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Mini-Reviews in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1389-5575
ISSN (Online): 1875-5607

Review Article

Novel Sulfones with Antifungal Properties: Antifungal Activities and Interactions with Candida spp. Virulence Factors

Author(s): Małgorzata Gizińska, Monika Staniszewska* and Zbigniew Ochal*

Volume 19, Issue 1, 2019

Page: [12 - 21] Pages: 10

DOI: 10.2174/1389557518666180924121209

Price: $65

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Abstract

Since candidiasis is so difficult to eradicate with an antifungal treatment and the existing antimycotics display many limitations, hopefully new sulfone derivatives may overcome these deficiencies. It is pertinent to study new strategies such as sulfone derivatives targeting the virulence attributes of C. albicans that differentiate them from the host. During infections, the pathogenic potential of C. albicans relies on the virulence factors as follows: hydrolytic enzymes, transcriptional factors, adhesion, and development of biofilms. In the article we explored how the above-presented C. albicans fitness and virulence attributes provided a robust response to the environmental stress exerted by sulfones upon C. albicans; C. albicans fitness and virulence attributes are fungal properties whose inactivation attenuates virulence. Our understanding of how these mechanisms and factors are inhibited by sulfones has increased over the last years. As lack of toxicity is a prerequisite for medical approaches, sulfones (non-toxic as assessed in vitro and in vivo) may prove to be useful for reducing C. albicans pathogenesis in humans. The antifungal activity of sulfones dealing with these multiple virulence factors and fitness attributes is discussed.

Keywords: Antifungal activity, anti-virulence agents, Candida spp., fungal infections, sulfone derivatives, virulence.

Graphical Abstract
[1]
Pfaller, M.A.; Diekema, D.J.; Gibbs, D.L.; Newell, V.A.; Ellis, D.; Tullio, V.; Rodloff, A.; Fu, W.; Ling, T.A. Global Antifungal Surveillance Group. Results from the ARTEMIS DISK global antifungal surveillance study, 1997 to 2007: A 10.5-year analysis of susceptibilities of Candida species to fluconazole and voriconazole as determined by CLSI standardized disk diffusion. J. Clin. Microbiol., 2010, 48, 1366-1377.
[2]
Pfaller, M.A.; Diekema, D.J. Epidemiology of invasive mycoses in North America. Crit. Rev. Microbiol., 2010, 36, 1-53.
[3]
Brown, G.D.; Denning, D.W.; Gow, N.A.R.; Levitz, S.M.; Netea, M.G.; White, T.C. Hidden killers: human fungal infections. Sci. Transl. Med., 2012, 4, 165rv13.
[4]
Kołaczkowska, A.; Kołaczkowski, M. Drug resistance mechanisms and their regulation in non-albicans Candida species. J. Antimicrob. Chemother., 2016, 71, 1438-1450.
[5]
Pappas, P.G.; Kauffman, C.A.; Andes, D.R.; Clancy, C.J.; Marr, K.A.; Ostrosky-Zeichner, L.; Reboli, A.C.; Schuster, M.G.; Vazquez, J.A.; Walsh, T.J. Clinical practicce guideline for the management of candidiasis: 2016 update by the Infectious Disease Society of America. Clin. Infect. Dis., 2016, 62, e1-e50.
[6]
Nucci, M.; Queiroz-Telles, F.; Alvarado-Matute, T.; Tiraboschi, I.N.; Cortes, J.; Zurita, J.; Guzman-Blanco, M.; Santolaya, M.E.; Thompson, L.; Sifuentes-Osornio, J. Epidemiology of candidemia in Latin America: a laboratory-based survey. PLoS One, 2013, 8, e59373.
[7]
Yapar, N. Epidemiology and risk factors for invasive candidiasis. Ther. Clin. Risk Manag., 2014, 10, 95-105.
[8]
Govender, N.P.; Patel, J.; Magobo, R.E.; Naicker, S.; Wadula, J.; Whitelaw, A.; Coovadia, Y.; Kalaratne, R.; Govind, C.; Lockhart, S.R. Emergence of azole-resistant Candida parapsilosis causing bloodstream infection: Results from laboratory-based sentinel surveillance in South Africa. J. Antimicrob. Chemother., 2016, 71, 1994-2004.
[9]
Cortegiani, A.; Russotto, V.; Maggiore, A.; Attanasio, M.; Naro, A.R.; Raineri, S.M.; Giarratano, A. Antifungal agents for preventing fungal infections in non-neutropenic critically ill patients. Cochrane Database Syst. Rev., 2016, 1, CD004920.
[10]
Hahn-Ast, C.; Felder, L.; Mayer, K.; Mückter, S.; Ruhnke, M.; Hein, R.; Hellmich, M.; Schwab, K.; Rachow, T.; Brossart, P.; von Lilienfeld-Toal, M. Outcome of empirical or targeted antifungal therapy after antifungal prophylaxis in febrile neutropenia. Ann. Hematol., 2016, 95, 1001-1009.
[11]
Schmiedel, Y.; Zimmerli, S. Common invasive fungal diseases: An overview of invasive candidiasis, aspergillosis, cryptococcosis, and Pneumocystis pneumonia. Swiss Med. Wkly., 2016, 146, w14281.
[12]
Silveira, F.P.; Husain, S. Fungal infections in solid organ transplantation. Med. Mycol., 2007, 45, 305-320.
[13]
Singh, N. Invasive aspergillosis in organ transplant recipients: New issues in epidemiologic characteristics, diagnosis, and management. Med. Mycol., 2005, 43(Suppl. 1), S267-S270.
[14]
Singh, N.; Peterson, D.L. Aspergilus infections in transplant recipients. Clin. Microbiol. Rev., 2005, 18, 44-69.
[15]
Solé, A.; Morant, P.; Salavert, M.; Pemán, J.; Morales, P. Valencia Lung Transplant Group. Aspergillus infections in lung transplant recipients: risk factors and outcome. Clin. Microbiol. Infect., 2005, 11, 359-365.
[16]
Solé, A.; Salavert, M. Fungal infection after lung transplantation. Transplant. Rev., 2008, 22, 89-104.
[17]
Singh, N.; Alexander, B.D.; Lortholary, O.; Dromer, F.; Gupta, K.L.; John, G.T.; del Busto, R.; Klintmalm, G.B.; Somani, J.; Lyon, G.M.; Pursell, K.; Stosor, V. Mu oz, P.; Limaye, A.P.; Kalil, A.C.; Pruett, T.L.; Garcia-Diaz, J.; Humar, A.; Houston, S.; House, A.A.; Wray, D.; Orloff, S.; Dowdy, L.A.; Fisher, R.A.; Heitman, J.; Wagener, M.M.; Husain, S. Cryptococcus neoformans in organ transplant recipients: Impact of calcineurin-inhibitor agents on mortality. J. Infect. Dis., 2007, 195, 756-764.
[18]
van Burik, J.A. Role of new antifungal agents in prphylaxis of mycoses in high risk patients. Curr. Opin. Infect. Dis., 2005, 18, 479-483.
[19]
Metcalf, S.C.; Dockrell, D.H. Improved outcomes associated with advances in therapy for invasive fungal infections in immunocompromised hosts. J. Infect., 2007, 55, 287-299.
[20]
Zaragoza, R.; Pemán, J.; Salavert, M.; Viudes, Á.; Solé, A.; Jarque, I.; Monte, E.; Romá, E.; Cantón, E. Multidisciplinary approach to the treatment of invasive fungal infections in adult patients. Prophylaxis, empirical, preemptive or targeted therapy, which is the best in the different hosts? Ther. Clin. Risk Manag., 2008, 4, 1261-1280.
[21]
Peron, I.H.; Reichert-Lima, F.; Busso-Lopes, A.F.; Nagasako, C.K.; Lyra, L.; Moretti, M.L.; Schreiber, A.Z. Resistance surveillance in Candida albicans: a five-year antifungal susceptibility evaluation in a brazilian University Hospital. PLoS One, 2016, 11, e0158126.
[22]
Fasoli, M.; Kerridge, D. Isolation and characterization of fluoropyrimidine-resistant mutants in two Candida species. Ann. N. Y. Acad. Sci., 1988, 544, 260-263.
[23]
Barchiesi, F.; Arzeni, D.; Caselli, F.; Scalise, G. Primary resistance to flucytosine among clinical isolates of Candida spp. J. Antimicrob. Chemother., 2000, 45, 408-409.
[24]
Pfaller, M.A.; Messer, S.A.; Boyken, L.; Huynh, H.; Hollis, R.J.; Diakema, D.J. In vitro activities of 5-fluorocytosine against 8,803 clinical isolates of Candida spp.: Global assessment of primary resistance using national committee for Clinical Laboratory Standards susceptibility testing methods. Antimicrob. Agents Chemother., 2002, 46, 3518-3521.
[25]
Pujol, C.; Pfaller, M.A.; Soll, D.R. Flucytosine resistance is restricted to a single genetic clade of Candida albicans. Antimicrob. Agents Chemother., 2004, 48, 262-266.
[26]
Hope, W.W.; Tabernero, L.; Denning, D.W.; Anderson, M.J. Molecular mechanisms of primary resistance to flucytosine in Candida albicans. Antimicrob. Agents Chemother., 2004, 48, 4377-4386.
[27]
Dodgson, A.R.; Dodgson, K.J.; Pujol, C.; Pfaller, M.A.; Soll, D.R. Clade-specific flucytosine resistance is due to a single nucleotide change in the FUR1 gene of Candida albicans. Antimicrob. Agents Chemother., 2004, 48, 2223-2227.
[28]
Jiang, C.; Dong, D.; Yu, B.; Cai, G.; Wang, X.; Ji, Y.; Peng, Y. Mechanisms of azole resistance in 52 clinical isolates of Candida tropicalis in China. J. Antimicrob. Chemother., 2013, 68, 778-785.
[29]
Sanglard, D. Emerging threats in antifungal-resistant fungal pathogens. Front. Med., 2016, 3, 11.
[30]
Pfaller, M.A.; Castanheira, M.; Lockhart, S.R.; Ahlquist, A.M.; Messer, S.A.; Jones, R.N. Frequency of decreased susceptibility and resistance to chinocandins among fluconazole-resistant bloodstream isolates of Candida glabrata. J. Clin. Microbiol., 2012, 50, 1199-1203.
[31]
Alexander, B.D.; Johnson, M.D.; Pfeiffer, C.D.; Jiménez-Ortigosa, C.; Catania, J.; Booker, R.; Castanheira, M.; Messer, S.A.; Perlin, D.S.; Pfaller, M.A. Increasing echinocandin resistance in Candida glabrata: Clinical failure correlates with presence of FKS mutations and elevated minimum inhibitory concentrations. Clin. Infect. Dis., 2013, 56, 1724-1732.
[32]
Forastiero, A.; Mesa-Arango, A.C.; Alastruey-Izquierdo, A.; Alcazar-Fouli, A.; Bernal-Martinez, L.; Pelaez, T.; Lopez, J.F.; Grimalt, J.O.; Gomez-Lopez, A.; Cuesta, I.; Zaragoza, O.; Mellado, E. Candida tropicalis antifungal cross-resistance is related to different azole target (Erg11p) modifications. Antimicrob. Agents Chemother., 2013, 57, 4769-4781.
[33]
Aoki, W.; Ueda, M. Characterization of antimicrobial peptides toward the development of novel antibiotics. Pharmaceuticals, 2013, 6, 1055-1081.
[34]
Castelli, M.V.; Butassi, E.; Monteiro, M.C.; Svetaz, L.A.; Vicente, F.; Zacchino, S.A. Novel antifungal agents: A patent review (2011-present). Expert Opin. Ther. Pat., 2014, 24, 323-338.
[35]
Ahmad, I. Shagufta. Sulfones: an important class of organic compounds with diverse biological activities. Int. J. Pharma Sci., 2015, 7, 19-27.
[36]
Feng, M.; Tang, B.; Liang, S.H.; Jiang, X. Sulfur containing scaffolds in drugs: Synthesis and application in medicinal chemistry. Curr. Top. Med. Chem., 2016, 16, 1200-1216.
[37]
Haddadi, H.; Farsani, M.R. Selective oxidation of sulfides to sulfones by H2O2 catalyzed by Fe-substituted sandwich type polyoxometalate. J. Cluster Sci., 2016, 27, 373-386.
[38]
Mac Bean, C. The Pesticide Manual: A World Compedium, 16th ed; Hampshire: British Crop Ptoduction Council, 2013.
[39]
Richards-Taylor, C.S.; Blankemore, D.C.; Willis, M.C. One-pot three-component sulfone synthesis exploiting palladium-catalysed aryl halide aminosulfonylation. Chem. Sci., 2014, 5, 222-228.
[40]
Borys, K.M.; Ochal, Z. Synthetic approaches to aryl halomethyl sulfones. Curr. Org. Chem., 2016, 20, 963-970.
[41]
Su, W. An efficient method for the oxidation of sulfides to sulfones. Tetrahedron Lett., 1994, 35, 4955-4958.
[42]
Sato, K.; Hyodo, M.; Aoki, M.; Zheng, X.Q.; Noyori, R. Oxidation of sulfides to sulfoxides and slufones with 30% hydrogen peroxide under organic solvent and halogen-free conditions. Tetrahedron, 2001, 57, 2469-2476.
[43]
Karimi, B.; Ghoreishi-Nezhad, M.; Clark, J.H. Selective oxidation of sulfides to sulfoxides using 30% hydrogen peroxide catalyzed with a recoverable silica-based tungstate interphase catalyst. Org. Lett., 2005, 17, 625-628.
[44]
Jeyakumar, K.; Chakravarthy, R.D.; Chand, D.K. Simple and efficient method for the oxidation of sulfides to sulfones using hydrogen peroxide and a Mo(VI) based catalyst. Catal. Commun., 2009, 10, 1948-1951.
[45]
Trost, B.M.; Curran, D.P. Chemoselective oxidation of sulfides to sulfones with potassium hydrogen persulfate. Tetrahedron Lett., 1981, 22, 1287-1290.
[46]
Konduru, N.K.; Dey, S.; Sajid, M.; Owais, M.; Ahmed, N. Synthesis and antibacterial and antifungal evaluation of some chalcone based sulfones and bisulfones. Eur. J. Med. Chem., 2013, 59, 23-30.
[47]
Xu, L.; Cheng, J.; Trudell, M.L. Chromium(VI) oxide catalyzed oxidation of sulfides to sulfones with periodic acid. J. Org. Chem., 2003, 68, 5388-5391.
[48]
Suryakiran, N. Srikanth, Reddy T.; Ashalatha, K.; Lakshman, M.; Venkateswarlu, Y. Facile polyethylene glycol (PEG-400) promoted synthesis of β-ketosulfones. Tetrahedron Lett., 2006, 47, 3853-3856.
[49]
Chen, C.C.; Waser, J. One-pot, three-component arylalkynyl sulfone synthesis. Org. Lett., 2015, 17, 736-739.
[50]
Staniszewska, M.; Bondaryk, M.; Ochal, Z. New synthetic sulfone derivatives inhibit growth, adhesion and the leucine arylamidase APE2 gene expression of Candida albicans in vitro. Bioorg. Med. Chem., 2015, 23, 314-321.
[51]
Umerski, N.; Manolikakes, G. Metal-free synthesis of diaryl sulfones from arylsulfinic acid salts and diaryliodonium salts. Org. Lett., 2013, 15, 188-191.
[52]
Zhdankin, V.V.; Stang, P.J. Alkyliodonium salts in organic synthesis. Tetrahedron, 1998, 54, 10927-10966.
[53]
Hamnett, D.J.; Moran, W.J. Improving alkynyl(aryl)iodonium salts: 2-anisyl as superior aryl group. Org. Biomol. Chem., 2014, 12, 4156-4162.
[54]
Suryakiran, N.; Prabhakar, P.; Srikanth Reddy, T.; Chinni Mahesh, K.; Rajesh, K.; Venkateswarlu, Y. Chemoselective mono halogenation of β-keto-sulfones using potassium halide and hydrogen peroxide; synthesis of halomethyl sulfones and dihalomethyl sulfones. Tetrahedron Lett., 2007, 48, 877-881.
[55]
Ochal, Z.; Kamiński, R. Transformations of bromodichloromethyl-4-chlorophenyl sulfone into New compounds with potential pesticidal activity. Pol. J. Appl. Chem., 2005, 49, 215-225.
[56]
Ochal, Z.; Mizerski, A.; Gajadhur, A.; Ejmocki, Z. Benzimidazole derivatives substituted fluoro-, difluoro- and trifluorometyhlsulfonyl group. PL Pat., 202745 B1, July 31, 2009.
[57]
Xu, W.; He, J.; He, M.; Han, F.; Chen, X.; Pan, Z.; Wang, J.; Tong, M. Synthesis and antifungal activity of novel sulfone derivatives containing 1,3,4-oxydiazole moieties. Molecules, 2011, 16, 9129-9141.
[58]
Ochal, Z.; Bretner, M.; Wolinowska, R.; Tyski, S. Synthesis and in vitro antibacterial activity of 5-halogenomethylsulfonyl-benzoimidazole and benzotriazole derivatives. Med. Chem., 2013, 9, 1129-1136.
[59]
Chen, C.J.; Song, B.A.; Yang, S.; Xu, G.F.; Bhadury, P.S.; Jin, L.H.; Hu, D.Y.; Li, Q.Z.; Liu, F.; Xue, W.; Lu, P.; Chen, Z. Synthesis and antifungal activities of 5-(3,4,5-trimethoxyphenyl)-2-sulfonyl-1,3,4-thiadiazole and 5-(3,4,5-trimethoxyphenyl)-2-sulfonyl-1,3,4-oxadiazole derivatives. Bioorg. Med. Chem., 2007, 15, 3981-3989.
[60]
Curti, C.; Laget, M.; Carle, A.O.; Gellis, A.; Vanelle, P. Rapid synthesis of sulfone derivatives as potential anti-infectious agents. Eur. J. Med. Chem., 2007, 42, 880-884.
[61]
Kumar, A.B.V.K.; Rao, K.S.V.K.; Chandra, M.S.; Subha, M.C.S.; Choi, Y.L. Synthesis and antimicrobial evaluation of sulfides, sulfoxides, and sulfones. J. Korean Soc. Appl. Biol. Chem., 2009, 52, 34-39.
[62]
Kumar, L.V.; Naik, P.J.; Naveen, M.; Chandrasekhar, T.; Reddy, A.B.; Penchalaiah, N.; Swamy, G.N. Synthesis and biological evaluation of some new 2,5-disubstituted 1,3,4-oxadiazoles from 3-(arylsulfonyl) propanehydrazides. Indian J. Chem., 2014, 53B, 208-211.
[63]
Borys, K.M.; Korzyński, M.D.; Ochal, Z. Derivatives of phenyl tribromomethyl sulfone as novel compounds with potential pesticidal activity. Beilstein J. Org. Chem., 2012, 8, 259-265.
[64]
Korzyński, M.D.; Borys, K.M.; Białek, J.; Ochal, Z. A novel method for the synthesis of aryl trihalomethyl sulfones and their derivatization: the search for new sulfone fungicides. Tetrahedron Lett., 2014, 55, 745-748.
[65]
Bondaryk, M.; Ochal, Z.; Staniszewska, M. Comparison of anti-Candida albicans activities of halogenomethylsulfonyl derivatives. Med. Chem. Res., 2015, 24, 1799-1813.
[66]
Staniszewska, M.; Bondaryk, M.; Ochal, Z. Susceptibility of Candida albicans to new synthetic sulfone derivatives. Arch. Pharm. Chem. Life Sci., 2015, 348, 132-143.
[67]
Staniszewska, M.; Bondaryk, M.; Wieczorek, M.; Estrada-Mata, E.; Mora-Montes, H.M.; Ochal, Z. Antifungal effect of novel 2-Bromo-2-Chloro-2-(4-Chlorophenylsulfonyl)-1-Phenylethanone against Candida strains. Front. Microbiol., 2016, 7, 1309.
[68]
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.
[69]
Staniszewska, M.; Bondaryk, M.; Ochal, Z. Method for testing adhesion of Candida spp. cells to the surface of a model of epithelial cells monolayer in vitro, method of estimation of inhibition level of Candida spp. cells adhesion to the epithelium cells and the compound to be applied in the treatment of mycosis diseases, preferably those caused by Candida spp. PL Patent Application, P.408765, July 4, 2014.
[70]
Ochal, Z.; Staniszewska, M.; Bondaryk, M.; Borowiecki, P. Application of halogen methyl aryl sulfones. PL Pat., P.408200, May 13, 2014.
[71]
Mehra, T.; Köberle, M.; Braunsdorf, C.; Mailänder-Sanchez, D.; Borelli, C.; Schaller, M. Alternative approaches to antifungal therapies. Exp. Dermatol., 2012, 21, 778-782.
[72]
Cui, J.; Ren, B.; Tong, Y.; Dai, H.; Zhang, L. Synergistic combinations of antifungals and anti-virulence agents to fight against Candida albicans. Virulence, 2015, 6, 362-371.
[73]
Bahn, Y.S. Exploiting fungal virulence-regulating transcription factors as novel antifungal drug targets. PLoS Pathog., 2015, 11, e1004936.
[74]
Gauwerky, K.; Borelli, C.; Korting, H.C. Targeting virulence: A new paradigm for antifungals. Drug Discov. Today, 2009, 14, 214-222.
[75]
Li, X.; Hou, Y.; Yue, L.; Liu, S.; Du, J.; Sun, S. Potential targets for antifungal drug discovery based on growth and virulence in Candida albicans. Antimicrob. Agents Chemother., 2015, 59, 5885-5891.
[76]
Naglik, J.R.; Challacombe, S.J.; Hube, B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol. Mol. Biol. Rev., 2003, 67, 400-428.
[77]
Wu, H.; Downs, D.; Ghosh, K.; Ghosh, A.K.; Staib, P.; Monod, M.; Tang, J. Candida albicans secreted aspartic proteases 4–6 induce apoptosis of epithelial cells by a novel Trojan horse mechanism. FASEB J., 2013, 27, 2132-2144.
[78]
Albrecht, A.; Felk, A.A.; Pichova, I.; Naglik, J.R.; Schaller, M.; de Groot, P.; MacCallum, D.; Odds, F.C.; Schäfer, W.; Klis, F. Glycosylphosphatidylinositol-anchored proteases of Candida albicans target proteins necessary for both cellular processes and host-pathogen interactions. J. Biol. Chem., 2006, 281, 688-694.
[79]
Sorgo, A.G.; Heilmann, C.J.; Brul, S.; de Koster, C.G.; Klis, F.M. Beyong the wall: Candida albicans secret(e)s to survive. FEMS Microbiol. Lett., 2013, 338, 10-17.
[80]
Naglik, J.; Albrecht, A.; Bader, O.; Hube, B. Candida albicans proteinases and host/pathogen interactions. Cell. Microbiol., 2004, 6, 915-928.
[81]
Bondaryk, M.; Ochal, Z.; Staniszewska, M. Sulfone derivatives reduce growth, adhesion and aspartic protease SAP2 gene expression. World J. Microbiol. Biotechnol., 2014, 30, 2511-2521.
[82]
Staniszewska, M.; Bondaryk, M.; Ochal, Z. Role of virulence determinants in Candida albicans’ resistance to novel 2-bromo-2-chloro-2-(4-chlorophenylsulfonyl)-1-phenylethanone. J. Fungi, 2017, 3, 32.
[83]
Newport, G.; Agabian, N. KEX2 influences Candida albicans proteinase secretion and hyphae formation. J. Biol. Chem., 1997, 272, 28954-28961.
[84]
Yang, S.; Kuang, Y.; Li, H.; Liu, Y.; Hui, X.; Li, P.; Jiang, Z.; Zhou, Y.; Wang, Y.; Xu, A.; Li, S.; Liu, P.; Wu, D. Enhanced production of recombinant secretory proteins in Pichia pastoris by optimizing Kex2 P1′ site. PLoS One, 2013, 8, e75347.
[85]
Bader, O.; Schaller, M.; Klein, S.; Kukula, J.; Haack, K.; Mühlschlegel, F.; Korting, H.C.; Schäfer, W.; Hube, B. The KEX2 gene of Candida glabrata is required for cell surface integrity. Mol. Microbiol., 2001, 41, 1431-1444.
[86]
Newport, G.; Kuo, A.; Flattery, A.; Gill, C.; Blake, J.J.; Kurtz, M.B.; Abruzzo, G.K.; Agabian, N. Inactivation of Kex2p diminishes the virulence of Candida albicans. J. Biol. Chem., 2003, 278, 1713-1720.
[87]
Bondaryk, M.; Grabowska-Jadach, I.; Ochal, Z.; Sygitowicz, G.; Staniszewska, M. Possible role of hydrolytic enzymes (Sap, Kex2) in Candida albicans response to aromatic compounds bearing a sulfone moiety. Chem. Pap., 2016, 70, 1336-1350.
[88]
Shareck, J.; Belhumeur, P. Modulation of morphogenesis in Candida albicans by various small molecules. Eukaryot. Cell, 2011, 10, 1004-1012.
[89]
Mayer, F.L.; Wilson, D.; Hube, B. Candida albicans pathogenicity mechanisms. Virulence, 2013, 15, 119-128.
[90]
Lo, H.J.; Köhler, J.R.; DiDomenico, B.; Loebenberg, D.; Cacciapuoti, A.; Fink, G.R. Nonfilamentous C. albicans mutants are avirulent. Cell, 1997, 90, 939-949.
[91]
Peters, B.M.; Palmer, G.E.; Nash, A.K.; Lilly, E.A.; Fidel, P.L., Jr; Noverr, M.C. Fungal morphogenetic pathways are required for the hallmark inflammatory response during Candida albicans vaginitis. Infect. Immun., 2014, 82, 532-543.
[92]
Pierce, C.G.; Lopez-Ribot, J.L. Candidiasis drug discovery and development: New approaches targeting virulence for discovering and identifying new drugs. Expert Opin. Drug Discov., 2013, 8, 1117-1126.
[93]
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, 849-856.
[94]
Bink, A.; Govaert, G.; Vandenbosch, D.; Kuchariková, S.; Coenye, T.; Nelis, H.; Van Dijck, P.; Cammue, B.P.; Thevissen, K. Transcription factor Efg1 contributes to the tolerance of Candida albicans biofilms against antifungal agents in vitro and in vivo. J. Med. Microbiol., 2012, 61, 813-189.
[95]
Liu, H. Co-regulation of pathogenesis with dimorphism and phenotypic switching in Candida albicans, a commensal and a pathogen. Int. J. Med. Microbiol., 2002, 292, 299-311.
[96]
Nobile, C.J.; Fox, E.P.; Nett, J.E.; Sorrels, 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, 126-138.
[97]
Zavrel, M.; Majer, O.; Kuchler, K.; Rupp, S. Transcription factor Efg1 shows a haploinsufficiency phenotype in modulating the cell wall architecture and immunogenicity of Candida albicans. Eukaryot. Cell, 2012, 11, 129-140.
[98]
Sherry, L.; Rajendran, R.; Lappin, D.F.; Borghi, E.; Perdoni, F.; Falleni, M.; Tosi, D.; Smith, K.; Williams, C.; Jones, B.; Nile, C.J.; Ramage, G. Biofilms formed by Candida albicans bloodstream isolates display phenotypic and transcriptional heterogeneity that are associated with resistance and pathogenicity. BMC Microbiol., 2014, 14, 182.
[99]
dos Santos, J.D.; Piva, E.; Vilela, S.F.; Jorge, A.O.; Junqueira, J.C. Mixed biofilms formed by C. albicans and non-albicans species: A study of microbial interactions. Braz. Oral Res., 30, e23.
[100]
Nobile, C.J.; Johnson, A.D. Candida albicans biofilms and human disease. Annu. Rev. Microbiol., 2016, 69, 71-92.
[101]
Shi, L.; Li, P.; Wang, W.; Gao, M.; Wu, Z.; Song, X.; Hu, D. Antibacterial activity and mechanism of action of sulfone derivatives containing 1,3,4-oxadiazole moieties on rice bacterial leaf blight. Molecules, 2015, 20, 11660-11675.
[102]
Mora-Montes, H.M.; Gacser, A. Editorial: Recent advances in the study of the host-fungus interaction. Front. Microbiol., 2016, 7, 1694.
[103]
Haque, F.; Alfatah, M.; Ganesan, K.; Bhattacharyya, M.S. Inhibitory effect of sophorolipid on Candida albicans biofilm formation and hyphal growth. Sci. Rep., 2016, 6, 23575.
[104]
Rajeshkumar, R.; Sundararaman, M. Emergence of Candida spp. And exploration of natural bioactive molecules for anticandidal therapy – status quo. Mycoses, 2012, 55, e60-e73.
[105]
Gordon, Y.J.; Romanowski, E.G.; McDermott, A.M. A review of antimicrobial peptides and their therapeutic potential as anti-infective drugs. Curr. Eye Res., 2005, 30, 505-515.
[106]
Ghabbour, H.A.; Qabeel, M.M.; Eldehna, W.M.; Al-Dhfyan, A.; Abdel-Aziz, H. Design, synthesis, and molecular docking of 1-(1-(4-chlorophenyl)-2-(phenylsulfonyl)ethylidene)-2-phenylhydrazine as potent nonazole anticandidal agent. J. Chem., 2014, 154357.
[107]
Fares, M.; Said, M.A.; Alsherbiny, M.A.; Eladwy, R.A.; Almahli, H.; Abdel-Aziz, M.M.; Ghabbour, H.A.; Eldehna, W.M.; Abdel-Aziz, H.A. Synthesis, biological evaluation and molecular docking of certain sulfones as potential nonazole antifungal agents. Molecules, 2016, 21, E114.
[108]
Hasim, S.; Allison, D.P.; Retterer, S.T.; Hopke, A. β-(1,3)-glucan unmasking in some Candida albicans mutants correlates with increases in cell wall surface roughness and decreases in cell wall elasticity. Infect. Immun., 2016, 85, e00601-e00616.
[109]
Davis, S.E.; Hopke, A. Minkin, Jr.; S.C. Montedonico, A.E.; Wheeler, R.T.; Reynolds, TB. Masking of β(1-3)-glucan in the cell wall of Candida albicans from detection by innate immune cells depends on phosphatidylserine. Infect. Immun., 2014, 82, 4405-4413.
[110]
El Kirat Chatel, S.; Dufrene, Y.F. Nanoscale imaging of the Candida-macrophage interaction using correlated fluorescence-atomic force microscopy. ACS Nano, 2012, 6, 10792-10799.
[111]
Formosa, C.; Schiavone, M.; Martin-Yken, H.; Francois, J.M.; Duval, R.E.; Dague, E. Nanoscale effects of caspofungin against two yeast species, Saccharomyces cerevisiae and Candida albicans. Antimicrob. Agents Chemother., 2013, 57, 3498-3506.
[112]
Formosa, C.; Pillet, F.; Schiavone, M.; Duval, R.E.; Ressier, L.; Dague, E. Generation of living cells arrays for atomic force microscopy. Nat. Protoc., 2015, 10, 199-204.
[113]
Repnik, U.; Česen, M.H.; Turk, B. Lysosomal membrane permeabilization in cell death: Concepts and challenges. Mitochondrion, 2014, 19, 49-57.
[114]
Brown, A.J.P.; Budge, S.; Koloriti, D.; Tillmann, A.; Jacobsen, M.D.; Yin, Z.; Ene, I.V.; Bohovych, I.; Sandai, D.; Kastora, S. Stress adaptation in a pathogenic fungus. J. Exp. Biol., 2014, 217, 144-155.

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