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Current Protein & Peptide Science

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ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

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Review Article

Virulence Factors in Candida species

Author(s): Monika Staniszewska*

Volume 21, Issue 3, 2020

Page: [313 - 323] Pages: 11

DOI: 10.2174/1389203720666190722152415

Price: $65

Abstract

Fungal diseases are severe and have very high morbidity as well as up to 60% mortality for patients diagnosed with invasive fungal infection. In this review, in vitro and in vivo studies provided us with the insight into the role of Candida virulence factors that mediate their success as pathogens, such as: membrane and cell wall (CW) barriers, dimorphism, biofilm formation, signal transduction pathway, proteins related to stress tolerance, hydrolytic enzymes (e.g. proteases, lipases, haemolysins), and toxin production. The review characterized the virulence of clinically important C. albicans, C. parapsilosis, C. tropicalis, C. glabrata and C. krusei. Due to the white-opaque transition in the mating-type locus MTL-homozygous cells, C. albicans demonstrates an advantage over other less related species of Candida as a human commensal and pathogen. It was reviewed that Candida ergosterol biosynthesis genes play a role in cellular stress and are essential for Candida pathogenesis both in invasive and superficial infections. Hydrolases associated with CW are involved in the host-pathogen interactions. Adhesins are crucial in colonization and biofilm formation, an important virulence factor for candidiasis. Calcineurin is involved in membrane and CW stress as well as virulence. The hyphae-specific toxin, named candidalysin, invades mucosal cells facilitating fungal invasion into deeper tissues. Expression of this protein promotes resistance to neutrophil killing in candidiasis. The virulence factors provide immunostimulatory factors, activating dendric cells and promoting T cell infiltration and activation. Targeting virulence factors, can reduce the risk of resistance development in Candida infections.

Keywords: Candida, pathogenicity, virulence targets, surface barriers, biofilm, morphogenesis, toxin, stress regulator.

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[1]
Rajendran, R.; Sherry, L.; Nile, C.J.; Sherriff, A.; Johnson, E.M.; Hanson, M.F.; Williams, C.; Munro, C.A.; Jones, B.J.; Ramage, G. Biofilm formation is a risk factor for mortality in patients with Candida albicans bloodstream infection-Scotland, 2012-2013. Clin. Microbiol. Infect., 2016, 22(1), 87-93.
[http://dx.doi.org/10.1016/j.cmi.2015.09.018] [PMID: 26432192]
[2]
Tsai, M.H.; Hsu, J.F.; Yang, L.Y.; Pan, Y.B.; Lai, M.Y.; Chu, S.M.; Huang, H.R.; Chiang, M.C.; Fu, R.H.; Lu, J.J. Candidemia due to uncommon Candida species in children: new threat and impacts on outcomes. Sci. Rep., 2018, 8(1), 15239.
[http://dx.doi.org/10.1038/s41598-018-33662-x] [PMID: 30323257]
[3]
Montagna, M.T.; De Giglio, O.; Napoli, C.; Lovero, G.; Caggiano, G.; Delia, M.; Pastore, D.; Santoro, N.; Specchia, G. Invasive fungal infections in patients with hematologic malignancies (aurora project): lights and shadows during 18-months surveillance. Int. J. Mol. Sci., 2012, 13(1), 774-787.
[http://dx.doi.org/10.3390/ijms13010774] [PMID: 22312285]
[4]
Guinea, J. Global trends in the distribution of Candida species causing candidemia. Clin. Microbiol. Infect., 2014, 20(Suppl. 6), 5-10.
[http://dx.doi.org/10.1111/1469-0691.12539] [PMID: 24506442]
[5]
Ishikane, M.; Hayakawa, K.; Kutsuna, S.; Takeshita, N.; Ohmagari, N. Epidemiology of blood stream infection due to Candida Species in a tertiary care hospital in Japan over 12 Years: Importance of peripheral line-associated candidemia. PLoS One, 2016, 11(10) e0165346
[http://dx.doi.org/10.1371/journal.pone.0165346] [PMID: 27798663]
[6]
Fu, J.; Ding, Y.; Jiang, Y.; Mo, S.; Xu, S.; Qin, P. Persistent candidemia in very low birth weight neonates: risk factors and clinical significance. BMC Infect. Dis., 2018, 18(1), 558.
[http://dx.doi.org/10.1186/s12879-018-3487-9] [PMID: 30419841]
[7]
Sardi, J.C.O.; Scorzoni, L.; Bernardi, T.; Fusco-Almeida, A.M.; Mendes Giannini, M.J.S. Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. J. Med. Microbiol., 2013, 62(Pt 1), 10-24.
[http://dx.doi.org/10.1099/jmm.0.045054-0] [PMID: 23180477]
[8]
Fisher, B.T.; Vendetti, N.; Bryan, M.; Prasad, P.A.; Russell Localio, A.; Damianos, A.; Coffin, S.E.; Bell, L.M.; Walsh, T.J.; Gross, R.; Zaoutis, T.E. Central Venous Catheter Retention and Mortality in Children With Candidemia: A Retrospective Cohort Analysis. J. Pediatric Infect. Dis. Soc., 2016, 5(4), 403-408.
[http://dx.doi.org/10.1093/jpids/piv048] [PMID: 26407279]
[9]
Wang, H.; Liu, N.; Yin, M.; Han, H.; Yue, J.; Zhang, F.; Shan, T.; Guo, H.; Wu, D. The epidemiology, antifungal use and risk factors of death in elderly patients with candidemia: a multicentre retrospective study. BMC Infect. Dis., 2014, 14, 609.
[http://dx.doi.org/10.1186/s12879-014-0609-x] [PMID: 25420435]
[10]
Araújo, D.; Henriques, M.; Silva, S. Portrait of Candida species biofilm regulatory network genes. Trends Microbiol., 2017, 25(1), 62-75.
[http://dx.doi.org/10.1016/j.tim.2016.09.004] [PMID: 27717660]
[11]
Lohse, M.B.; Gulati, M.; Johnson, A.D.; Nobile, C.J. Development and regulation of single- and multi-species Candida albicans biofilms. Nat. Rev. Microbiol., 2018, 16(1), 19-31.
[http://dx.doi.org/10.1038/nrmicro.2017.107] [PMID: 29062072]
[12]
Nakayama, H.; Nakayama, N.; Arisawa, M.; Aoki, Y. In vitro and in vivo effects of 14α-demethylase (ERG11) depletion in Candida glabrata. Antimicrob. Agents Chemother., 2001, 45(11), 3037-3045.
[http://dx.doi.org/10.1128/AAC.45.11.3037-3045.2001] [PMID: 11600353]
[13]
Mayer, F.L.; Kronstad, J.W. Breaking the bad: Bacillus blocks fungal virulence factors. Microb. Cell, 2017, 4(11), 384-386.
[http://dx.doi.org/10.15698/mic2017.11.599] [PMID: 29167801]
[14]
Zhou, Y.; Liao, M.; Zhu, C.; Hu, Y.; Tong, T.; Peng, X.; Li, M.; Feng, M.; Cheng, L.; Ren, B.; Zhou, X. ERG3 and ERG11 genes are critical for the pathogenesis of Candida albicans during the oral mucosal infection. Int. J. Oral Sci., 2018, 10(2), 9.
[http://dx.doi.org/10.1038/s41368-018-0013-2] [PMID: 29555898]
[15]
Soll, D.R. The evolution of alternative biofilms in an opportunistic fungal pathogen: an explanation for how new signal transduction pathways may evolve. Infect. Genet. Evol., 2014, 22, 235-243.
[http://dx.doi.org/10.1016/j.meegid.2013.07.013] [PMID: 23871837]
[16]
Becker, J.M.; Kauffman, S.J.; Hauser, M.; Huang, L.; Lin, M.; Sillaots, S.; Jiang, B.; Xu, D.; Roemer, T. Pathway analysis of Candida albicans survival and virulence determinants in a murine infection model. Proc. Natl. Acad. Sci. USA, 2010, 107(51), 22044-22049.
[http://dx.doi.org/10.1073/pnas.1009845107] [PMID: 21135205]
[17]
Sanglard, D.; Ischer, F.; Parkinson, T.; Falconer, D.; Bille, J. Candida albicans mutations in the ergosterol biosynthetic pathway and resistance to several antifungal agents. Antimicrob. Agents Chemother., 2003, 47(8), 2404-2412.
[http://dx.doi.org/10.1128/AAC.47.8.2404-2412.2003] [PMID: 12878497]
[18]
Rodrigues, M.L. The Multifunctional Fungal Ergosterol. MBio, 2018, 9(5), e01755-e18.
[http://dx.doi.org/10.1128/mBio.01755-18] [PMID: 30228244]
[19]
Vincent, B.M.; Lancaster, A.K.; Scherz-Shouval, R.; Whitesell, L.; Lindquist, S. Fitness trade-offs restrict the evolution of resistance to amphotericin B. PLoS Biol., 2013, 11(10) e1001692
[http://dx.doi.org/10.1371/journal.pbio.1001692] [PMID: 24204207]
[20]
Branco, J.; Ola, M.; Silva, R.M.; Fonseca, E.; Gomes, N.C.; Martins-Cruz, C.; Silva, A.P.; Silva-Dias, A.; Pina-Vaz, C.; Erraught, C.; Brennan, L.; Rodrigues, A.G.; Butler, G.; Miranda, I.M. Impact of ERG3 mutations and expression of ergosterol genes controlled by UPC2 and NDT80 in Candida parapsilosis azole resistance. Clin. Microbiol. Infect., 2017, 23(8), 575.e1-575.e8.
[http://dx.doi.org/10.1016/j.cmi.2017.02.002] [PMID: 28196695]
[21]
Adams, D.J. Fungal cell wall chitinases and glucanases. Microbiology, 2004, 150(Pt 7), 2029-2035.
[http://dx.doi.org/10.1099/mic.0.26980-0] [PMID: 15256547]
[22]
Lee, K.K.; Maccallum, D.M.; Jacobsen, M.D.; Walker, L.A.; Odds, F.C.; Gow, N.A.R.; Munro, C.A.; Elevated, C.W. Elevated cell wall chitin in Candida albicans confers echinocandin resistance in vivo. Antimicrob. Agents Chemother., 2012, 56(1), 208-217.
[http://dx.doi.org/10.1128/AAC.00683-11] [PMID: 21986821]
[23]
de Groot, P.W.J.; de Boer, A.D.; Cunningham, J.; Dekker, H.L.; de Jong, L.; Hellingwerf, K.J.; de Koster, C.; Klis, F.M. Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryot. Cell, 2004, 3(4), 955-965.
[http://dx.doi.org/10.1128/EC.3.4.955-965.2004] [PMID: 15302828]
[24]
Gulati, M.; Nobile, C.J. Candida albicans biofilms: development, regulation, and molecular mechanisms. Microbes Infect., 2016, 18(5), 310-321.
[http://dx.doi.org/10.1016/j.micinf.2016.01.002] [PMID: 26806384]
[25]
West, L.; Lowman, D.W.; Mora-Montes, H.M.; Grubb, S.; Murdoch, C.; Thornhill, M.H.; Gow, N.A.R.; Williams, D.; Haynes, K. Differential virulence of Candida glabrata glycosylation mutants. J. Biol. Chem., 2013, 288(30), 22006-22018.
[http://dx.doi.org/10.1074/jbc.M113.478743] [PMID: 23720756]
[26]
Kasper, L.; Seider, K.; Hube, B. Intracellular survival of Candida glabrata in macrophages: immune evasion and persistence. FEMS Yeast Res., 2015, 15(5) fov042
[http://dx.doi.org/10.1093/femsyr/fov042] [PMID: 26066553]
[27]
Ben-Ami, R.; Garcia-Effron, G.; Lewis, R.E.; Gamarra, S.; Leventakos, K.; Perlin, D.S.; Kontoyiannis, D.P. Fitness and virulence costs of Candida albicans FKS1 hot spot mutations associated with echinocandin resistance. J. Infect. Dis., 2011, 204(4), 626-635.
[http://dx.doi.org/10.1093/infdis/jir351] [PMID: 21791665]
[28]
Pereira, L.; Silva, S.; Ribeiro, B.; Henriques, M.; Azeredo, J. Influence of glucose concentration on the structure and quantity of biofilms formed by Candida parapsilosis. FEMS Yeast Res., 2015, 15(5) fov043
[http://dx.doi.org/10.1093/femsyr/fov043] [PMID: 26071437]
[29]
Bain, J.M.; Louw, J.; Lewis, L.E.; Okai, B.; Walls, C.A.; Ballou, E.R.; Walker, L.A.; Reid, D.; Munro, C.A.; Brown, A.J.P.; Brown, G.D.; Gow, N.A.R.; Erwig, L.P. Candida albicans hypha formation and mannan masking of β-glucan inhibit macrophage phagosome maturation. MBio, 2014, 5(6), e01874-e14.
[http://dx.doi.org/10.1128/mBio.01874-14] [PMID: 25467440]
[30]
O’Meara, T.R.; Veri, A.O.; Polvi, E.J.; Li, X.; Valaei, S.F.; Diezmann, S.; Cowen, L.E. Mapping the Hsp90 genetic network reveals ergosterol biosynthesis and phosphatidylinositol-4-kinase signaling as core circuitry governing cellular stress. PLoS Genet., 2016, 12(6) e1006142
[http://dx.doi.org/10.1371/journal.pgen.1006142] [PMID: 27341673]
[31]
Butler, G.; Rasmussen, M.D.; Lin, M.F.; Santos, M.A.; Sakthikumar, S.; Munro, C.A.; Rheinbay, E.; Grabherr, M.; Forche, A.; Reedy, J.L.; Agrafioti, I.; Arnaud, M.B.; Bates, S.; Brown, A.J.; Brunke, S.; Costanzo, M.C.; Fitzpatrick, D.A.; de Groot, P.W.; Harris, D.; Hoyer, L.L.; Hube, B.; Klis, F.M.; Kodira, C.; Lennard, N.; Logue, M.E.; Martin, R.; Neiman, A.M.; Nikolaou, E.; Quail, M.A.; Quinn, J.; Santos, M.C.; Schmitzberger, F.F.; Sherlock, G.; Shah, P.; Silverstein, K.A.; Skrzypek, M.S.; Soll, D.; Staggs, R.; Stansfield, I.; Stumpf, M.P.; Sudbery, P.E.; Srikantha, T.; Zeng, Q.; Berman, J.; Berriman, M.; Heitman, J.; Gow, N.A.; Lorenz, M.C.; Birren, B.W.; Kellis, M.; Cuomo, C.A. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature, 2009, 459(7247), 657-662.
[http://dx.doi.org/10.1038/nature08064] [PMID: 19465905]
[32]
Ferwerda, G.; Netea, M.G.; Joosten, L.A.; van der Meer, J.W.; Romani, L.; Kullberg, B.J. The role of Toll-like receptors and C-type lectins for vaccination against Candida albicans. Vaccine, 2010, 28(3), 614-622.
[http://dx.doi.org/10.1016/j.vaccine.2009.10.082] [PMID: 19887129]
[33]
Tam, P.; Gee, K.; Piechocinski, M.; Macreadie, I. Candida glabrata, Friend and Foe. J. Fungi (Basel), 2015, 1(2), 277-292.
[http://dx.doi.org/10.3390/jof1020277] [PMID: 29376912]
[34]
Wan, H.W.H.A.; Jamil, N.A.; Jamaludin, N.H.; Nordin, M.A. Effect of Piper betle and Brucea javanica on the Differential Expression of Hyphal Wall Protein (HWP1) in Non-Candida albicans Candida (NCAC) Species. Evid. Based Complement. Alternat. Med., 2013, 2013 397268
[http://dx.doi.org/10.1155/2013/134852]
[35]
d’Enfert, C.; Janbon, G. Biofilm formation in Candida glabrata: What have we learnt from functional genomics approaches? FEMS Yeast Res., 2016, 16(1) fov111
[http://dx.doi.org/10.1093/femsyr/fov111] [PMID: 26678748]
[36]
Netea, M.G.; Maródi, L. Innate immune mechanisms for recognition and uptake of Candida species. Trends Immunol., 2010, 31(9), 346-353.
[http://dx.doi.org/10.1016/j.it.2010.06.007] [PMID: 20705510]
[37]
de Barros, P.P.; Freire, F.; Rossoni, R.D.; Junqueira, J.C.; Jorge, A.O.C. Candida krusei and Candida glabrata reduce the filamentation of Candida albicans by downregulating expression of HWP1 gene. Folia Microbiol. (Praha), 2017, 62(4), 317-323.
[http://dx.doi.org/10.1007/s12223-017-0500-4] [PMID: 28164244]
[38]
Reedy, J.L.; Filler, S.G.; Heitman, J. Elucidating the Candida albicans calcineurin signaling cascade controlling stress response and virulence. Fungal Genet. Biol., 2010, 47(2), 107-116.
[http://dx.doi.org/10.1016/j.fgb.2009.09.002] [PMID: 19755168]
[39]
LaFayette, S.L.; Collins, C.; Zaas, A.K.; Schell, W.A.; Betancourt-Quiroz, M.; Gunatilaka, A.A.L.; Perfect, J.R.; Cowen, L.E. PKC signaling regulates drug resistance of the fungal pathogen Candida albicans via circuitry comprised of Mkc1, calcineurin, and Hsp90. PLoS Pathog., 2010, 6(8) e1001069
[http://dx.doi.org/10.1371/journal.ppat.1001069] [PMID: 20865172]
[40]
Karababa, M.; Valentino, E.; Pardini, G.; Coste, A.T.; Bille, J.; Sanglard, D. CRZ1, a target of the calcineurin pathway in Candida albicans. Mol. Microbiol., 2006, 59(5), 1429-1451.
[http://dx.doi.org/10.1111/j.1365-2958.2005.05037.x] [PMID: 16468987]
[41]
Bader, T.; Bodendorfer, B.; Schröppel, K.; Morschhäuser, J. Calcineurin is essential for virulence in Candida albicans. Infect. Immun., 2003, 71(9), 5344-5354.
[http://dx.doi.org/10.1128/IAI.71.9.5344-5354.2003] [PMID: 12933882]
[42]
Staniszewska, A. European Union Contest for Young Scientist (EUCYS), Warsaw, Poland, 13.04-15.04.2018, Copernicus Science Centre, Characteristics of the Candida albicans’ Calcineurin Stress Response under a Polybrominated Proxyphylline Derivative. 2018.
[43]
Moyes, D.L.; Wilson, D.; Richardson, J.P.; Mogavero, S.; Tang, S.X.; Wernecke, J.; Höfs, S.; Gratacap, R.L.; Robbins, J.; Runglall, M.; Murciano, C.; Blagojevic, M.; Thavaraj, S.; Förster, T.M.; Hebecker, B.; Kasper, L.; Vizcay, G.; Iancu, S.I.; Kichik, N.; Häder, A.; Kurzai, O.; Luo, T.; Krüger, T.; Kniemeyer, O.; Cota, E.; Bader, O.; Wheeler, R.T.; Gutsmann, T.; Hube, B.; Naglik, J.R. Candidalysin is a fungal peptide toxin critical for mucosal infection. Nature, 2016, 532(7597), 64-68.
[http://dx.doi.org/10.1038/nature17625] [PMID: 27027296]
[44]
Chen, Y-L.; Konieczka, J.H.; Springer, D.J.; Bowen, S.E.; Zhang, J.; Silao, F.G.S.; Bungay, A.A.C.; Bigol, U.G.; Nicolas, M.G.; Abraham, S.N.; Thompson, D.A.; Regev, A.; Heitman, J. Convergent evolution of calcineurin pathway roles in thermotolerance and virulence in Candida glabrata. G3 (Bethesda), 2012, 2(6), 675-691.
[http://dx.doi.org/10.1534/g3.112.002279] [PMID: 22690377]
[45]
Xie, J.L.; Grahl, N.; Sless, T.; Leach, M.D.; Kim, S.H.; Hogan, D.A.; Robbins, N.; Cowen, L.E. Signaling through Lrg1, Rho1 and Pkc1 Governs Candida albicans morphogenesis in response to diverse cues. PLoS Genet., 2016, 12(10) e1006405
[http://dx.doi.org/10.1371/journal.pgen.1006405] [PMID: 27788136]
[46]
Nett, J.E. The host’s replay to Candida biofilm. Pathogens, 2016, 5(1), 33.
[http://dx.doi.org/10.3390/pathogens5010033] [PMID: 26999221]
[47]
Guo, D.; Yue, H.; Wei, Y.; Huang, G. [Genetic regulatory mechanisms of Candida albicans biofilm formation]. Sheng Wu Gong Cheng Xue Bao, 2017, 33(9), 1567-1581.
[PMID: 28956402]
[48]
Glazier, V.E.; Murante, T.; Murante, D.; Koselny, K.; Liu, Y.; Kim, D.; Koo, H.; Krysan, D.J. Genetic analysis of the Candida albicans biofilm transcription factor network using simple and complex haploinsufficiency. PLoS Genet., 2017, 13(8) e1006948
[http://dx.doi.org/10.1371/journal.pgen.1006948] [PMID: 28793308]
[49]
Zheng, Q.; Zhang, Q.; Bing, J.; Ding, X.; Huang, G. Environmental and genetic regulation of white-opaque switching in Candida tropicalis. Mol. Microbiol., 2017, 106(6), 999-1017.
[http://dx.doi.org/10.1111/mmi.13862] [PMID: 29030879]
[50]
Srikantha, T.; Daniels, K.J.; Pujol, C.; Kim, E.; Soll, D.R. Identification of genes upregulated by the transcription factor Bcr1 that are involved in impermeability, impenetrability, and drug resistance of Candida albicans a/α biofilms. Eukaryot. Cell, 2013, 12(6), 875-888.
[http://dx.doi.org/10.1128/EC.00071-13] [PMID: 23563485]
[51]
Riera, M.; Mogensen, E.; d’Enfert, C.; Janbon, G. New regulators of biofilm development in Candida glabrata. Res. Microbiol., 2012, 163(4), 297-307.
[http://dx.doi.org/10.1016/j.resmic.2012.02.005] [PMID: 22426249]
[52]
O’Meara, T.R.; Veri, A.O.; Ketela, T.; Jiang, B.; Roemer, T.; Cowen, L.E. Global analysis of fungal morphology exposes mechanisms of host cell escape. Nat. Commun., 2015, 6, 6741.
[http://dx.doi.org/10.1038/ncomms7741] [PMID: 25824284]
[53]
Diezmann, S.; Michaut, M.; Shapiro, R.S.; Bader, G.D.; Cowen, L.E. Mapping the Hsp90 genetic interaction network in Candida albicans reveals environmental contingency and rewired circuitry. PLoS Genet., 2012, 8(3) e1002562
[http://dx.doi.org/10.1371/journal.pgen.1002562] [PMID: 22438817]
[54]
Verma, A.H.; Richardson, J.P.; Zhou, C.; Coleman, B.M.; Moyes, D.L.; Ho, J.; Huppler, A.R.; Ramani, K.; McGeachy, M.J.; Mufazalov, I.A.; Waisman, A.; Kane, L.P.; Biswas, P.S.; Hube, B.; Naglik, J.R.; Gaffen, S.L. Oral epithelial cells orchestrate innate type 17 responses to Candida albicans through the virulence factor candidalysin. Sci. Immunol., 2017, 2(17) eaam8834
[http://dx.doi.org/10.1126/sciimmunol.aam8834] [PMID: 29101209]
[55]
Iliev, I.D.; Underhill, D.M. Striking a balance: fungal commensalism versus pathogenesis. Curr. Opin. Microbiol., 2013, 16(3), 366-373.
[http://dx.doi.org/10.1016/j.mib.2013.05.004] [PMID: 23756050]
[56]
Seider, K.; Heyken, A.; Lüttich, A.; Miramón, P.; Hube, B. Interaction of pathogenic yeasts with phagocytes: survival, persistence and escape. Curr. Opin. Microbiol., 2010, 13(4), 392-400.
[http://dx.doi.org/10.1016/j.mib.2010.05.001] [PMID: 20627672]
[57]
Collette, J.R.; Lorenz, M.C. Mechanisms of immune evasion in fungal pathogens. Curr. Opin. Microbiol., 2011, 14(6), 668-675.
[http://dx.doi.org/10.1016/j.mib.2011.09.007] [PMID: 21955887]
[58]
Connolly, L.A.; Riccombeni, A.; Grózer, Z.; Holland, L.M.; Lynch, D.B.; Andes, D.R.; Gácser, A.; Butler, G. The APSES transcription factor Efg1 is a global regulator that controls morphogenesis and biofilm formation in Candida parapsilosis. Mol. Microbiol., 2013, 90(1), 36-53.
[PMID: 23895281]
[59]
Mancera, E.; Porman, A.M.; Cuomo, C.A.; Bennett, R.J.; Johnson, A.D. Finding a Missing Gene: EFG1 Regulates Morphogenesis in Candida tropicalis. G3 (Bethesda), 2015, 5(5), 849-856.
[http://dx.doi.org/10.1534/g3.115.017566] [PMID: 25758825]
[60]
Nobile, C.J.; Fox, E.P.; Nett, J.E.; Sorrells, T.R.; Mitrovich, Q.M.; Hernday, A.D.; Tuch, B.B.; Andes, D.R.; Johnson, A.D. A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell, 2012, 148(1-2), 126-138.
[http://dx.doi.org/10.1016/j.cell.2011.10.048] [PMID: 22265407]
[61]
Zawrotniak, M.; Bochenska, O.; Karkowska-Kuleta, J.; Seweryn-Ozog, K.; Aoki, W.; Ueda, M.; Kozik, A. Rapala-Kozik, Maria. Aspartic proteases and major CW components in Candida albicans trigger the release of neutrophil extracellular traps. Front. Cell. Infect. Microbiol., 2017, 7, 414.
[http://dx.doi.org/10.3389/fcimb.2017.00414] [PMID: 28983472]
[62]
Martin, R.; Wächtler, B.; Schaller, M.; Wilson, D.; Hube, B. Host-pathogen interactions and virulence-associated genes during Candida albicans oral infections. Int. J. Med. Microbiol., 2011, 301(5), 417-422.
[http://dx.doi.org/10.1016/j.ijmm.2011.04.009] [PMID: 21555244]
[63]
Miramón, P.; Lorenz, M.C. A feast for Candida: Metabolic plasticity confers an edge for virulence. PLoS Pathog., 2017, 13(2) e1006144
[http://dx.doi.org/10.1371/journal.ppat.1006144] [PMID: 28182769]
[64]
Deorukhkar, S.C.; Saini, S.; Mathew, S. Virulence factors contributing to pathogenicity of Candida tropicalis and its antifungal susceptibility profile. Int. J. Microbiol., 2014, 2014 456878
[http://dx.doi.org/10.1155/2014/456878] [PMID: 24803934]
[65]
Melo, A.S.; Bizerra, F.C.; Freymüller, E.; Arthington-Skaggs, B.A.; Colombo, A.L. Biofilm production and evaluation of antifungal susceptibility amongst clinical Candida spp. isolates, including strains of the Candida parapsilosis complex. Med. Mycol., 2011, 49(3), 253-262.
[http://dx.doi.org/10.3109/13693786.2010.530032] [PMID: 21039308]
[66]
Ferreira, C.; Gonçalves, B.; Vilas Boas, D.; Oliveira, H.; Henriques, M. Azeredo, J.; Silva, S. Candida tropicalis biofilm and human epithelium invasion is highly influenced by environmental pH. Pathog. Dis., 2016, 74, 101.
[http://dx.doi.org/10.1093/femspd/ftw101]
[67]
Alonso, M.F.; Gow, N.A.R.; Erwig, L.P.; Bain, J.M. Macrophage migration is impaired within Candida albicans biofilms. J. Fungi (Basel), 2017, 3(3), 1-12.
[PMID: 29371549]
[68]
Martin, R.; Wächtler, B.; Schaller, M.; Wilson, D.; Hube, B. Host-pathogen interactions and virulence-associated genes during Candida albicans oral infections. Int. J. Med. Microbiol., 2011, 301(5), 417-422.
[http://dx.doi.org/10.1016/j.ijmm.2011.04.009] [PMID: 21555244]
[69]
Biswas, S.; Van Dijck, P.; Datta, A. Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans. Microbiol. Mol. Biol. Rev., 2007, 71(2), 348-376.
[http://dx.doi.org/10.1128/MMBR.00009-06] [PMID: 17554048]
[70]
Danhof, H.A.; Vylkova, S.; Vesely, E.M.; Ford, A.E.; Gonzalez-Garay, M.; Lorenz, M.C. Robust extracellular pH modulation by Candida albicans during growth in carboxylic acids. MBio, 2016, 7(6), e01646-e16.
[http://dx.doi.org/10.1128/mBio.01646-16] [PMID: 27935835]
[71]
Maccallum, D.M. Hosting infection: experimental models to assay Candida virulence. Int. J. Microbiol., 2012, 2012 363764
[http://dx.doi.org/10.1155/2012/363764] [PMID: 22235206]
[72]
Jacobsen, I.D.; Brunke, S.; Seider, K.; Schwarzmüller, T.; Firon, A.; d’Enfért, C.; Kuchler, K.; Hube, B. Candida glabrata persistence in mice does not depend on host immunosuppression and is unaffected by fungal amino acid auxotrophy. Infect. Immun., 2010, 78(3), 1066-1077.
[http://dx.doi.org/10.1128/IAI.01244-09] [PMID: 20008535]
[73]
Conti, H.R.; Bruno, V.M.; Childs, E.E.; Daugherty, S.; Hunter, J.P.; Mengesha, B.G.; Saevig, D.L.; Hendricks, M.R.; Coleman, B.M.; Brane, L.; Solis, N.; Cruz, J.A.; Verma, A.H.; Garg, A.V.; Hise, A.G.; Richardson, J.P.; Naglik, J.R.; Filler, S.G.; Kolls, J.K.; Sinha, S.; Gaffen, S.L. IL-17 Receptor signaling in oral epithelial cells is critical for protection against oropharyngeal candidiasis. Cell Host Microbe, 2016, 20(5), 606-617.
[http://dx.doi.org/10.1016/j.chom.2016.10.001] [PMID: 27923704]
[74]
Li, S.S.; Ogbomo, H.; Mansour, M.K.; Xiang, R.F.; Szabo, L.; Munro, F.; Mukherjee, P.; Mariuzza, R.A.; Amrein, M.; Vyas, J.M.; Robbins, S.M.; Mody, C.H. Identification of the fungal ligand triggering cytotoxic PRR-mediated NK cell killing of Cryptococcus and Candida. Nat. Commun., 2018, 9(1), 751-765.
[http://dx.doi.org/10.1038/s41467-018-03014-4] [PMID: 29467448]
[75]
Mora-Montes, H.M.; Ponce-Noyola, P.; Villagómez-Castro, J.C.; Gow, N.A.R.; Flores-Carreón, A.; López-Romero, E. Protein glycosylation in Candida. Future Microbiol., 2009, 4(9), 1167-1183.
[http://dx.doi.org/10.2217/fmb.09.88] [PMID: 19895219]
[76]
Conti, H.R.; Gaffen, S.L. IL-17-mediated immunity to the opportunistic fungal pathogen Candida albicans. J. Immunol., 2015, 195(3), 780-788.
[http://dx.doi.org/10.4049/jimmunol.1500909] [PMID: 26188072]
[77]
Katragkou, A.; Simitsopoulou, M.; Chatzimoschou, A.; Georgiadou, E.; Walsh, T.J.; Roilides, E. Effects of interferon-γ and granulocyte colony-stimulating factor on antifungal activity of human polymorphonuclear neutrophils against Candida albicans grown as biofilms or planktonic cells. Cytokine, 2011, 55(3), 330-334.
[http://dx.doi.org/10.1016/j.cyto.2011.05.007] [PMID: 21641233]
[78]
Katragkou, A.; Kruhlak, M.J.; Simitsopoulou, M.; Chatzimoschou, A.; Taparkou, A.; Cotten, C.J.; Paliogianni, F.; Diza-Mataftsi, E.; Tsantali, C.; Walsh, T.J.; Roilides, E. Interactions between human phagocytes and Candida albicans biofilms alone and in combination with antifungal agents. J. Infect. Dis., 2010, 201(12), 1941-1949.
[http://dx.doi.org/10.1086/652783] [PMID: 20415537]
[79]
Schindler, B.; Segal, E. Candida albicans metabolite affects the cytoskeleton and phagocytic activity of murine macrophages. Med. Mycol., 2008, 46(3), 251-258.
[http://dx.doi.org/10.1080/13693780701837157] [PMID: 18404553]
[80]
Palmer, G.E.; Kelly, M.N.; Sturtevant, J.E. Autophagy in the pathogen Candida albicans. Microbiology, 2007, 153(Pt 1), 51-58.
[http://dx.doi.org/10.1099/mic.0.2006/001610-0] [PMID: 17185534]
[81]
Liu, F.; Fan, X.; Auclair, S.; Ferguson, M.; Sun, J.; Soong, L.; Hou, W.; Redfield, R.R.; Birx, D.L.; Ratto-Kim, S.; Robb, M.L.; Kim, J.H.; Michael, N.L.; Hu, H. Sequential dysfunction and progressive depletion of Candida albicans-specific CD4 T cell response in HIV-1 infection. PLoS Pathog., 2016, 12(6) e1005663
[http://dx.doi.org/10.1371/journal.ppat.1005663] [PMID: 27280548]
[82]
Bonfim-Mendonça. Pde.S.; Ratti, B.A.; Godoy, Jda.S.; Negri, M.; Lima, N.C.; Fiorini, A.; Hatanaka, E.; Consolaro, M.E.; de Oliveira Silva, S.; Svidzinski, T.I.E. β-Glucan induces reactive oxygen species production in human neutrophils to improve the killing of Candida albicans and Candida glabrata isolates from vulvovaginal candidiasis. PLoS One, 2014, 9(9)e107805
[http://dx.doi.org/10.1371/journal.pone.0107805] [PMID: 25229476]
[83]
Whibley, N.; Gaffen, S.L. Beyond Candida albicans: Mechanisms of immunity to non-albicans Candida species. Cytokine, 2015, 76(1), 42-52.
[http://dx.doi.org/10.1016/j.cyto.2015.07.025] [PMID: 26276374]
[84]
Garcia-Effron, G.; Lee, S.; Park, S.; Cleary, J.D.; Perlin, D.S. Effect of Candida glabrata FKS1 and FKS2 mutations on echinocandin sensitivity and kinetics of 1,3-beta-D-glucan synthase: implication for the existing susceptibility breakpoint. Antimicrob. Agents Chemother., 2009, 53(9), 3690-3699.
[http://dx.doi.org/10.1128/AAC.00443-09] [PMID: 19546367]
[85]
Whitesell, L.; Mimnaugh, E.G.; De Costa, B.; Myers, C.E.; Neckers, L.M. Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc. Natl. Acad. Sci. USA, 1994, 91(18), 8324-8328.
[http://dx.doi.org/10.1073/pnas.91.18.8324] [PMID: 8078881]
[86]
Borowiecki, P.; Wińska, P.; Bretner, M.; Gizińska, M.; Koronkiewicz, M.; Staniszewska, M. Synthesis of novel proxyphylline derivatives with dual Anti-Candida albicans and anticancer activity. Eur. J. Med. Chem., 2018, 150, 307-333.
[http://dx.doi.org/10.1016/j.ejmech.2018.02.077] [PMID: 29533875]
[87]
Pierce, C.G.; Chaturvedi, A.K.; Lazzell, A.L.; Powell, A.T.; Saville, S.P.; McHardy, S.F.; Lopez-Ribot, J.L. A novel small molecule inhibitor of Candida albicans biofilm formation, filamentation and virulence with low potential for the development of resistance. NPJ Biofilms Microbiomes, 2015, 1, 15012.
[http://dx.doi.org/10.1038/npjbiofilms.2015.12] [PMID: 26691764]
[88]
Staniszewska, M.; Bondaryk, M.; Kazek, M.; Gliniewicz, A.; Braunsdorf, C.; Schaller, M.; Mora-Montes, H.M.; Ochal, Z. Effect of serine protease KEX2 on Candida albicans virulence under halogenated methyl sulfones. Future Microbiol., 2017, 12, 285-306.
[http://dx.doi.org/10.2217/fmb-2016-0141] [PMID: 28287299]
[89]
Gizińska, M.; Staniszewska, M.; Ochal, Z. Novel sulfones with antifungal properties: antifungal activities and interactions with Candida spp. virulence factors. Mini Rev. Med. Chem., 2019, 19(1), 12-21.
[http://dx.doi.org/10.2174/1389557518666180924121209] [PMID: 30246638]

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