to cultured vascular endothelial cells: mechanisms of attachment and endothelial cell penetration. J. Infect. Dis. 152: 12641274.
187. Rotstein, D.,, J. Parodo,, R. Taneja, and, J. C. Marshall. 2000. Phagocytosis of Candida albicans induces apoptosis of human neutrophils. Shock 14: 278283.
188. Rubin-Bejerano, I.,, I. Fraser,, P. Grisafi, and, G. R. Fink. 2003. Phagocytosis by neutrophils induces an amino acid deprivation response in Saccharomyces cerevisiae and Candida albicans. Proc. Natl. Acad. Sci. USA 100: 1100711012.
189. Sanchez, A. A.,, D. A. Johnston,, C. Myers,, J. E. Edwards, Jr.,, A. P. Mitchell, and, S. G. Filler. 2004. Relationship between Candida albicans virulence during experimental hematogenously disseminated infection and endothelial cell damage in vitro. Infect. Immun. 72: 598601.
190. Sandovsky-Losica, H.,, N. Chauhan,, R. Calderone, and, E. Segal. 2006. Gene transcription studies of Candida albicans following infection of HEp2 epithelial cells. Med. Mycol. 44: 329334.
191. Sanglard, D.,, B. Hube,, M. Monod,, F. C. Odds, and, N. A. Gow. 1997. A triple deletion of the secreted aspartyl proteinase genes SAP4, SAP5, and SAP6 of Candida albicans causes attenuated virulence. Infect. Immun. 65: 35393546.
192. Sato, T.,, K. Iwabuchi,, I. Nagaoka,, Y. Adachi,, N. Ohno,, H. Tamura,, K. Seyama,, Y. Fukuchi,, H. Nakayama,, F. Yoshizaki,, K. Takamori, and, H. Ogawa. 2006. Induction of human neutrophil chemotaxis by Candida albicans-derived beta-1,6-long glycoside side-chain-branched beta-glucan. J. Leukoc. Biol. 80: 204211.
193. Saville, S. P.,, A. L. Lazzell,, C. Monteagudo, and, J. L. Lopez-Ribot. 2003. Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot. Cell 2: 10531060.
194. Schaller, M.,, M. Bein,, H. C. Korting,, S. Baur,, G. Hamm,, M. Monod,, S. Beinhauer, and, B. Hube. 2003. The secreted aspartyl proteinases Sap1 and Sap2 cause tissue damage in an in vitro model of vaginal candidiasis based on reconstituted human vaginal epithelium. Infect. Immun. 71: 32273234.
195. Schaller, M.,, C. Borelli,, H. C. Korting, and, B. Hube. 2005. Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 48: 365377.
196. Schaller, M.,, H. C. Korting,, W. Schafer,, J. Bastert,, W. Chen, and, B. Hube. 1999. Secreted aspartic proteinase (Sap) activity contributes to tissue damage in a model of human oral candidosis. Mol. Microbiol. 34: 169180.
197. Schaller, M., and, G. Weindl. 2009. Models of oral and vaginal candidiasis based on in vitro reconstituted human epithelia for the study of host-pathogen interactions. Methods Mol. Biol. 470: 327345.
198. Schaller, M.,, K. Zakikhany,, J. R. Naglik,, G. Weindl, and, B. Hube. 2006. Models of oral and vaginal candidiasis based on in vitro reconstituted human epithelia. Nat. Protoc. 1: 27672773.
199. Scheper, M. A.,, M. E. Shirtliff,, T. F. Meiller,, B. M. Peters, and, M. A. Jabra-Rizk. 2008. Farnesol, a fungal quorum-sensing molecule triggers apoptosis in human oral squamous carcinoma cells. Neoplasia 10: 954963.
200. Schroppel, K.,, M. Kryk,, M. Herrmann,, E. Leberer,, M. Rollinghoff, and, C. Bogdan. 2001. Suppression of type 2 NO-synthase activity in macrophages by Candida albicans. Int. J. Med. Microbiol. 290: 659668.
201. Sentandreu, M.,, M. V. Elorza,, R. Sentandreu, and, W. A. Fonzi. 1998. Cloning and characterization of PRA1, a gene encoding a novel pH-regulated antigen of Candida albicans. J. Bacteriol. 180: 282289.
202. Sharkey, L. L.,, W. L. Liao,, A. K. Ghosh, and, W. A. Fonzi. 2005. Flanking direct repeats of hisG alter URA3 marker expression at the HWP1 locus of Candida albicans. Microbiology 151: 10611071.
203. Sheppard, D. C.,, M. R. Yeaman,, W. H. Welch,, Q. T. Phan,, Y. Fu,, A. S. Ibrahim,, S. G. Filler,, M. Zhang,, A. J. Waring, and, J. E. Edwards, Jr. 2004. Functional and structural diversity in the Als protein family of Candida albicans. J. Biol. Chem. 279: 3048030489.
204. Shin, D. H.,, S. Jung,, S. J. Park,, Y. J. Kim,, J. M. Ahn,, W. Kim, and, W. Choi. 2005. Characterization of thiolspecific antioxidant 1 (TSA1) of Candida albicans. Yeast 22: 907918.
205. Slekar, K. H.,, D. J. Kosman, and, V. C. Culotta. 1996. The yeast copper/zinc superoxide dismutase and the pentose phosphate pathway play overlapping roles in oxidative stress protection. J. Biol. Chem. 271: 2883128836.
206. Smith, D. A.,, S. Nicholls,, B. A. Morgan,, A. J. Brown, and, J. Quinn. 2004. A conserved stress-activated protein kinase regulates a core stress response in the human pathogen Candida albicans. Mol. Biol. Cell 15: 41794190.
207. Soloviev, D. A.,, W. A. Fonzi,, R. Sentandreu,, E. Pluskota,, C. B. Forsyth,, S. Yadav, and, E. F. Plow. 2007. Identification of pH-regulated antigen 1 released from Candida albicans as the major ligand for leukocyte integrin alphaMbeta2. J. Immunol. 178: 20382046.
208. Staab, J. F.,, S. D. Bradway,, P. L. Fidel, and, P. Sund-strom. 1999. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283: 15351538.
209. Staib, P.,, M. Kretschmar,, T. Nichterlein,, G. Kohler,, S. Michel,, H. Hof,, J. Hacker, and, J. Morschhauser. 1999. Host-induced, stage-specific virulence gene activation in Candida albicans during infection. Mol. Microbiol. 32: 533546.
210. Stanley, V. C., and, R. Hurley. 1969. The growth of Candida species in cultures of mouse peritoneal macrophages. J. Pathol. 97: 357366.
211. Stehr, F.,, A. Felk,, A. Gacser,, M. Kretschmar,, B. Mahnss,, K. Neuber,, B. Hube, and, W. Schafer. 2004. Expression analysis of the Candida albicans lipase gene family during experimental infections and in patient samples. FEMS Yeast Res. 4: 401408.
212. Strijbis, K.,, C. W. van Roermund,, W. F. Visser,, E. C. Mol,, J. van den Burg,, D. M. MacCallum,, F. C. Odds,, E. Paramonova,, B. P. Krom, and, B. Distel. 2008. Carnitine-dependent transport of acetyl coenzyme A in Candida albicans is essential for growth on nonfermentable carbon sources and contributes to biofilm formation. Eukaryot. Cell 7: 610618.
213. Sundstrom, P. 2002. Adhesion in Candida spp. Cell. Microbiol. 4: 461469.
214. Sundstrom, P.,, J. E. Cutler, and, J. F. Staab. 2002. Reevaluation of the role of HWP1 in systemic candidiasis by use of Candida albicans strains with selectable marker URA3 targeted to the ENO1 locus. Infect. Immun. 70: 32813283.
215. Szabo, I.,, L. Guan, and, T. J. Rogers. 1995. Modulation of macrophage phagocytic activity by cell wall components of Candida albicans. Cell. Immunol. 164: 182188.
216. Theiss, S.,, G. Ishdorj,, A. Brenot,, M. Kretschmar,, C. Y. Lan,, T. Nichterlein,, J. Hacker,, S. Nigam,, N. Agabian, and, G. A. Kohler. 2006. Inactivation of the phospholipase B gene PLB5 in wild-type Candida albicans reduces cell-associated phospholipase A2 activity and attenuates virulence. Int. J. Med. Microbiol. 296: 405420.
217. Thewes, S.,, M. Kretschmar,, H. Park,, M. Schaller,, S. G. Filler, and, B. Hube. 2007. In vivo and ex vivo comparative transcriptional profiling of invasive and non-invasive Candida albicans isolates identifies genes associated with tissue invasion. Mol. Microbiol. 63: 16061628.
218. Ullmann, B. D.,, H. Myers,, W. Chiranand,, A. L. Lazzell,, Q. Zhao,, L. A. Vega,, J. L. Lopez-Ribot,, P. R. Gardner, and, M. C. Gustin. 2004. Inducible defense mechanism against nitric oxide in Candida albicans. Eukaryot. Cell 3: 715723.
219. Urban, C.,, K. Sohn,, F. Lottspeich,, H. Brunner, and, S. Rupp. 2003. Identification of cell surface determinants in Candida albicans reveals Tsa1p, a protein differentially localized in the cell. FEBS Lett. 544: 228235.
220. Urban, C.,, X. Xiong,, K. Sohn,, K. Schroppel,, H. Brunner, and, S. Rupp. 2005. The moonlighting protein Tsa1p is implicated in oxidative stress response and in cell wall biogenesis in Candida albicans. Mol. Microbiol. 57: 13181341.
221. van Loon, A. P.,, B. Pesold-Hurt, and, G. Schatz. 1986. A yeast mutant lacking mitochondrial manganese-super-oxide dismutase is hypersensitive to oxygen. Proc. Natl. Acad. Sci. USA 83: 38203824.
222. Vergne, I.,, J. Chua,, S. B. Singh, and, V. Deretic. 2004. Cell biology of Mycobacterium tuberculosis phagosome. Annu. Rev. Cell Dev. Biol. 20: 367394.
223. Vylkova, S.,, W. S. Jang,, W. Li,, N. Nayyar, and, M. Edgerton. 2007. Histatin 5 initiates osmotic stress response in Candida albicans via activation of the Hog1 mitogenactivated protein kinase pathway. Eukaryot. Cell 6: 18761888.
224. Walker, L. A.,, D. M. Maccallum,, G. Bertram,, N. A. Gow,, F. C. Odds, and, A. J. Brown. 2009. Genome-wide analysis of Candida albicans gene expression patterns during infection of the mammalian kidney. Fungal Genet. Biol. 46: 210219.
225. Wellington, M.,, K. Dolan, and, D. J. Krysan. 2009. Live Candida albicans suppresses production of reactive oxygen species in phagocytes. Infect. Immun. 77: 405413.
226. White, S. J.,, A. Rosenbach,, P. Lephart,, D. Nguyen,, A. Benjamin,, S. Tzipori,, M. Whiteway,, J. Mecsas, and, C. A. Kumamoto. 2007. Self-regulation of Candida albicans population size during GI colonization. PLoS Pathog. 3: e184.
227. Wysong, D. R.,, L. Christin,, A. M. Sugar,, P. W. Robbins, and, R. D. Diamond. 1998. Cloning and sequencing of a Candida albicans catalase gene and effects of disruption of this gene. Infect. Immun. 66: 19531961.
228. Yang, Z.,, R. C. Pascon,, A. Alspaugh,, G. M. Cox, and, J. H. McCusker. 2002. Molecular and genetic analysis of the Cryptococcus neoformans MET3 gene and a met3 mutant. Microbiology 148: 26172625.
229. Zakikhany, K.,, J. R. Naglik,, A. Schmidt-Westhausen,, G. Holland,, M. Schaller, and, B.