Distinct roles of Candida albicans-specific genes in host-pathogen interactions

Eukaryotic Cell

Volumn 13, Issue 8, 2014, Pages 977-989

  Wilson, Duncan ^a,d   Mayer, François L ^a,e   Miramón, Pedro ^a,f   Citiulo, Francesco ^a   Slesiona, Silvia ^a   Jacobsen, Ilse D ^a   Hubea, Bernhard ^a,b,c  

^a HANS KNÖLL INSTITUTE   (Germany)

^b JENA UNIVERSITY HOSPITAL   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^d UNIVERSITY OF ABERDEEN   (United Kingdom)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^f UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANDIDA ALBICANS;

FUNGAL PROTEIN; INTERLEUKIN 1BETA;

AMINO ACID SEQUENCE; ANIMAL; BAGG ALBINO MOUSE; CANDIDA ALBICANS; CANDIDIASIS; CHEMISTRY; FEMALE; FUNGAL GENE; FUNGUS HYPHAE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; KIDNEY; MACROPHAGE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PATHOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CANDIDA ALBICANS; CANDIDIASIS; FEMALE; FUNGAL PROTEINS; GENE EXPRESSION; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; HOST-PATHOGEN INTERACTIONS; HUMANS; HYPHAE; INTERLEUKIN-1BETA; KIDNEY; MACROPHAGES; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA;

EID: 84907454603     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00051-14     Document Type: Article

References (54)

1. Blackwell M. 2011. The fungi: 1, 2, 3. 5.1 million species? Am. J. Bot. 98:426-438. http://dx.doi.org/10.3732/ajb.1000298.
2. Mora C, Tittensor DP, Adl S, Simpson AG, Worm B. 2011. How many species are there on Earth and in the ocean? PLoS Biol. 9:e1001127. http: //dx.doi.org/10.1371/journal.pbio.1001127.
3. Brown GD, Denning DW, Levitz SM. 2012. Tackling human fungal infections. Science 336:647. http://dx.doi.org/10.1126/science.1222236.
4. Brown GD, Denning DW, Gow NA, Levitz SM, Netea MG, White TC. 2012. Hidden killers: human fungal infections. Sci. Transl. Med. 4:165rv13. http://dx.doi.org/10.1126/scitranslmed.3004404.
5. Ruhnke M. 2002. Skin and mucous membrane infections, p 307-325. In Calderone RA (ed), Candida and candidiasis. ASM Press, Washington, DC.
6. Perlroth J, Choi B, Spellberg B. 2007. Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med. Mycol. 45:321-346. http: //dx.doi.org/10.1080/13693780701218689.
7. Mayer FL, Wilson D, Hube B. 2013. Candida albicans pathogenicity mechanisms. Virulence 4:119-128. http://dx.doi.org/10.4161/viru.22913.
8. Fitzpatrick DA, Logue ME, Stajich JE, Butler G. 2006. A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol. Biol. 6:99. http://dx.doi.org/10.1186/1471-2148 -6-99.
9. Bowman BH, Taylor JW, White TJ. 1992. Molecular evolution of the fungi: human pathogens. Mol. Biol. Evol. 9:893-904.
10. Gola S, Martin R, Walther A, Dunkler A, Wendland J. 2003. New modules for PCR-based gene targeting in Candida albicans: rapid and efficient gene targeting using 100 bp of flanking homology region. Yeast 20:1339-1347. http://dx.doi.org/10.1002/yea.1044.
11. Walther A, Wendland J. 2003. An improved transformation protocol for the human fungal pathogen Candida albicans. Curr. Genet. 42:339-343. http://dx.doi.org/10.1007/s00294-002-0349-0.
12. Murad AM, Lee PR, Broadbent ID, Barelle CJ, Brown AJ. 2000. CIp10, an efficient and convenient integrating vector for Candida albicans. Yeast 16:325-327. http://dx.doi.org/10.1002/1097-0061(20000315)16:4_325:: AID-YEA5383.0.CO;2-#.
13. Mayer FL, Wilson D, Jacobsen ID, Miramon P, Grosse K, Hube B. 2012. The novel Candida albicans transporter Dur31 is a multi-stage pathogenicity factor. PLoS Pathog. 8:e1002592. http://dx.doi.org/10.1371 /journal.ppat.1002592.
14. Wachtler B, Wilson D, Haedicke K, Dalle F, Hube B. 2011. From attachment to damage: defined genes of Candida albicans mediate adhesion, invasion and damage during interaction with oral epithelial cells. PLoS One 6:e17046. http://dx.doi.org/10.1371/journal.pone.0017046.
15. Rossignol T, Lechat P, Cuomo C, Zeng Q, Moszer I, d'Enfert C. 2008. CandidaDB: a multi-genome database for Candida species and related Saccharomycotina. Nucleic Acids Res. 36:D557-D561. http://dx.doi.org /10.1093/nar/gkm1010.
16. Inglis DO, Arnaud MB, Binkley J, Shah P, Skrzypek MS, Wymore F, Binkley G, Miyasato SR, Simison M, Sherlock G. 2012. The Candida genome database incorporates multiple Candida species: multispecies search and analysis tools with curated gene and protein information for Candida albicans and Candida glabrata. Nucleic Acids Res. 40:D667- D674. http://dx.doi.org/10.1093/nar/gkr945.
17. Falkow S. 1988. Molecular Koch's postulates applied to microbial pathogenicity. Rev. Infect. Dis. 10(Suppl 2):S274-S276.
18. Zakikhany K, Naglik JR, Schmidt-Westhausen A, Holland G, Schaller M, Hube B. 2007. In vivo transcript profiling of Candida albicans identifies a gene essential for interepithelial dissemination. Cell. Microbiol. 9:2938-2954. http://dx.doi.org/10.1111/j.1462-5822.2007.01009.x.
19. Thewes S, Kretschmar M, Park H, Schaller M, Filler SG, Hube B. 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. 63:1606-1628. http://dx.doi.org/10.1111/j. 1365-2958.2007.05614.x.
20. De Groot PW, Hellingwerf KJ, Klis FM. 2003. Genome-wide identification of fungal GPI proteins. Yeast 20:781-796. http://dx.doi.org/10.1002 /yea.1007.
21. Nather K, Munro CA. 2008. Generating cell surface diversity in Candida albicans and other fungal pathogens. FEMS Microbiol. Lett. 285:137-145. http://dx.doi.org/10.1111/j.1574-6968.2008.01263.x.
22. McDonagh A, Fedorova ND, Crabtree J, Yu Y, Kim S, Chen D, Loss O, Cairns T, Goldman G, Armstrong-James D, Haynes K, Haas H, Schrettl M, May G, Nierman WC, Bignell E. 2008. Sub-telomere directed gene expression during initiation of invasive aspergillosis. PLoS Pathog. 4:e1000154. http://dx.doi.org/10.1371/journal.ppat.1000154.
23. Kumamoto CA. 2008. Niche-specific gene expression during C. albicans infection. Curr. Opin. Microbiol. 11:325-330. http://dx.doi.org/10.1016/j. mib.2008.05.008.
24. Southern P, Horbul J, Maher D, Davis DA. 2008. C. albicans colonization of human mucosal surfaces. PLoS One 3:e2067. http://dx.doi.org/10. 1371/journal.pone.0002067.
25. Miramon P, Dunker C, Windecker H, Bohovych IM, Brown AJ, Kurzai O, Hube B. 2012. 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 7:e52850. http://dx.doi.org/10.1371/journal.pone.0052850.
26. Spellberg B, Ibrahim AS, Edwards JE, Jr, Filler SG. 2005. Mice with disseminated candidiasis die of progressive sepsis. J. Infect. Dis. 192:336- 343. http://dx.doi.org/10.1086/430952.
27. Cai B, Deitch EA, Ulloa L. 2010. Novel insights for systemic inflammation in sepsis and hemorrhage. Mediators Inflamm. 2010:642462. http: //dx.doi.org/10.1155/2010/642462.
28. van de Veerdonk FL, Kullberg BJ, Netea MG. 2010. Pathogenesis of invasive candidiasis. Curr. Opin. Crit. Care 16:453-459. http://dx.doi.org /10.1097/MCC.0b013e32833e046e.
29. Netea MG, Brown GD, Kullberg BJ, Gow NA. 2008. An integrated model of the recognition of Candida albicans by the innate immune system. Nat. Rev. Microbiol. 6:67-78. http://dx.doi.org/10.1038/nrmicro1815.
30. Butler G, Rasmussen MD, Lin MF, Santos MA, Sakthikumar S, Munro CA, Rheinbay E, Grabherr M, Forche A, Reedy JL, Agrafioti I, Arnaud MB, Bates S, Brown AJ, Brunke S, Costanzo MC, Fitzpatrick DA, de Groot PW, Harris D, Hoyer LL, Hube B, Klis FM, Kodira C, Lennard N, Logue ME, Martin R, Neiman AM, Nikolaou E, Quail MA, Quinn J, Santos MC, Schmitzberger FF, Sherlock G, Shah P, Silverstein KA, Skrzypek MS, Soll D, Staggs R, Stansfield I, Stumpf MP, Sudbery PE, Srikantha T, Zeng Q, Berman J, Berriman M, Heitman J, Gow NA, Lorenz MC, Birren BW, Kellis M, Cuomo CA. 2009. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459:657-662. http://dx.doi.org/10.1038/nature08064.
31. Noble SM, French S, Kohn LA, Chen V, Johnson AD. 2010. Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat. Genet. 42:590-598. http: //dx.doi.org/10.1038/ng.605.
32. Kumamoto CA, Vinces MD. 2005. Contributions of hyphae and hyphaco- regulated genes to Candida albicans virulence. Cell. Microbiol. 7:1546-1554. http://dx.doi.org/10.1111/j.1462-5822.2005.00616.x.
33. Jacobsen ID, Wilson D, Wachtler B, Brunke S, Naglik JR, Hube B. 2012. Candida albicans dimorphism as a therapeutic target. Expert Rev. Anti Infect. Ther. 10:85-93. http://dx.doi.org/10.1586/eri.11.152.
34. Lee SA, Wormsley S, Kamoun S, Lee AF, Joiner K, Wong B. 2003. An analysis of the Candida albicans genome database for soluble secreted proteins using computer-based prediction algorithms. Yeast 20:595-610. http://dx.doi.org/10.1002/yea.988.
35. Brown GD, Gordon S. 2001. Immune recognition. A new receptor for beta-glucans. Nature 413:36-37. http://dx.doi.org/10.1038/35092620.
36. Saijo S, Ikeda S, Yamabe K, Kakuta S, Ishigame H, Akitsu A, Fujikado N, Kusaka T, Kubo S, Chung SH, Komatsu R, Miura N, Adachi Y, Ohno N, Shibuya K, Yamamoto N, Kawakami K, Yamasaki S, Saito T, Akira S, Iwakura Y. 2010. Dectin-2 recognition of alpha-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity 32:681-691. http://dx.doi.org/10.1016/j. immuni.2010.05.001.
37. Gasparoto TH, Tessarolli V, Garlet TP, Torres SA, Garlet GP, Da Silva JS, Campanelli AP. 2010. Absence of functional TLR4 impairs response of macrophages after Candida albicans infection. Med. Mycol. 48:1009- 1017. http://dx.doi.org/10.3109/13693786.2010.481292.
38. Netea MG, Van Der Graaf CA, Vonk AG, Verschueren I, Van Der Meer JW, Kullberg BJ. 2002. The role of Toll-like receptor (TLR) 2 and TLR4 in the host defense against disseminated candidiasis. J. Infect. Dis. 185:1483- 1489. http://dx.doi.org/10.1086/340511.
39. Netea MG, Gow NA, Joosten LA, Verschueren I, van der Meer JW, Kullberg BJ. 2010. Variable recognition of Candida albicans strains by TLR4 and lectin recognition receptors. Med. Mycol. 48:897-903. http://dx. doi.org/10.3109/13693781003621575.
40. Kumar H, Kumagai Y, Tsuchida T, Koenig PA, Satoh T, Guo Z, Jang MH, Saitoh T, Akira S, Kawai T. 2009. Involvement of the NLRP3 inflammasome in innate and humoral adaptive immune responses to fungal beta-glucan. J. Immunol. 183:8061-8067. http://dx.doi.org/10.4049 /jimmunol.0902477.
41. Pietrella D, Rachini A, Pandey N, Schild L, Netea M, Bistoni F, Hube B, Vecchiarelli A. 2010. The inflammatory response induced by aspartic proteases of Candida albicans is independent of proteolytic activity. Infect. Immun. 78:4754-4762. http://dx.doi.org/10.1128/IAI.00789-10.
42. Mech F, Wilson D, Lehnert T, Hube B, Thilo Figge M. 2014. Epithelial invasion outcompetes hypha development during Candida albicans infection as revealed by an image-based systems biology approach. Cytometry A 85:126-139. http://dx.doi.org/10.1002/cyto.a.22418.
43. Veses V, Richards A, Gow NA. 2009. Vacuole inheritance regulates cell size and branching frequency of Candida albicans hyphae. Mol. Microbiol. 71:505-519. http://dx.doi.org/10.1111/j.1365-2958.2008.06545.x.
44. Palanisamy SK, Ramirez MA, Lorenz M, Lee SA. 2010. Candida albicans PEP12 is required for biofilm integrity and in vivo virulence. Eukaryot. Cell 9:266-277. http://dx.doi.org/10.1128/EC.00295-09.
45. Hausauer DL, Gerami-Nejad M, Kistler-Anderson C, Gale CA. 2005. Hyphal guidance and invasive growth in Candida albicans require the Ras-like GTPase Rsr1p and its GTPase-activating protein Bud2p. Eukaryot. Cell 4:1273-1286. http://dx.doi.org/10.1128/EC.4.7.1273-1286. 2005.
46. Brand A, Vacharaksa A, Bendel C, Norton J, Haynes P, Henry-Stanley M, Wells C, Ross K, Gow NA, Gale CA. 2008. An internal polarity landmark is important for externally induced hyphal behaviors in Candida albicans. Eukaryot. Cell 7:712-720. http://dx.doi.org/10.1128/EC. 00453-07.
47. Nobile CJ, Andes DR, Nett JE, Smith FJ, Yue F, Phan QT, Edwards JE, Filler SG, Mitchell AP. 2006. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog. 2:e63. http://dx.doi.org/10.1371/journal.ppat.0020063.
48. Uhl MA, Biery M, Craig N, Johnson AD. 2003. Haploinsufficiencybased large-scale forward genetic analysis of filamentous growth in the diploid human fungal pathogen C. albicans. EMBO J. 22:2668-2678. http: //dx.doi.org/10.1093/emboj/cdg256.
49. Xu D, Jiang B, Ketela T, Lemieux S, Veillette K, Martel N, Davison J, Sillaots S, Trosok S, Bachewich C, Bussey H, Youngman P, Roemer T. 2007. Genome-wide fitness test and mechanism-of-action studies of inhibitory compounds in Candida albicans. PLoS Pathog. 3:e92. http://dx. doi.org/10.1371/journal.ppat.0030092.
50. Zavrel M, Majer O, Kuchler K, Rupp S. 2012. Transcription factor Efg1 shows a haploinsufficiency phenotype in modulating the cell wall architecture and immunogenicity of Candida albicans. Eukaryot. Cell 11:129- 140. http://dx.doi.org/10.1128/EC.05206-11.
51. Lay J, Henry LK, Clifford J, Koltin Y, Bulawa CE, Becker JM. 1998. Altered expression of selectable marker URA3 in gene-disrupted Candida albicans strains complicates interpretation of virulence studies. Infect. Immun. 66:5301-5306.
52. Bain JM, Stubberfield C, Gow NA. 2001. Ura-status-dependent adhesion of Candida albicans mutants. FEMS Microbiol. Lett. 204:323-328. http: //dx.doi.org/10.1111/j.1574-6968.2001.tb10905.x.
53. Staab JF, Sundstrom P. 2003. URA3 as a selectable marker for disruption and virulence assessment of Candida albicans genes. Trends Microbiol. 11:69-73. http://dx.doi.org/10.1016/S0966-842X(02)00029-X.
54. Sharkey LL, Liao WL, Ghosh AK, Fonzi WA. 2005. Flanking direct repeats of hisG alter URA3 marker expression at the HWP1 locus of Candida albicans. Microbiology 151:1061-1071. http://dx.doi.org/10.1099 /mic.0.27487-0.