Metabolism impacts upon candida immunogenicity and pathogenicity at multiple levels

Trends in Microbiology

Volumn 22, Issue 11, 2014, Pages 614-622

  Brown, Alistair J P ^a   Brown, Gordon D ^a   Netea, Mihai G ^b   Gow, Neil A R ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Cell wall; Fungal immunology; Metabolic adaptation; Regulatory networks; Stress adaptation; Virulence factors

Indexed keywords

CARBON; NITROGEN; OXYGEN; PHOSPHORUS; SULFUR;

ADAPTATION; BIOMASS PRODUCTION; CANDIDA ALBICANS; CARBON METABOLISM; COMMENSALISM; DISEASE COURSE; FUNGAL CELL WALL; FUNGAL METABOLISM; FUNGAL VIRULENCE; HOST PATHOGEN INTERACTION; IMMUNOGENICITY; IMMUNOMODULATION; IMMUNOSURVEILLANCE; MICROBIAL COLONIZATION; NITROGEN METABOLISM; NONHUMAN; PHOSPHATE METABOLISM; PRIORITY JOURNAL; REVIEW; STRESS; HUMAN; IMMUNOLOGY; METABOLISM; PATHOGENICITY;

CANDIDA; CANDIDA ALBICANS;

ADAPTATION, PHYSIOLOGICAL; CANDIDA ALBICANS; HOST-PATHOGEN INTERACTIONS; HUMANS;

EID: 84926988356     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2014.07.001     Document Type: Review

References (101)

1. Odds F.C. Candida and Candidosis 1988, Bailliere Tindall. 2nd edn.
2. Calderone R.A., Clancy C.J. Candida and Candidiasis 2012, ASM Press. 2nd edition.
3. Perlroth J., et al. Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med. Mycol. 2007, 45:321-346.
4. Brown G.D., et al. Hidden killers: human fungal infections. Sci. Transl. Med. 2012, 4:165rv13.
5. Brown A.J.P., et al. Stress responses in Candida. Candida and Candidiasis 2012, 225-242. ASM Press. 2nd edn. C.J. Clancy, R.A. Calderone (Eds.).
6. Gow N.A.R., Hube B. Importance of the Candida albicans cell wall during commensalism and infection. Curr. Opin. Microbiol. 2012, 15:406-412.
7. Leach M.D., et al. Hsp90 - a biological transistor that tunes cellular outputs to thermal inputs. Nat. Rev. Microbiol. 2012, 10:693-704.
8. Brown A.J.P., et al. Stress adaptation in a pathogenic fungus. J. Exp. Biol. 2014, 217:144-155.
9. Ene I.V., Brown A.J.P. Integration of metabolism with virulence in Candida albicans. Mycota 2014, 13:349-370.
10. Rodaki A., et al. Effects of depleting the essential central metabolic enzyme, fructose-1,6-bisphosphate aldolase, upon the growth and viability of Candida albicans: implications for antifungal drug target discovery. Eukaryot. Cell 2006, 5:1371-1377.
11. Xu D., et al. Chemical genetic profiling and characterization of small-molecule compounds that affect the biosynthesis of unsaturated fatty acids in Candida albicans. J. Biol. Chem. 2009, 284:19754-19764.
12. Barelle C.J., et al. Niche-specific regulation of central metabolic pathways in a fungal pathogen. Cell. Microbiol. 2006, 8:961-971.
13. Owen D.H., Katz D.F. A vaginal fluid simulant. Contraception 1999, 59:91-95.
14. Brown A.J.P., et al. Infection-related gene expression in Candida albicans. Curr. Opin. Microbiol. 2007, 10:307-313.
15. Whittington A., et al. From commensal to pathogen: Candida albicans. Mycota 2014, 12:3-18.
16. Zakikhany K., et al. In vivo transcript profiling of Candida albicans identifies a gene essential for interepithelial dissemination. Cell. Microbiol. 2007, 9:2938-2954.
17. Wilson D., et al. Identifying infection-associated genes of Candida albicans in the postgenomic era. FEMS Yeast Res. 2009, 9:688-700.
18. Fradin C., et al. Stage-specific gene expression of Candida albicans in human blood. Mol. Microbiol. 2003, 47:1523-1543.
19. Fradin C., et al. Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol. Microbiol. 2005, 56:397-415.
20. Lorenz M.C., et al. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot. Cell 2004, 3:1076-1087.
21. Rubin-Bejerano I., et al. Phagocytosis by neutrophils induces an amino acid deprivation response in Saccharomyces cerevisiae and Candida albicans. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:11007-11012.
22. Ueno K., et al. Intestinal resident yeast Candida glabrata requires Cyb2p-mediated lactate assimilation to adapt in mouse intestine. PLoS ONE 2011, 6:e24759.
23. Askew C., et al. Transcriptional regulation of carbohydrate metabolism in the human pathogen Candida albicans. PLoS Pathog. 2009, 5:e1000612.
24. Lavoie H., et al. Evolutionary tinkering with conserved components of a transcriptional regulatory network. PLoS Biol. 2010, 8:e1000329.
25. Tripathi G., et al. CaGcn4 co-ordinates morphogenetic and metabolic responses to amino acid starvation in Candida albicans. EMBO J. 2002, 21:5448-5456.
26. Sabina J., Brown V. Glucose sensing network in Candida albicans: a sweet spot for fungal morphogenesis. Eukaryot. Cell 2009, 8:1314-1320.
27. Perez J.C., et al. Candida albicans commensalism and pathogenicity are intertwined traits directed by a tightly knit transcriptional regulatory circuit. PLoS Biol. 2013, 11:e1001510.
28. Pande K., et al. Passage through the mammalian gut triggers a phenotypic switch that promotes Candida albicans commensalism. Nat. Genet. 2013, 45:1088-1091.
29. Lan C.Y., et al. Metabolic specialization associated with phenotypic switching in Candida albicans. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:14907-14912.
30. Nantel A., et al. Transcript profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol. Biol. Cell 2002, 13:3452-3465.
31. Arana D.M., et al. Differential susceptibility of mitogen-activated protein kinase pathway mutants to oxidative-mediated killing by phagocytes in the fungal pathogen Candida albicans. Cell. Microbiol. 2007, 9:1647-1659.
32. Patterson M.J., et al. Ybp1 and Gpx3 signaling in Candida albicans govern hydrogen peroxide-induced oxidation of the Cap1 transcription factor and macrophage escape. Antiox. Redox Signal. 2013, 19:2244-2260.
33. Ene I.V., et al. Host carbon sources modulate cell wall architecture, drug resistance and virulence in a fungal pathogen. Cell. Microbiol. 2012, 14:1319-1335.
34. Rodaki A., et al. Glucose promotes stress resistance in the fungal pathogen, Candida albicans. Mol. Biol. Cell 2009, 20:4845-4855.
35. Mitchell A., et al. Adaptive prediction of environmental changes by microorganisms. Nature 2009, 460:220-224.
36. Garreau H., et al. Hyperphosphorylation of Msn2 and Msn4 in response to heat shock and the diauxic shift is inhibited by cAMP in Saccharomyces cerevisiae. Microbiology 2000, 146:2113-2120.
37. Gasch A.P., et al. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 2000, 11:4241-4257.
38. Roetzer A., et al. Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors. Mol. Microbiol. 2008, 69:603-620.
39. Ramsdale M., et al. The novel gene MNL1 regulates weak acid induced stress responses of the fungal pathogen Candida albicans. Mol. Biol. Cell 2008, 19:4393-4403.
40. Ene I.V., et al. Carbon source-induced reprogramming of the cell wall proteome and secretome modulates the adherence and drug resistance of the fungal pathogen Candida albicans. Proteomics 2012, 12:3164-3179.
41. Giacometti R., et al. Catalytic isoforms Tpk1 and Tpk2 of Candida albicans PKA have non-redundant roles in stress response and glycogen storage. Yeast 2009, 26:273-285.
42. 2 and the acquisition of oxidative tolerance in Candida albicans. Yeast 2003, 20:1161-1169.
43. Gonzalez-Parraga P., et al. Adaptive tolerance to oxidative stress and the induction of antioxidant enzymatic activities in Candida albicans are independent of the Hog1 and Cap1-mediated pathways. FEMS Yeast Res. 2010, 10:747-756.
44. Hall R.A., Gow N.A.R. Mannosylation in Candida albicans: role in cell wall function and immune recognition. Mol. Microbiol. 2013, 90:1147-1161.
45. de Groot P.W.J., et al. Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryot. Cell 2004, 3:955-965.
46. Hall R.A., et al. The Mnn2 mannosyltransferases regulate mannoprotein fibril length, immune recognition and virulence of Candida albicans. PLoS Pathog. 2013, 9:e1003276.
47. Sosinska G.J., et al. Hypoxic conditions and iron restriction affect the cell-wall proteome of Candida albicans grown under vagina-simulative conditions. Microbiology 2008, 154:510-520.
48. Lowman D.W., et al. Mannan structural complexity is decreased when Candida albicans is cultivated in blood or serum at physiological temperature. Carbohydr. Res. 2011, 346:2752-2759.
49. Hudson D.A., et al. Identification of the dialysable serum inducer of germ-tube formation in Candida albicans. Microbiology 2004, 150:3041-3304.
50. Maidan M.M., et al. Carbon source induced yeast-to-hypha transition in Candida albicans is dependent on the presence of amino acids and on the G-protein-coupled receptor Gpr1. Biochem. Soc. Trans. 2005, 33:291-293.
51. Hube B., et al. Expression of seven members of the gene family encoding secretory aspartyl proteinases in Candida albicans. Mol. Microbiol. 1994, 14:87-99.
52. Samaranayake L.P., Macfarlane T.W. The effect of dietary carbohydrates on the in vitro adhesion of Candida albicans to epithelial cells. J. Med. Microbiol. 1982, 15:511-517.
53. Critchley I., Douglas L.J. Differential adhesion of pathogenic Candida species to epithelial and inert surfaces. FEMS Microbiol. Lett. 1985, 28:199-203.
54. Jin Y., et al. Biofilm formation of Candida albicans is variably affected by saliva and dietary sugars. Arch. Oral Biol. 2004, 49:789-798.
55. Enjalbert B., et al. Niche-specific activation of the oxidative stress response by the pathogenic fungus Candida albicans. Infect. Immun. 2007, 75:2143-2151.
56. Miramon P., et al. Cellular responses of Candida albicans to phagocytosis and the extracellular activities of neutrophils are critical to counteract carbohydrate starvation, oxidative and nitrosative stress. PLoS ONE 2012, 7:e52850.
57. Pierce J.V., et al. Normal adaptation of Candida albicans to the murine gastrointestinal tract requires Efg1p-dependent regulation of metabolic and host defense genes. Eukaryot. Cell 2013, 12:37-49.
58. Thewes S., et al. In vivo and ex vivo comparative transcriptional profiling of invasive and non-invasive Candida albicans isolates identifies genes associated with tissue invasion. Mol. Microbiol. 2007, 63:1606-1628.
59. Doedt T., et al. APSES proteins regulate morphogenesis and metabolism in Candida albicans. Mol. Biol. Cell 2004, 15:3167-3180.
60. Harcus D., et al. Transcription profiling of cyclic AMP signaling in Candida albicans. Mol. Biol. Cell 2004, 15:4490-4499.
61. Zordan R.E., et al. Interlocking transcriptional feedback loops control white-opaque switching in Candida albicans. PLoS Biol. 2007, 5:e256.
62. Morschhauser J. Regulation of white-opaque switching in Candida albicans. Med. Microbiol. Immunol. 2010, 199:165-172.
63. Murad A.M.A., et al. NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J. 2001, 20:4742-4752.
64. Lu Y., et al. Hyphal development in Candida albicans requires two temporally linked changes in promoter chromatin for initiation and maintenance. PLoS Biol. 2011, 9:e1001105.
65. Su C., et al. Reduced TOR signaling sustains hyphal development in Candida albicans by lowering Hog1 basal activity. Mol. Biol. Cell 2013, 24:385-397.
66. Lo H.J., et al. Nonfilamentous C. albicans mutants are avirulent. Cell 1997, 90:939-949.
67. Brega E., et al. Candida albicans Csy1p Is a nutrient sensor important for activation of amino acid uptake and hyphal morphogenesis. Eukaryot. Cell 2004, 3:135-143.
68. Lorenz M.C., Fink G.R. The glyoxylate cycle is required for fungal virulence. Nature 2001, 412:83-86.
69. Martinez P., Ljungdahl P.O. Divergence of Stp1 and Stp2 transcription factors in Candida albicans places virulence factors required for proper nutrient acquisition under amino acid control. Mol. Cell. Biol. 2005, 25:9435-9446.
70. Noble S.M., et al. Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat. Genet. 2010, 42:590-598.
71. Dagley M.J., et al. Cell wall integrity is linked to mitochondria and phospholipid homeostasis in Candida albicans through the activity of the post- transcriptional regulator Ccr4-Pop2. Mol. Microbiol. 2011, 79:968-989.
72. Nobile C.J., et al. A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 2012, 148:126-138.
73. Vylkova S., et al. The fungal pathogen Candida albicans autoinduces hyphal morphogenesis by raising extracellular pH. MBio 2011, 2. e00055-11.
74. Losse J., et al. Role of pH-regulated antigen 1 of Candida albicans in the fungal recognition and antifungal response of human neutrophils. Mol. Immunol. 2011, 48:2135-2143.
75. Brown G.D. Innate antifungal immunity: the key role of phagocytes. Annu. Rev. Immunol. 2011, 29:1-21.
76. Gow N.A.R., et al. Candida albicans morphogenesis and the host defence: discriminating invasion from colonization. Nat. Rev. Microbiol. 2012, 10:112-122.
77. Fernandez-Arenas E., et al. Candida albicans actively modulates intracellular membrane trafficking in mouse macrophage phagosomes. Cell. Microbiol. 2009, 11:560-589.
78. Brothers K.M., et al. NADPH oxidase-driven phagocyte recruitment controls Candida albicans filamentous growth and prevents mortality. PLoS Pathog. 2013, 9:e1003634.
79. + flux. Nature 2002, 416:291-297.
80. McKenzie C.G.J., et al. Contribution of Candida albicans cell wall components to recognition by and escape from murine macrophages. Infect. Immun. 2010, 78:1650-1658.
81. Lewis L.E., et al. Stage specific assessment of Candida albicans phagocytosis by macrophages identifies cell wall composition and morphogenesis as key determinants. PLoS Pathog. 2012, 8:e1002578.
82. Ene I.V., et al. Growth of Candida albicans cells on the physiologically relevant carbon source, lactate, affects their recognition and phagocytosis by immune cells. Infect. Immun. 2013, 81:238-248.
83. Netea M.G., et al. Immune sensing of Candida albicans: cooperative recognition of mannans and glucan by lectin and Toll-like receptors. J. Clin. Invest. 2006, 116:1642-1650.
84. Adams E.L., et al. Differential high affinity interaction of Dectin-1 with natural or synthetic glucans is dependent upon primary structure and is influenced by polymer chain length and side chain branching. J. Pharmacol. Exp. Ther. 2008, 325:115-123.
85. Lowman D.W., et al. Novel structural features in Candida albicans hyphal glucan provide a basis for differential innate immune recognition of hyphae versus yeast. J. Biol. Chem. 2014, 289:3432-3443.
86. Lohse M.B., Johnson A.D. differential phagocytosis of white versus opaque Candida albicans by Drosophila and mouse phagocytes. PLoS ONE 2008, 3:e1473.
87. Citiulo F., et al. Candida albicans scavenges host zinc via Pra1 during endothelial invasion. PLoS Pathog. 2012, 8:e1002777.
88. Almeida R.S., et al. The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog. 2008, 4:e1000217.
89. Marakalala M.J., et al. Differential adaptation of Candida albicans in vivo modulates immune recognition by Dectin- 1. PLoS Pathog. 2013, 9:e1003315.
90. Delgoffe G.M., et al. The kinase mTOR regulates the differentiation of helper T cells through the selective activation of signaling by mTORC1 and mTORC2. Nat. Immunol. 2011, 12:295-303.
91. Kim J.S., et al. Natural and inducible TH17 cells are regulated differently by Akt and mTOR pathways. Nat. Immunol. 2013, 14:611-618.
92. Tannahill G.M., et al. Succinate is an inflammatory signal that induces IL-1β through HIF-1α. Nature 2013, 496:238-242.
93. Moyes D.L., et al. Protection against epithelial damage during Candida albicans infection is mediated by PI3K/Akt and mammalian target of rapamycin signaling. J. Infect. Dis. 2014, 209:1816-1826.
94. Zelante T., et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 2013, 39:372-385.
95. Odds F.C., et al. Survival in experimental Candida albicans infections depends on inoculum growth conditions as well as animal host. Microbiology 2000, 146:1881-1889.
96. Lee K.K., et al. Elevated cell wall chitin in Candida albicans confers echinocandin resistance in vivo. Antimicrob. Agents Chemother. 2011, 56:208-217.
97. Baker H., et al. Rapamycin (AY-22, 989), a new antifungal antibiotic. III. In vitro and in vivo evaluation. J. Antibiot. (Tokyo) 1978, 31:539-545.
98. Potrykus J., et al. Fungal iron availability during deep seated candidiasis defined by a complex interplay of systemic and local events. PLoS Pathog. 2013, 9:e1003676.
99. Enjalbert B., et al. A multifunctional, synthetic Gaussia princeps luciferase reporter for live imaging of Candida albicans infections. Infect. Immun. 2009, 77:4847-4858.
100. Delgado-Silva Y., et al. Participation of Candida albicans transcription factor RLM1 in cell wall biogenesis and virulence. PLoS ONE 2014, 9:e86270.
101. Cutfield S.M., et al. The crystal structure of a major secreted aspartic proteinase from Candida albicans in complexes with two inhibitors. Structure 1995, 3:1261-1271.