Candida albicans dimorphism as a therapeutic target

Expert Review of Anti-Infective Therapy

Volumn 10, Issue 1, 2012, Pages 85-93

  Jacobsen, Ilse D ^a   Wilson, Duncan ^a   Wächtler, Betty ^a   Brunke, Sascha ^a,b   Naglik, Julian R ^c   Hube, Bernhard ^a,d  

^a HANS KNÖLL INSTITUTE   (Germany)

^b JENA UNIVERSITY HOSPITAL   (Germany)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

adhesion; commensal; damage; dimorphism; hyphae; immune response; infection; invasion; phagocytes; yeast

Indexed keywords

ANTIFUNGAL AGENT; FARNESOL; GELDANAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; NISIN; NISIN Z; UNCLASSIFIED DRUG;

ANTIFUNGAL ACTIVITY; BLOODSTREAM INFECTION; CANDIDA ALBICANS; CANDIDIASIS; CELL INTERACTION; DRUG EFFECT; DRUG MECHANISM; DRUG TARGETING; FUNGAL CELL CULTURE; FUNGAL GENE; FUNGAL MORPHOLOGY; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS HYPHAE; FUNGUS TRANSMISSION; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOCOMPETENT CELL; INFECTION RISK; INNATE IMMUNITY; INTRACELLULAR SIGNALING; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PHAGOCYTOSIS; REVIEW; THRUSH;

CANDIDA ALBICANS; CANDIDIASIS; GENE EXPRESSION REGULATION, FUNGAL; HUMANS; HYPHAE; VIRULENCE; VIRULENCE FACTORS;

EID: 83455236481     PISSN: 14787210     EISSN: 17448336     Source Type: Journal    
DOI: 10.1586/eri.11.152     Document Type: Review

References (86)

1. Berman J, Sudbery PE. Candida albicans: a molecular revolution built on lessons from budding yeast. Nat. Rev. Genet. 3(12), 918-930 (2002).
2. Martin SW, Douglas LM, Konopka JB. Cell cycle dynamics and quorum sensing in Candida albicans chlamydospores are distinct from budding and hyphal growth. Eukaryot. Cell 4(7), 1191-1202 (2005).
3. Citiulo F, Moran GP, Coleman DC, Sullivan DJ. Purification and germination of Candida albicans and Candida dubliniensis chlamydospores cultured in liquid media. FEMS Yeast Res. 9(7), 1051-1060 (2009).
4. Miller MG, Johnson AD. White-opaque switching in Candida albicans is controlled by mating-type locus homeodomain proteins and allows efficient mating. Cell 110(3), 293-302 (2002).
5. Daniels KJ, Srikantha T, Lockhart SR, Pujol C, Soll DR. Opaque cells signal white cells to form biofilms in Can. Albicans. EMBO J. 25(10), 2240-2252 (2006).
6. Biswas S, Van Dijck P, Datta A. Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans. Microbiol. Mol. Biol. Rev. 71(2), 348-376 (2007).
7. Whiteway M, Bachewich C. Morphogenesis in Candida albicans. Ann. Rev. Microbiol. 61, 529-553 (2007).
8. Shapiro RS, Cowen L. Coupling temperature sensing and development: Hsp90 regulates morphogenetic signalling in Candida albicans. Virulence 1(1), 45-48 (2010).
9. Sudbery PE. Growth of Candida albicans hyphae. Nat. Rev. Microbiol. 9(10), 737-748 (2011).
10. Odds FC. Candida species and virulence. ASM News 60, 313-318 (1994).
11. Perlroth J, Choi B, Spellberg B. Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med. Mycol. 45(4), 321-346 (2007).
12. Gow NA, Brown AJ, Odds FC. Fungal morphogenesis and host invasion. Curr. Opin. Microbiol. 5(4), 366-371 (2002).
13. Pope LM, Cole GT. Comparative studies of gastrointestinal colonization and systemic spread by Candida albicans and nonlethal yeast in the infant mouse. Scan. Electron. Microsc. (Pt 4), 1667-1676 (1982).
14. Ray TL, Payne CD. Scanning electron microscopy of epidermal adherence and cavitation in murine candidiasis: a role for Candida acid proteinase. Infect. Immun. 56(8), 1942-1949 (1988).
15. Saville SP, Lazzell AL, Monteagudo C, Lopez-Ribot JL. Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot. Cell 2(5), 1053-1060 (2003).
16. Odds FC. Morphogenesis in Candida, with special reference to C. albicans. In: Candida and Candidosis. A Review and Bibliography. Odds FC (Ed.). Ballière Tindall, London, UK, 42-59 (1988).
17. Lionakis MS, Lim JK, Lee CC, Murphy PM. Organ-specific innate immune responses in a mouse model of invasive candidiasis. J. Innate. Immun. 3(2), 180-199 (2011).
18. Mavor AL, Thewes S, Hube B. Systemic fungal infections caused by Candida species: epidemiology, infection process and virulence attributes. Curr. Drug Targets 6(8), 863-874 (2005).
19. Fradin C, De Groot P, MacCallum D, et al. Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol. Microbiol. 56(2), 397-415 (2005).
20. White SJ, Rosenbach A, Lephart P, et al. Self-regulation of Candida albicans population size during GI colonization. PLoS Pathog. 3(12), e184 (2007).
21. Lachke SA, Lockhart SR, Daniels KJ, Soll DR. Skin facilitates Candida albicans mating. Infect. Immun. 71(9), 4970-4976 (2003).
22. Uppuluri P, Chaturvedi AK, Srinivasan A, et al. Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog. 6(3), e1000828 (2010).
23. Naglik JR, Fostira F, Ruprai J, Staab JF, Challacombe SJ, Sundstrom P. Candida albicans HWP1 gene expression and host antibody responses in colonization and disease. J. Med. Microbiol. 55(Pt 10), 1323-1327 (2006).
24. Naglik JR, Rodgers CA, Shirlaw PJ, et al. 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(3), 469-479 (2003).
25. Mochon AB, Ye J, Kayala MA, et al. Serological profiling of a Candida albicans protein microarray reveals permanent host-pathogen interplay and stage-specific responses during candidemia. PLoS Pathog. 6(3), e1000827 (2010).
26. Sosinska GJ, de Groot PW, Teixeira de Mattos MJ, et al. Hypoxic conditions and iron restriction affect the cell-wall proteome of Candida albicans grown under vagina-simulative conditions. Microbiology (Read. Engl.), 154(Pt 2), 510-520 (2008).
27. Andaluz E, Ciudad T, Gomez-Raja J, Calderone R, Larriba G. Rad52 depletion in Candida albicans triggers both the DNA-damage checkpoint and filamentation accompanied by but independent of expression of hypha-specific genes. Mol. Microbiol. 59(5), 1452-1472 (2006).
28. Rosenbach A, Dignard D, Pierce JV, Whiteway M, Kumamoto CA. Adaptations of Candida albicans for growth in the mammalian intestinal tract. Eukaryot. Cell 9(7), 1075-1086 (2010).
29. Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cacciapuoti A, Fink GR. Nonfilamentous C. albicans mutants are avirulent. Cell 90(5), 939-949 (1997).
30. Zheng X, Wang Y. Hgc1, a novel hypha-specific G1 cyclin-related protein regulates Candida albicans hyphal morphogenesis. EMBO J. 23(8), 1845-1856 (2004).
31. Murad AM, Leng P, Straffon M, et al. NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J. 20(17), 4742-4752 (2001).
32. Braun BR, Kadosh D, Johnson AD. NRG1, a repressor of filamentous growth in C. albicans, is down-regulated during filament induction. EMBO J. 20(17), 4753-4761 (2001).
33. Braun BR, Johnson AD. Control of filament formation in Candida albicans by the transcriptional repressor TUP1 Sci. 277(5322), 105-109 (1997).
34. Shen J, Cowen LE, Griffin AM, Chan L, Kohler JR. The Candida albicans pescadillo homolog is required for normal hypha-to-yeast morphogenesis and yeast proliferation. Proc. Natl Acad. Sci. USA 105(52), 20918-20923 (2008).
35. Martin R, Moran GP, Jacobsen ID, et al. The Candida albicans-specific gene EED1 encodes a key regulator of hyphal extension. PLoS One 6(4), e18394 (2011).
36. Zakikhany K, Naglik JR, Schmidt-Westhausen A, Holland G, Schaller M, Hube B. In vivo transcript profiling of Candida albicans identifies a gene essential for interepithelial dissemination. Cell Microbiol. 9(12), 2938-2954 (2007).
37. Banerjee M, Thompson DS, Lazzell A, et al. UME6, a novel filament-specific regulator of Candida albicans hyphal extension and virulence. Mol. Biol. Cell 19(4), 1354-1365 (2008).
38. Loeb JD, Sepulveda-Becerra M, Hazan I, Liu H. A G1 cyclin is necessary for maintenance of filamentous growth in Candida albicans. Mol. Cell Biol. 19(6), 4019-4027 (1999).
39. Dalle F, Wachtler B, LOllivier C, et al. Cellular interactions of Candida albicans with human oral epithelial cells and enterocytes. Cell. Microbiol. 12(2), 248-271 (2010).
40. Wächtler B, Wilson D, Haedicke K, Dalle F, Hube B. From attachment to damage: defined genes of Candida albicans mediate adhesion, invasion and damage during interaction with oral epithelial cells. PLoS One 6(2), e17046 (2011).
41. Phan QT, Myers CL, Fu Y, et al. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol. 5(3), e64 (2007).
42. Moreno-Ruiz E, Galan-Diez M, Zhu W, et al. Candida albicans internalization by host cells is mediated by a clathrin-dependent mechanism. Cell Microbiol. 11(8), 1179-1189 (2009).
43. Almeida RS, Brunke S, Albrecht A, et al. The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog. 4(11), e1000217 (2008).
44. Naglik JR, Challacombe SJ, Hube B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol. Mol. Biol. Rev. 67(3), 400-428 (2003).
45. Rubin-Bejerano I, Fraser I, Grisafi P, Fink GR. Phagocytosis by neutrophils induces an amino acid deprivation response in Saccharomyces cerevisiae and Candida albicans. Proc. Natl Acad. Sci. USA 100(19), 11007-11012 (2003).
46. Fradin C, Kretschmar M, Nichterlein T, Gaillardin C, dEnfert C, Hube B. Stage-specific gene expression of Candida albicans in human blood. Mol. Microbiol. 47(6), 1523-1543 (2003).
47. Lorenz MC, Bender JA, Fink GR. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot. Cell 3(5), 1076-1087 (2004).
48. Martchenko M, Alarco AM, Harcus D, Whiteway M. Superoxide dismutases in Candida albicans: transcriptional regulation and functional characterization of the hyphal-induced SOD5 gene. Mol. Biol. Cell 15(2), 456-467 (2004).
49. Frohner IE, Bourgeois C, Yatsyk K, Majer O, Kuchler K. C. albicans cell surface superoxide dismutases degrade host-derived reactive oxygen species to escape innate immune surveillance. Mol. Microbiol. 71(1), 240-252 (2008).
50. Wilson D, Hube B. Hgc1 mediates dynamic Candida albicans-endothelium adhesion events during circulation. Eukaryot. Cell 9(2), 278-287 (2010).
51. Grubb SE, Murdoch C, Sudbery PE, Saville SP, Lopez-Ribot JL, Thornhill MH. Adhesion of Candida albicans to endothelial cells under physiological conditions of flow. Infect. Immun. 77(9), 3872-3878 (2009).
52. Hube B. From commensal to pathogen: stage-and tissue-specific gene expression of Candida albicans. Curr. Opin. Microbiol. 7(4), 336-341 (2004).
53. Mitchell A, Romano GH, Groisman B, et al. Adaptive prediction of environmental changes by microorganisms. Nature 460(7252), 220-224 (2009).
54. Saville SP, Lazzell AL, Chaturvedi AK, Monteagudo C, Lopez-Ribot JL. Use of a genetically engineered strain to evaluate the pathogenic potential of yeast cell and filamentous forms during Candida albicans systemic infection in immunodeficient mice. Infect. Immun. 76(1), 97-102 (2008).
55. Koh AY, Kohler JR, Coggshall KT, Van Rooijen N, Pier GB. Mucosal damage and neutropenia are required for Candida albicans dissemination. PLoS Pathogens 4(2), e35 (2008).
56. MacCallum DM. Massive induction of innate immune response to Candida albicans in the kidney in a murine intravenous challenge model. FEMS Yeast Res. 9(7), 1111-1122 (2009).
57. MacCallum DM, Castillo L, Brown AJ, Gow NA, Odds FC. Early-expressed chemokines predict kidney immunopathology in experimental disseminated Candida albicans infections. PLoS One, 4(7), e6420 (2009).
58. Moyes DL, Runglall M, Murciano C, et al. A biphasic innate immune MAPK response discriminates between the yeast and hyphal forms of Candida albicans in epithelial cells. Cell Host Microbe 8(3), 225-235 (2010).
59. Weindl G, Naglik JR, Kaesler S, et al. Human epithelial cells establish direct antifungal defense through TLR4-mediated signaling. J. Clin. Invest. 117(12), 3664-3672 (2007).
60. dOstiani CF, Del Sero G, Bacci A, et al. 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(10), 1661-1674 (2000).
61. Wozniok I, Hornbach A, Schmitt C, et al. Induction of ERK-kinase signalling triggers morphotype-specific killing of Candida albicans filaments by human neutrophils. Cell Microbiol. 10(3), 807-820 (2008).
62. Urban CF, Reichard U, Brinkmann V, Zychlinsky A. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol. 8(4), 668-676 (2006).
63. Marcil A, Gadoury C, Ash J, Zhang J, Nantel A, Whiteway M. Analysis of PRA1 and its relationship to Candida albicans-macrophage interactions. Infect. Immun. 76(9), 4345-4358 (2008).
64. Keppler-Ross S, Douglas L, Konopka JB, Dean N. Recognition of yeast by murine macrophages requires mannan but not glucan. Eukaryot. Cell 9(11), 1776-1787 (2010).
65. Netea MG, Gijzen K, Coolen N, et al. Human dendritic cells are less potent at killing Candida albicans than both monocytes and macrophages. Microbes Infect. 6(11), 985-989 (2004).
66. Torosantucci A, Chiani P, Cassone A. Differential chemokine response of human monocytes to yeast and hyphal forms of Candida albicans and its relation to the b-1,6 glucan of the fungal cell wall. J. Leukoc. Biol. 68(6), 923-932 (2000).
67. Chaffin WL. Candida albicans cell wall proteins. Microbiol. Mol. Biol. Rev. 72(3), 495-544 (2008).
68. Netea MG, Brown GD, Kullberg BJ, Gow NA. An integrated model of the recognition of Candida albicans by the innate immune system. Nat. Rev. Microbiol. 6(1), 67-78 (2008).
69. Jouault T, Sarazin A, Martinez-Esparza M, Fradin C, Sendid B, Poulain D. Host responses to a versatile commensal: PAMPs and PRRs interplay leading to tolerance or infection by Candida albicans. Cell Microbiol. 11(7), 1007-1015 (2009).
70. Romani L, Montagnoli C, Bozza S, et al. The exploitation of distinct recognition receptors in dendritic cells determines the full range of host immune relationships with Candida albicans. Int. Immunol. 16(1), 149-161 (2004).
71. Wheeler RT, Kombe D, Agarwala SD, Fink GR. Dynamic, morphotype-specific Candida albicans b-glucan exposure during infection and drug treatment. PLoS Pathogens 4(12), e1000227 (2008).
72. Wheeler RT, Fink GR. A drug-sensitive genetic network masks fungi from the immune system. PLoS Pathogens 2(4), e35 (2006).
73. Pietrella D, Rachini A, Pandey N, et al. The Inflammatory response induced by aspartic proteases of Candida albicans is independent of proteolytic activity. Infect. Immun. 78(11), 4754-4762 (2010).
74. Alksne LE, Projan SJ. Bacterial virulence as a target for antimicrobial chemotherapy. Curr. Opin. Biotechnol. 11(6), 625-636 (2000).
75. Gauwerky K, Borelli C, Korting HC. Targeting virulence: a new paradigm for antifungals. Drug Discov. Today 14(3-4), 214-222 (2009).
76. Shareck J, Belhumeur P. Modulation of morphogenesis in Candida albicans by various small molecules. Eukaryot. Cell 10(8), 1004-1012 (2011).
77. Fidel PL Jr. History and update on host defense against vaginal candidiasis. Am. J. Reprod. Immunol. 57(1), 2-12 (2007).
78. Moyes DL, Naglik JR. Mucosal immunity and Candida albicans infection. Clin. Dev. Immunol. 2011, 346307 (2011).
79. Saville SP, Lazzell AL, Bryant AP, et al. Inhibition of filamentation can be used to treat disseminated candidiasis. Antimicrob. Agents Chemother. 50(10), 3312-3316 (2006).
80. Spiering MJ, Moran GP, Chauvel M, et al. Comparative transcript profiling of Candida albicans and Candida dubliniensis identifies SFL2, a C. albicans gene required for virulence in a reconstituted epithelial infection model. Eukaryot. Cell 9(2), 251-265 (2010).
81. Cowen LE, Singh SD, Kohler JR, et al. Harnessing Hsp90 function as a powerful, broadly effective therapeutic strategy for fungal infectious disease. Proc. Natl Acad. Sci. USA 106(8), 2818-2823 (2009).
82. Akerey B, Le-Lay C, Fliss I, Subirade M, Rouabhia M. In vitro efficacy of nisin Z against Candida albicans adhesion and transition following contact with normal human gingival cells. J. Appl. Microbiol. 107(4), 1298-1307 (2009).
83. Hisajima T, Maruyama N, Tanabe Y, et al. Protective effects of farnesol against oral candidiasis in mice. Microbiol. Immunol. 52(7), 327-333 (2008).
84. Wächtler B, Wilson D, Hube B. Candida albicans adhesion to and invasion and damage of vaginal epithelial cells: stage-specific inhibition by clotrimazole and bifonazole. Antimicrob. Agents Chemother. 55(9), 4436-4439 (2011).
85. Langford ML, Atkin AL, Nickerson KW. Cellular interactions of farnesol, a quorum-sensing molecule produced by Candida albicans. Future Microbiol. 4(10), 1353-1362 (2009).
86. Phan QT, Belanger PH, Filler SG. Role of hyphal formation in interactions of Candida albicans with endothelial cells. Infect. Immun. 68(6), 3485-3490 (2000).