Emerging Complexity and the Need for Advanced Drug Delivery in Targeting Candida Species

Author(s): Ridhima Wadhwa, Parijat Pandey, Gaurav Gupta, Taru Aggarwal, Nitesh Kumar, Meenu Mehta, Saurabh Satija, Monica Gulati, Jyotsna R. Madan, Harish Dureja, Sri R. Balusamy, Haribalan Perumalsamy, Pawan K. Maurya, Trudi Collet, Murtaza M. Tambuwala, Philip M. Hansbro, Dinesh Kumar Chellappan*, Kamal Dua*

Journal Name: Current Topics in Medicinal Chemistry

Volume 19 , Issue 28 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Background: Candida species are the important etiologic agents for candidiasis, the most prevalent cause of opportunistic fungal infections. Candida invasion results in mucosal to systemic infections through immune dysfunction and helps in further invasion and proliferation at several sites in the host. The host defence system utilizes a wide array of the cells, proteins and chemical signals that are distributed in blood and tissues which further constitute the innate and adaptive immune system. The lack of antifungal agents and their limited therapeutic effects have led to high mortality and morbidity related to such infections.

Methods: The necessary information collated on this review has been gathered from various literature published from 1995 to 2019.

Results: This article sheds light on novel drug delivery approaches to target the immunological axis for several Candida species (C. albicans, C. glabrata, C. parapsilosis, C. tropicalis, C. krusei, C. rugose, C. hemulonii, etc.).

Conclusion: It is clear that the novel drug delivery approaches include vaccines, adoptive transfer of primed immune cells, recombinant cytokines, therapeutic antibodies, and nanoparticles, which have immunomodulatory effects. Such advancements in targeting various underpinning mechanisms using the concept of novel drug delivery will provide a new dimension to the fungal infection clinic particularly due to Candida species with improved patient compliance and lesser side effects. This advancement in knowledge can also be extended to target various other similar microbial species and infections.

Keywords: Candida, Immune cells, Receptor-mediated recognition, Immune-compromised patients, Novel drug delivery system, Antifungal therapy.

[1]
Arikan-Akdagli, S.; Ghannoum, M.; Meis, J.F. Antifungal resistance: specific focus on multidrug resistance in candida auris and secondary azole resistance in aspergillus fumigatus. J. Fungi (Basel), 2018, 4(4), 129.
[http://dx.doi.org/10.3390/jof4040129] [PMID: 30563053]
[2]
Ko, J.H.; Jung, D.S.; Lee, J.Y.; Kim, H.A.; Ryu, S.Y.; Jung, S.I.; Joo, E.J.; Cheon, S.; Kim, Y.S.; Kim, S.W.; Cho, S.Y.; Kang, C.I.; Chung, D.R.; Lee, N.Y.; Peck, K.R. Changing epidemiology of non-albicans candidemia in Korea. J. Infect. Chemother., 2018, 25(5), 388.
[3]
Nasri, E.; Fakhim, H.; Vaezi, A.; Khalilzadeh, S.; Ahangarkani, F.; Laal Kargar, M.; Abtahian, Z.; Badali, H. Airway colonisation by Candida and Aspergillus species in Iranian cystic fibrosis patients. Mycoses, 2019, 62(5), 434-440.
[http://dx.doi.org/10.1111/myc.12898] [PMID: 30681747]
[4]
Otašević, S.; Momčilović, S.; Golubović, M.; Ignjatović, A.; Rančić, N.; Đorđević, M.; Ranđelović, M.; Hay, R.; Arsić-Arsenijević, V. Species distribution and epidemiological characteristics of superficial fungal infections in Southeastern Serbia. Mycoses, 2019, 62(5), 458-465.
[http://dx.doi.org/10.1111/myc.12900] [PMID: 30687976]
[5]
Reagan, K.L.; Dear, J.D.; Kass, P.H.; Sykes, J.E. Risk factors for Candida urinary tract infections in dogs and cats. J. Vet. Intern. Med., 2019, 33(2), 648-653.
[http://dx.doi.org/10.1111/jvim.15444] [PMID: 30758081]
[6]
Schlager, E.; Ashack, K.; Khachemoune, A. Erosio interdigitalis blastomycetica: A review of interdigital candidiasis. Dermatol. Online J., 2018, 24(8) 13030/qt8tm443f6.
[PMID: 30677843]
[7]
Walsh, T.J.; Katragkou, A.; Chen, T.; Salvatore, C.M.; Roilides, E. Invasive candidiasis in infants and children: Recent advances in epidemiology, diagnosis, and treatment. J. Fungi (Basel), 2019, 5(1), 11.
[http://dx.doi.org/10.3390/jof5010011] [PMID: 30678324]
[8]
Abe, M.; Kinjo, Y.; Ueno, K.; Takatsuka, S.; Nakamura, S.; Ogura, S.; Kimura, M.; Araoka, H.; Sadamoto, S.; Shinozaki, M.; Shibuya, K.; Yoneyama, A.; Kaku, M.; Miyazaki, Y. Differences in ocular complications between candida albicans and non-albicans candida infection analyzed by epidemiology and a mouse ocular candidiasis model. Front. Microbiol., 2018, 9, 2477.
[http://dx.doi.org/10.3389/fmicb.2018.02477] [PMID: 30386320]
[9]
Awad, L.; Tamim, H.; Abdallah, D.; Salameh, M.; Mugharbil, A.; Jisr, T.; Zahran, K.; Droubi, N.; Ibrahim, A.; Moghnieh, R. Correlation between antifungal consumption and the distribution of Candida species in different hospital departments of a Lebanese medical Centre. BMC Infect. Dis., 2018, 18(1), 589.
[http://dx.doi.org/10.1186/s12879-018-3512-z] [PMID: 30453891]
[10]
Cao, H.F.; Dong, Y.; Yang, T.; Li, B.B.; Zhao, J. [Prevalence of candida albicans and its relationship with early childhood caries among children of three ethnic groups (Han, Uygur, Mongolian) in bortala mongol autonomous prefecture of xinjiang uygur autonomous region]. Zhonghua kou qiang yi xue za zhi, 2018, 53(11), 730.
[11]
Cortegiani, A.; Misseri, G.; Fasciana, T.; Giammanco, A.; Giarratano, A.; Chowdhary, A. Epidemiology, clinical characteristics, resistance, and treatment of infections by Candida auris. J. Intensive Care, 2018, 6, 69.
[http://dx.doi.org/10.1186/s40560-018-0342-4] [PMID: 30397481]
[12]
Sadrossadati, S.Z.; Ghahri, M.; Imani Fooladi, A.A.; Sayyahfar, S.; Beyraghi, S.; Baseri, Z. Phenotypic and genotypic characterization of Candida species isolated from candideamia in Iran. Curr Med Mycol, 2018, 4(2), 14-20.
[http://dx.doi.org/10.18502/cmm.4.2.64] [PMID: 30324152]
[13]
Marton, T.; Feri, A.; Commere, P.H.; Maufrais, C.; d’Enfert, C.; Legrand, M. Identification of recessive lethal alleles in the diploid genome of a candida albicans laboratory strain unveils a potential role of repetitive sequences in buffering their deleterious impact. MSphere, 2019, 4(1), e00709-e00718.
[http://dx.doi.org/10.1128/mSphere.00709-18] [PMID: 30760617]
[14]
Shimamura, S.; Miyazaki, T.; Tashiro, M.; Takazono, T.; Saijo, T.; Yamamoto, K.; Imamura, Y.; Izumikawa, K.; Yanagihara, K.; Kohno, S.; Mukae, H. Autophagy-inducing factor atg1 is required for virulence in the pathogenic fungus candida glabrata. Front. Microbiol., 2019, 10, 27.
[http://dx.doi.org/10.3389/fmicb.2019.00027] [PMID: 30761093]
[15]
Van Ende, M.; Wijnants, S.; Van Dijck, P. Sugar Sensing and Signaling in Candida albicans and Candida glabrata. Front. Microbiol., 2019, 10, 99.
[http://dx.doi.org/10.3389/fmicb.2019.00099] [PMID: 30761119]
[16]
Welsh, R.M.; Sexton, D.J.; Forsberg, K.; Vallabhaneni, S.; Litvintseva, A. Insights into the unique nature of the east asian clade of the emerging pathogenic yeast candida auris. J. Clin. Microbiol., 2019, 57(4), e00007-e00019.
[http://dx.doi.org/10.1128/JCM.00007-19] [PMID: 30760535]
[17]
Wensing, L.; Sharma, J.; Uthayakumar, D.; Proteau, Y.; Chavez, A.; Shapiro, R.S. A CRISPR Interference platform for efficient genetic repression in candida albicans. MSphere, 2019, 4(1), e00002-e00019.
[http://dx.doi.org/10.1128/mSphere.00002-19] [PMID: 30760609]
[18]
Pfaller, M.A.; Diekema, D.J. Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev., 2007, 20(1), 133-163.
[http://dx.doi.org/10.1128/CMR.00029-06] [PMID: 17223626]
[19]
Gudlaugsson, O.; Gillespie, S.; Lee, K.; Vande Berg, J.; Hu, J.; Messer, S.; Herwaldt, L.; Pfaller, M.; Diekema, D. Attributable mortality of nosocomial candidemia, revisited. Clin. Infect. Dis., 2003, 37(9), 1172-1177.
[http://dx.doi.org/10.1086/378745] [PMID: 14557960]
[20]
Pappas, P.G.; Kauffman, C.A.; Andes, D.; Benjamin, D.K., Jr; Calandra, T.F.; Edwards, J.E., Jr; Filler, S.G.; Fisher, J.F.; Kullberg, B-J.; Ostrosky-Zeichner, L. Clinical practice guidelines for the management of candidiasis: 2009 update of the infectious diseases society of America. Clin. Infect. Dis., 2009, 48(5), 503-537.
[http://dx.doi.org/10.1086/596757] [PMID: 19191635]
[21]
Pittet, D.; Li, N.; Woolson, R.F.; Wenzel, R.P. Microbiological factors influencing the outcome of nosocomial bloodstream infections: A 6-year validated, population-based model. Clin. Infect. Dis., 1997, 24(6), 1068-1078.
[http://dx.doi.org/10.1086/513640] [PMID: 9195059]
[22]
Zaoutis, T.E.; Argon, J.; Chu, J.; Berlin, J.A.; Walsh, T.J.; Feudtner, C. The epidemiology and attributable outcomes of candidemia in adults and children hospitalized in the United States: a propensity analysis. Clin. Infect. Dis., 2005, 41(9), 1232-1239.
[http://dx.doi.org/10.1086/496922] [PMID: 16206095]
[23]
Wilson, L.S.; Reyes, C.M.; Stolpman, M.; Speckman, J.; Allen, K.; Beney, J. The direct cost and incidence of systemic fungal infections. Value Health, 2002, 5(1), 26-34.
[http://dx.doi.org/10.1046/j.1524-4733.2002.51108.x] [PMID: 11873380]
[24]
Bhattacharjee, P. Epidemiology and antifungal susceptibility of Candida species in a tertiary care hospital, Kolkata, India. Curr. Med. Mycol., 2016, 2(2), 20.
[25]
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]
[26]
Janeway, C.A., Jr; Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol., 2002, 20(1), 197-216.
[http://dx.doi.org/10.1146/annurev.immunol.20.083001.084359] [PMID: 11861602]
[27]
Plato, A.; Willment, J.A.; Brown, G.D. C-type lectin-like receptors of the dectin-1 cluster: ligands and signaling pathways. Int. Rev. Immunol., 2013, 32(2), 134-156.
[http://dx.doi.org/10.3109/08830185.2013.777065] [PMID: 23570314]
[28]
Bourgeois, C.; Kuchler, K. Fungal pathogens-a sweet and sour treat for toll-like receptors. Front. Cell. Infect. Microbiol., 2012, 2, 142.
[http://dx.doi.org/10.3389/fcimb.2012.00142] [PMID: 23189270]
[29]
Takeuchi, O.; Akira, S. Pattern recognition receptors and inflammation. Cell, 2010, 140(6), 805-820.
[http://dx.doi.org/10.1016/j.cell.2010.01.022] [PMID: 20303872]
[30]
Rogier, R.; Koenders, M.I.; Abdollahi-Roodsaz, S. Toll-like receptor mediated modulation of T cell response by commensal intestinal microbiota as a trigger for autoimmune arthritis. J. Immunol. Res., 2015, 2015527696
[http://dx.doi.org/10.1155/2015/527696] [PMID: 25802876]
[31]
Suresh, R.; Mosser, D.M. Pattern recognition receptors in innate immunity, host defense, and immunopathology. Adv. Physiol. Educ., 2013, 37(4), 284-291.
[http://dx.doi.org/10.1152/advan.00058.2013] [PMID: 24292903]
[32]
Pang, B. Efficient search and comparison algorithms for 3D protein binding site retrieval and structure alignment from large-scale databases.. PhD Thesis, University of Missouri: Columbia,, 2013.
[33]
Del Fresno, C.; Iborra, S.; Saz-Leal, P.; Martínez-López, M.; Sancho, D. Flexible signaling of myeloid C-type lectin receptors in immunity and inflammation. Front. Immunol., 2018, 9, 804.
[http://dx.doi.org/10.3389/fimmu.2018.00804] [PMID: 29755458]
[34]
Strasser, D.; Neumann, K.; Bergmann, H.; Marakalala, M.J.; Guler, R.; Rojowska, A.; Hopfner, K-P.; Brombacher, F.; Urlaub, H.; Baier, G.; Brown, G.D.; Leitges, M.; Ruland, J. Syk kinase-coupled C-type lectin receptors engage protein kinase C-σ to elicit Card9 adaptor-mediated innate immunity. Immunity, 2012, 36(1), 32-42.
[http://dx.doi.org/10.1016/j.immuni.2011.11.015] [PMID: 22265677]
[35]
Gringhuis, S.I.; den Dunnen, J.; Litjens, M.; van der Vlist, M.; Wevers, B.; Bruijns, S.C.; Geijtenbeek, T.B. Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-kappaB activation through Raf-1 and Syk. Nat. Immunol., 2009, 10(2), 203-213.
[http://dx.doi.org/10.1038/ni.1692] [PMID: 19122653]
[36]
Gazendam, R.P.; van Hamme, J.L.; Tool, A.T.; van Houdt, M.; Verkuijlen, P.J.; Herbst, M.; Liese, J.G.; van de Veerdonk, F.L.; Roos, D.; van den Berg, T.K.; Kuijpers, T.W. Two independent killing mechanisms of Candida albicans by human neutrophils: evidence from innate immunity defects. Blood, 2014, 124(4), 590-597.
[http://dx.doi.org/10.1182/blood-2014-01-551473] [PMID: 24948657]
[37]
van Bruggen, R.; Drewniak, A.; Jansen, M.; van Houdt, M.; Roos, D.; Chapel, H.; Verhoeven, A.J.; Kuijpers, T.W. Complement receptor 3, not Dectin-1, is the major receptor on human neutrophils for β-glucan-bearing particles. Mol. Immunol., 2009, 47(2-3), 575-581.
[http://dx.doi.org/10.1016/j.molimm.2009.09.018] [PMID: 19811837]
[38]
Netea, M.G.; Brown, G.D.; Kullberg, B.J.; Gow, N.A. An integrated model of the recognition of Candida albicans by the innate immune system. Nat. Rev. Microbiol., 2008, 6(1), 67-78.
[http://dx.doi.org/10.1038/nrmicro1815] [PMID: 18079743]
[39]
Cambi, A.; Netea, M.G.; Mora-Montes, H.M.; Gow, N.A.; Hato, S.V.; Lowman, D.W.; Kullberg, B-J.; Torensma, R.; Williams, D.L.; Figdor, C.G. Dendritic cell interaction with Candida albicans critically depends on N-linked mannan. J. Biol. Chem., 2008, 283(29), 20590-20599.
[http://dx.doi.org/10.1074/jbc.M709334200] [PMID: 18482990]
[40]
Means, T.K.; Mylonakis, E.; Tampakakis, E.; Colvin, R.A.; Seung, E.; Puckett, L.; Tai, M.F.; Stewart, C.R.; Pukkila-Worley, R.; Hickman, S.E.; Moore, K.J.; Calderwood, S.B.; Hacohen, N.; Luster, A.D.; El Khoury, J. Evolutionarily conserved recognition and innate immunity to fungal pathogens by the scavenger receptors SCARF1 and CD36. J. Exp. Med., 2009, 206(3), 637-653.
[http://dx.doi.org/10.1084/jem.20082109] [PMID: 19237602]
[41]
Zheng, N-X.; Wang, Y.; Hu, D-D.; Yan, L.; Jiang, Y-Y. The role of pattern recognition receptors in the innate recognition of Candida albicans. Virulence, 2015, 6(4), 347-361.
[http://dx.doi.org/10.1080/21505594.2015.1014270] [PMID: 25714264]
[42]
Miramón, P.; Kasper, L.; Hube, B. Thriving within the host: Candida spp. interactions with phagocytic cells. Med. Microbiol. Immunol. (Berl.), 2013, 202(3), 183-195.
[http://dx.doi.org/10.1007/s00430-013-0288-z] [PMID: 23354731]
[43]
Svobodová, E.; Staib, P.; Losse, J.; Hennicke, F.; Barz, D.; Józsi, M. Differential interaction of the two related fungal species Candida albicans and Candida dubliniensis with human neutrophils. J. Immunol., 2012, 189(5), 2502-2511.
[http://dx.doi.org/10.4049/jimmunol.1200185] [PMID: 22851712]
[44]
Amulic, B.; Cazalet, C.; Hayes, G.L.; Metzler, K.D.; Zychlinsky, A. Neutrophil function: from mechanisms to disease. Annu. Rev. Immunol., 2012, 30, 459-489.
[http://dx.doi.org/10.1146/annurev-immunol-020711-074942] [PMID: 22224774]
[45]
Mattila, J.T.; Ojo, O.O.; Kepka-Lenhart, D.; Marino, S.; Kim, J.H.; Eum, S.Y.; Via, L.E.; Barry, C.E., III; Klein, E.; Kirschner, D.E.; Morris, S.M., Jr; Lin, P.L.; Flynn, J.L. Microenvironments in tuberculous granulomas are delineated by distinct populations of macrophage subsets and expression of nitric oxide synthase and arginase isoforms. J. Immunol., 2013, 191(2), 773-784.
[http://dx.doi.org/10.4049/jimmunol.1300113] [PMID: 23749634]
[46]
Hesse, M.; Modolell, M.; La Flamme, A.C.; Schito, M.; Fuentes, J.M.; Cheever, A.W.; Pearce, E.J.; Wynn, T.A. Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of L-arginine metabolism. J. Immunol., 2001, 167(11), 6533-6544.
[http://dx.doi.org/10.4049/jimmunol.167.11.6533] [PMID: 11714822]
[47]
Jiménez-López, C.; Lorenz, M.C. Fungal immune evasion in a model host-pathogen interaction: Candida albicans versus macrophages. PLoS Pathog., 2013, 9(11)e1003741
[http://dx.doi.org/10.1371/journal.ppat.1003741] [PMID: 24278014]
[48]
Bonifazi, P.; Zelante, T.; D’Angelo, C.; De Luca, A.; Moretti, S.; Bozza, S.; Perruccio, K.; Iannitti, R.G.; Giovannini, G.; Volpi, C.; Fallarino, F.; Puccetti, P.; Romani, L. Balancing inflammation and tolerance in vivo through dendritic cells by the commensal Candida albicans. Mucosal Immunol., 2009, 2(4), 362-374.
[http://dx.doi.org/10.1038/mi.2009.17] [PMID: 19421183]
[49]
Romani, L. Immunity to fungal infections. Nat. Rev. Immunol., 2004, 4(1), 1-23.
[http://dx.doi.org/10.1038/nri1255] [PMID: 14661066]
[50]
Cenci, E.; Mencacci, A.; Spaccapelo, R.; Tonnetti, L.; Mosci, P.; Enssle, K-H.; Puccetti, P.; Romani, L.; Bistoni, F. T helper cell type 1 (Th1)- and Th2-like responses are present in mice with gastric candidiasis but protective immunity is associated with Th1 development. J. Infect. Dis., 1995, 171(5), 1279-1288.
[http://dx.doi.org/10.1093/infdis/171.5.1279] [PMID: 7751704]
[51]
Gringhuis, S.I.; Wevers, B.A.; Kaptein, T.M.; van Capel, T.M.; Theelen, B.; Boekhout, T.; de Jong, E.C.; Geijtenbeek, T.B. Selective C-Rel activation via Malt1 controls anti-fungal T(H)-17 immunity by dectin-1 and dectin-2. PLoS Pathog., 2011, 7(1)e1001259
[http://dx.doi.org/10.1371/journal.ppat.1001259] [PMID: 21283787]
[52]
Kuchroo, V.K.; Awasthi, A. Emerging new roles of Th17 cells. Eur. J. Immunol., 2012, 42(9), 2211-2214.
[http://dx.doi.org/10.1002/eji.201242872] [PMID: 22949318]
[53]
Korn, T.; Bettelli, E.; Oukka, M.; Kuchroo, V.K. IL-17 and Th17 Cells. Annu. Rev. Immunol., 2009, 27, 485-517.
[http://dx.doi.org/10.1146/annurev.immunol.021908.132710] [PMID: 19132915]
[54]
Hernández-Santos, N.; Gaffen, S.L. Th17 cells in immunity to Candida albicans. Cell Host Microbe, 2012, 11(5), 425-435.
[http://dx.doi.org/10.1016/j.chom.2012.04.008] [PMID: 22607796]
[55]
De Luca, A.; Carvalho, A.; Cunha, C.; Iannitti, R.G.; Pitzurra, L.; Giovannini, G.; Mencacci, A.; Bartolommei, L.; Moretti, S.; Massi-Benedetti, C.; Fuchs, D.; De Bernardis, F.; Puccetti, P.; Romani, L. IL-22 and IDO1 affect immunity and tolerance to murine and human vaginal candidiasis. PLoS Pathog., 2013, 9(7)e1003486
[http://dx.doi.org/10.1371/journal.ppat.1003486] [PMID: 23853597]
[56]
Casadevall, A.; Pirofski, L.A. Immunoglobulins in defense, pathogenesis, and therapy of fungal diseases. Cell Host Microbe, 2012, 11(5), 447-456.
[http://dx.doi.org/10.1016/j.chom.2012.04.004] [PMID: 22607798]
[57]
Calcedo, R.; Ramirez-Garcia, A.; Abad, A.; Rementeria, A.; Pontón, J.; Hernando, F.L. Phosphoglycerate kinase and fructose bisphosphate aldolase of Candida albicans as new antigens recognized by human salivary IgA. Rev. Iberoam. Micol., 2012, 29(3), 172-174.
[http://dx.doi.org/10.1016/j.riam.2011.07.004] [PMID: 21906693]
[58]
Sandini, S.; La Valle, R.; Deaglio, S.; Malavasi, F.; Cassone, A.; De Bernardis, F. A highly immunogenic recombinant and truncated protein of the secreted aspartic proteases family (rSap2t) of Candida albicans as a mucosal anticandidal vaccine. FEMS Immunol. Med. Microbiol., 2011, 62(2), 215-224.
[http://dx.doi.org/10.1111/j.1574-695X.2011.00802.x] [PMID: 21535228]
[59]
Brena, S.; Cabezas-Olcoz, J.; Moragues, M.D.; Fernández de Larrinoa, I.; Domínguez, A.; Quindós, G.; Pontón, J. Fungicidal monoclonal antibody C7 interferes with iron acquisition in Candida albicans. Antimicrob. Agents Chemother., 2011, 55(7), 3156-3163.
[http://dx.doi.org/10.1128/AAC.00892-10] [PMID: 21518848]
[60]
Martinez, L.R.; Casadevall, A. Specific antibody can prevent fungal biofilm formation and this effect correlates with protective efficacy. Infect. Immun., 2005, 73(10), 6350-6362.
[http://dx.doi.org/10.1128/IAI.73.10.6350-6362.2005] [PMID: 16177306]
[61]
Moragues, M.D.; Omaetxebarria, M.J.; Elguezabal, N.; Sevilla, M.J.; Conti, S.; Polonelli, L.; Pontón, J. A monoclonal antibody directed against a Candida albicans cell wall mannoprotein exerts three anti-C. albicans activities. Infect. Immun., 2003, 71(9), 5273-5279.
[http://dx.doi.org/10.1128/IAI.71.9.5273-5279.2003] [PMID: 12933874]
[62]
Steele, C.; Rapaka, R.R.; Metz, A.; Pop, S.M.; Williams, D.L.; Gordon, S.; Kolls, J.K.; Brown, G.D. The beta-glucan receptor dectin-1 recognizes specific morphologies of Aspergillus fumigatus. PLoS Pathog., 2005, 1(4)e42
[http://dx.doi.org/10.1371/journal.ppat.0010042] [PMID: 16344862]
[63]
Gringhuis, S.I.; Kaptein, T.M.; Wevers, B.A.; Theelen, B.; van der Vlist, M.; Boekhout, T.; Geijtenbeek, T.B. Dectin-1 is an extracellular pathogen sensor for the induction and processing of IL-1β via a noncanonical caspase-8 inflammasome. Nat. Immunol., 2012, 13(3), 246-254.
[http://dx.doi.org/10.1038/ni.2222] [PMID: 22267217]
[64]
Gross, O.; Poeck, H.; Bscheider, M.; Dostert, C.; Hannesschläger, N.; Endres, S.; Hartmann, G.; Tardivel, A.; Schweighoffer, E.; Tybulewicz, V.; Mocsai, A.; Tschopp, J.; Ruland, J. Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature, 2009, 459(7245), 433-436.
[http://dx.doi.org/10.1038/nature07965] [PMID: 19339971]
[65]
Wellington, M.; Koselny, K.; Sutterwala, F.S.; Krysan, D.J. Candida albicans triggers NLRP3-mediated pyroptosis in macrophages. Eukaryot. Cell, 2014, 13(2), 329-340.
[http://dx.doi.org/10.1128/EC.00336-13] [PMID: 24376002]
[66]
Tomalka, J.; Ganesan, S.; Azodi, E.; Patel, K.; Majmudar, P.; Hall, B.A.; Fitzgerald, K.A.; Hise, A.G. A novel role for the NLRC4 inflammasome in mucosal defenses against the fungal pathogen Candida albicans. PLoS Pathog., 2011, 7(12)e1002379
[http://dx.doi.org/10.1371/journal.ppat.1002379] [PMID: 22174673]
[67]
Netea, M.G.; Nold-Petry, C.A.; Nold, M.F.; Joosten, L.A.; Opitz, B.; van der Meer, J.H.; van de Veerdonk, F.L.; Ferwerda, G.; Heinhuis, B.; Devesa, I.; Funk, C.J.; Mason, R.J.; Kullberg, B.J.; Rubartelli, A.; van der Meer, J.W.; Dinarello, C.A. Differential requirement for the activation of the inflammasome for processing and release of IL-1β in monocytes and macrophages. Blood, 2009, 113(10), 2324-2335.
[http://dx.doi.org/10.1182/blood-2008-03-146720] [PMID: 19104081]
[68]
van de Veerdonk, F.L.; Joosten, L.A.; Devesa, I.; Mora-Montes, H.M.; Kanneganti, T-D.; Dinarello, C.A.; van der Meer, J.W.; Gow, N.A.; Kullberg, B.J.; Netea, M.G. Bypassing pathogen-induced inflammasome activation for the regulation of interleukin-1β production by the fungal pathogen Candida albicans. J. Infect. Dis., 2009, 199(7), 1087-1096.
[http://dx.doi.org/10.1086/597274] [PMID: 19222370]
[69]
Brown, G.D.; Denning, D.W.; Gow, N.A.; Levitz, S.M.; Netea, M.G.; White, T.C. Hidden killers: human fungal infections. Science translational medicine., 2012, 4(165)165rv113
[http://dx.doi.org/10.1126/scitranslmed.3004404]
[70]
Calderone, R.; Gow, N.A. Host recognition by Candida species. Candida and candidiasis; ASM Press: Washington, DC, 2002, pp. 67-86.
[71]
López-Martínez, R. Candidosis, a new challenge. Clin. Dermatol., 2010, 28(2), 178-184.
[http://dx.doi.org/10.1016/j.clindermatol.2009.12.014] [PMID: 20347660]
[72]
Redding, S.W.; Zellars, R.C.; Kirkpatrick, W.R.; McAtee, R.K.; Caceres, M.A.; Fothergill, A.W.; Lopez-Ribot, J.L.; Bailey, C.W.; Rinaldi, M.G.; Patterson, T.F. Epidemiology of oropharyngeal Candida colonization and infection in patients receiving radiation for head and neck cancer. J. Clin. Microbiol., 1999, 37(12), 3896-3900.
[PMID: 10565903]
[73]
Thompson, G.R., III; Patel, P.K.; Kirkpatrick, W.R.; Westbrook, S.D.; Berg, D.; Erlandsen, J.; Redding, S.W.; Patterson, T.F. Oropharyngeal candidiasis in the era of antiretroviral therapy. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod., 2010, 109(4), 488-495.
[http://dx.doi.org/10.1016/j.tripleo.2009.11.026] [PMID: 20156694]
[74]
Fidel, P.L., Jr Vaginal candidiasis: review and role of local mucosal immunity. AIDS Patient Care STDS, 1998, 12(5), 359-366.
[http://dx.doi.org/10.1089/apc.1998.12.359] [PMID: 11361971]
[75]
Edmond, M.B.; Wallace, S.E.; McClish, D.K.; Pfaller, M.A.; Jones, R.N.; Wenzel, R.P. Nosocomial bloodstream infections in United States hospitals: a three-year analysis. Clin. Infect. Dis., 1999, 29(2), 239-244.
[http://dx.doi.org/10.1086/520192] [PMID: 10476719]
[76]
Ostrosky-Zeichner, L.; Casadevall, A.; Galgiani, J.N.; Odds, F.C.; Rex, J.H. An insight into the antifungal pipeline: selected new molecules and beyond. Nat. Rev. Drug Discov., 2010, 9(9), 719-727.
[http://dx.doi.org/10.1038/nrd3074] [PMID: 20725094]
[77]
Odds, F.C.; Brown, A.J.; Gow, N.A. Antifungal agents: mechanisms of action. Trends Microbiol., 2003, 11(6), 272-279.
[http://dx.doi.org/10.1016/S0966-842X(03)00117-3] [PMID: 12823944]
[78]
Perea, S.; López-Ribot, J.L.; Kirkpatrick, W.R.; McAtee, R.K.; Santillán, R.A.; Martínez, M.; Calabrese, D.; Sanglard, D.; Patterson, T.F. Prevalence of molecular mechanisms of resistance to azole antifungal agents in Candida albicans strains displaying high-level fluconazole resistance isolated from human immunodeficiency virus-infected patients. Antimicrob. Agents Chemother., 2001, 45(10), 2676-2684.
[http://dx.doi.org/10.1128/AAC.45.10.2676-2684.2001] [PMID: 11557454]
[79]
Hernandez, S.; López-Ribot, J.L.; Najvar, L.K.; McCarthy, D.I.; Bocanegra, R.; Graybill, J.R. Caspofungin resistance in Candida albicans: correlating clinical outcome with laboratory susceptibility testing of three isogenic isolates serially obtained from a patient with progressive Candida esophagitis. Antimicrob. Agents Chemother., 2004, 48(4), 1382-1383.
[http://dx.doi.org/10.1128/AAC.48.4.1382-1383.2004] [PMID: 15047549]
[80]
Wiederhold, N.P.; Grabinski, J.L.; Garcia-Effron, G.; Perlin, D.S.; Lee, S.A. Pyrosequencing to detect mutations in FKS1 that confer reduced echinocandin susceptibility in Candida albicans. Antimicrob. Agents Chemother., 2008, 52(11), 4145-4148.
[http://dx.doi.org/10.1128/AAC.00959-08] [PMID: 18794385]
[81]
Cowen, L.E.; Sanglard, D.; Howard, S.J.; Rogers, P.D.; Perlin, D.S. Mechanisms of antifungal drug resistance. Cold Spring Harb. Perspect. Med., 2014, 5(7)a019752
[http://dx.doi.org/10.1101/cshperspect.a019752] [PMID: 25384768]
[82]
White, T.C.; Marr, K.A.; Bowden, R.A. Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin. Microbiol. Rev., 1998, 11(2), 382-402.
[http://dx.doi.org/10.1128/CMR.11.2.382] [PMID: 9564569]
[83]
Ford, C.B.; Funt, J.M.; Abbey, D.; Issi, L.; Guiducci, C.; Martinez, D.A.; Delorey, T.; Li, B.Y.; White, T.C.; Cuomo, C.; Rao, R.P.; Berman, J.; Thompson, D.A.; Regev, A. The evolution of drug resistance in clinical isolates of Candida albicans. eLife, 2015, 4e00662
[http://dx.doi.org/10.7554/eLife.00662] [PMID: 25646566]
[84]
Revie, N.M.; Iyer, K.R.; Robbins, N.; Cowen, L.E. Antifungal drug resistance: evolution, mechanisms and impact. Curr. Opin. Microbiol., 2018, 45, 70-76.
[http://dx.doi.org/10.1016/j.mib.2018.02.005] [PMID: 29547801]
[85]
Ksiezopolska, E.; Gabaldón, T. Evolutionary emergence of drug resistance in Candida opportunistic pathogens. Genes (Basel), 2018, 9(9), E461.
[http://dx.doi.org/10.3390/genes9090461] [PMID: 30235884]
[86]
Whaley, S.G.; Berkow, E.L.; Rybak, J.M.; Nishimoto, A.T.; Barker, K.S.; Rogers, P.D. Azole antifungal resistance in Candida albicans and emerging non-albicans Candida species. Front. Microbiol., 2017, 7, 2173.
[http://dx.doi.org/10.3389/fmicb.2016.02173] [PMID: 28127295]
[87]
Patil, A.; Majumdar, S. Echinocandins in antifungal pharmacotherapy. J. Pharm. Pharmacol., 2017, 69(12), 1635-1660.
[http://dx.doi.org/10.1111/jphp.12780] [PMID: 28744860]
[88]
Perlin, D.S. Echinocandin resistance in candida. Clin. Infect. Dis., 2015, 61(Suppl. 6), S612-S617.
[http://dx.doi.org/10.1093/cid/civ791] [PMID: 26567278]
[89]
Dunkel, N.; Liu, T.T.; Barker, K.S.; Homayouni, R.; Morschhäuser, J.; Rogers, P.D. A gain-of-function mutation in the transcription factor Upc2p causes upregulation of ergosterol biosynthesis genes and increased fluconazole resistance in a clinical Candida albicans isolate. Eukaryot. Cell, 2008, 7(7), 1180-1190.
[http://dx.doi.org/10.1128/EC.00103-08] [PMID: 18487346]
[90]
Lamb, D.C.; Kelly, D.E.; White, T.C.; Kelly, S.L. The R467K amino acid substitution in Candida albicans sterol 14 α-demethylase causes drug resistance through reduced affinity. Antimicrob. Agents Chemother., 2000, 44(1), 63-67.
[http://dx.doi.org/10.1128/AAC.44.1.63-67.2000] [PMID: 10602724]
[91]
Morio, F.; Loge, C.; Besse, B.; Hennequin, C.; Le Pape, P. Screening for amino acid substitutions in the Candida albicans Erg11 protein of azole-susceptible and azole-resistant clinical isolates: new substitutions and a review of the literature. Diagn. Microbiol. Infect. Dis., 2010, 66(4), 373-384.
[http://dx.doi.org/10.1016/j.diagmicrobio.2009.11.006] [PMID: 20226328]
[92]
Perlin, D.S. Echinocandin resistance in Candida. Clin. Infect. Dis., 2015, 61(suppl_6), S612-S617.
[http://dx.doi.org/10.1093/cid/civ791]
[93]
Asner, S.A.; Giulieri, S.; Diezi, M.; Marchetti, O.; Sanglard, D. Acquired multidrug antifungal resistance in Candida lusitaniae during therapy. Antimicrob. Agents Chemother., 2015, 59(12), 7715-7722.
[http://dx.doi.org/10.1128/AAC.02204-15] [PMID: 26438490]
[94]
Desnos-Ollivier, M.; Moquet, O.; Chouaki, T.; Guérin, A-M.; Dromer, F. Development of echinocandin resistance in Clavispora lusitaniae during caspofungin treatment. J. Clin. Microbiol., 2011, 49(6), 2304-2306.
[http://dx.doi.org/10.1128/JCM.00325-11] [PMID: 21490186]
[95]
Desnos-Ollivier, M.; Bretagne, S.; Raoux, D.; Hoinard, D.; Dromer, F.; Dannaoui, E. Mutations in the fks1 gene in Candida albicans, C. tropicalis, and C. krusei correlate with elevated caspofungin MICs uncovered in AM3 medium using the method of the european committee on antibiotic susceptibility testing. Antimicrob. Agents Chemother., 2008, 52(9), 3092-3098.
[http://dx.doi.org/10.1128/AAC.00088-08] [PMID: 18591282]
[96]
Garcia-Effron, G.; Katiyar, S.K.; Park, S.; Edlind, T.D.; Perlin, D.S. A naturally occurring proline-to-alanine amino acid change in Fks1p in Candida parapsilosis, Candida orthopsilosis, and Candida metapsilosis accounts for reduced echinocandin susceptibility. Antimicrob. Agents Chemother., 2008, 52(7), 2305-2312.
[http://dx.doi.org/10.1128/AAC.00262-08] [PMID: 18443110]
[97]
Chau, A.S.; Gurnani, M.; Hawkinson, R.; Laverdiere, M.; Cacciapuoti, A.; McNicholas, P.M. Inactivation of sterol Δ5,6-desaturase attenuates virulence in Candida albicans. Antimicrob. Agents Chemother., 2005, 49(9), 3646-3651.
[http://dx.doi.org/10.1128/AAC.49.9.3646-3651.2005] [PMID: 16127034]
[98]
Eddouzi, J.; Parker, J.E.; Vale-Silva, L.A.; Coste, A.; Ischer, F.; Kelly, S.; Manai, M.; Sanglard, D. Molecular mechanisms of drug resistance in clinical Candida species isolated from Tunisian hospitals. Antimicrob. Agents Chemother., 2013, 57(7), 3182-3193.
[http://dx.doi.org/10.1128/AAC.00555-13] [PMID: 23629718]
[99]
Martel, C.M.; Parker, J.E.; Bader, O.; Weig, M.; Gross, U.; Warrilow, A.G.; Rolley, N.; Kelly, D.E.; Kelly, S.L. Identification and characterization of four azole-resistant erg3 mutants of Candida albicans. Antimicrob. Agents Chemother., 2010, 54(11), 4527-4533.
[http://dx.doi.org/10.1128/AAC.00348-10] [PMID: 20733039]
[100]
Morio, F.; Pagniez, F.; Lacroix, C.; Miegeville, M.; Le Pape, P. Amino acid substitutions in the Candida albicans sterol Δ5,6-desaturase (Erg3p) confer azole resistance: characterization of two novel mutants with impaired virulence. J. Antimicrob. Chemother., 2012, 67(9), 2131-2138.
[http://dx.doi.org/10.1093/jac/dks186] [PMID: 22678731]
[101]
Kelly, S.L.; Lamb, D.C.; Corran, A.J.; Baldwin, B.C.; Kelly, D.E. Mode of action and resistance to azole antifungals associated with the formation of 14 α-methylergosta-8,24(28)-dien-3 β,6 α-diol. Biochem. Biophys. Res. Commun., 1995, 207(3), 910-915.
[http://dx.doi.org/10.1006/bbrc.1995.1272] [PMID: 7864896]
[102]
Jensen-Pergakes, K.L.; Kennedy, M.A.; Lees, N.D.; Barbuch, R.; Koegel, C.; Bard, M. Sequencing, disruption, and characterization of the Candida albicans sterol methyltransferase (ERG6) gene: drug susceptibility studies in erg6 mutants. Antimicrob. Agents Chemother., 1998, 42(5), 1160-1167.
[http://dx.doi.org/10.1128/AAC.42.5.1160] [PMID: 9593144]
[103]
Jia, N.; Arthington-Skaggs, B.; Lee, W.; Pierson, C.A.; Lees, N.D.; Eckstein, J.; Barbuch, R.; Bard, M. Candida albicans sterol C-14 reductase, encoded by the ERG24 gene, as a potential antifungal target site. Antimicrob. Agents Chemother., 2002, 46(4), 947-957.
[http://dx.doi.org/10.1128/AAC.46.4.947-957.2002] [PMID: 11897574]
[104]
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]
[105]
Gaur, M.; Puri, N.; Manoharlal, R.; Rai, V.; Mukhopadhayay, G.; Choudhury, D.; Prasad, R. MFS transportome of the human pathogenic yeast Candida albicans. BMC Genomics, 2008, 9(1), 579.
[http://dx.doi.org/10.1186/1471-2164-9-579] [PMID: 19055746]
[106]
Gbelska, Y.; Krijger, J-J.; Breunig, K.D. Evolution of gene families: the multidrug resistance transporter genes in five related yeast species. FEMS Yeast Res., 2006, 6(3), 345-355.
[http://dx.doi.org/10.1111/j.1567-1364.2006.00058.x] [PMID: 16630275]
[107]
Sanglard, D. Emerging threats in antifungal-resistant fungal pathogens. Front. Med. (Lausanne), 2016, 3, 11.
[http://dx.doi.org/10.3389/fmed.2016.00011] [PMID: 27014694]
[108]
Sanglard, D.; Coste, A.; Ferrari, S. Antifungal drug resistance mechanisms in fungal pathogens from the perspective of transcriptional gene regulation. FEMS Yeast Res., 2009, 9(7), 1029-1050.
[http://dx.doi.org/10.1111/j.1567-1364.2009.00578.x] [PMID: 19799636]
[109]
Ramage, G.; Saville, S.P.; Thomas, D.P.; López-Ribot, J.L. Candida biofilms: an update. Eukaryot. Cell, 2005, 4(4), 633-638.
[http://dx.doi.org/10.1128/EC.4.4.633-638.2005] [PMID: 15821123]
[110]
Desai, J.V.; Mitchell, A.P.; Andes, D.R. Fungal biofilms, drug resistance, and recurrent infection. Cold Spring Harb. Perspect. Med., 2014, 4(10)a019729
[http://dx.doi.org/10.1101/cshperspect.a019729] [PMID: 25274758]
[111]
Mitchell, K.F.; Zarnowski, R.; Sanchez, H.; Edward, J.A.; Reinicke, E.L.; Nett, J.E.; Mitchell, A.P.; Andes, D.R. Community participation in biofilm matrix assembly and function. Proc. Natl. Acad. Sci. USA, 2015, 112(13), 4092-4097.
[http://dx.doi.org/10.1073/pnas.1421437112] [PMID: 25770218]
[112]
Vediyappan, G.; Rossignol, T.; d’Enfert, C. Interaction of Candida albicans biofilms with antifungals: transcriptional response and binding of antifungals to beta-glucans. Antimicrob. Agents Chemother., 2010, 54(5), 2096-2111.
[http://dx.doi.org/10.1128/AAC.01638-09] [PMID: 20194705]
[113]
Clatworthy, A.E.; Pierson, E.; Hung, D.T. Targeting virulence: a new paradigm for antimicrobial therapy. Nat. Chem. Biol., 2007, 3(9), 541-548.
[http://dx.doi.org/10.1038/nchembio.2007.24] [PMID: 17710100]
[114]
Gauwerky, K.; Borelli, C.; Korting, H.C. Targeting virulence: a new paradigm for antifungals. Drug Discov. Today, 2009, 14(3-4), 214-222.
[http://dx.doi.org/10.1016/j.drudis.2008.11.013] [PMID: 19152839]
[115]
Casadevall, A.; Pirofski, L.A. The damage-response framework of microbial pathogenesis. Nat. Rev. Microbiol., 2003, 1(1), 17-24.
[http://dx.doi.org/10.1038/nrmicro732] [PMID: 15040176]
[116]
van de Veerdonk, F.L.; Netea, M.G.; Joosten, L.A.; van der Meer, J.W.; Kullberg, B.J. Novel strategies for the prevention and treatment of Candida infections: the potential of immunotherapy. FEMS Microbiol. Rev., 2010, 34(6), 1063-1075.
[http://dx.doi.org/10.1111/j.1574-6976.2010.00232.x] [PMID: 20528948]
[117]
Huang, W.; Na, L.; Fidel, P.L.; Schwarzenberger, P. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J. Infect. Dis., 2004, 190(3), 624-631.
[http://dx.doi.org/10.1086/422329] [PMID: 15243941]
[118]
Conti, H.R.; Shen, F.; Nayyar, N.; Stocum, E.; Sun, J.N.; Lindemann, M.J.; Ho, A.W.; Hai, J.H.; Yu, J.J.; Jung, J.W.; Filler, S.G.; Masso-Welch, P.; Edgerton, M.; Gaffen, S.L. Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J. Exp. Med., 2009, 206(2), 299-311.
[http://dx.doi.org/10.1084/jem.20081463] [PMID: 19204111]
[119]
Torosantucci, A.; Bromuro, C.; Chiani, P.; De Bernardis, F.; Berti, F.; Galli, C.; Norelli, F.; Bellucci, C.; Polonelli, L.; Costantino, P.; Rappuoli, R.; Cassone, A. A novel glyco-conjugate vaccine against fungal pathogens. J. Exp. Med., 2005, 202(5), 597-606.
[http://dx.doi.org/10.1084/jem.20050749] [PMID: 16147975]
[120]
Han, Y.; Ulrich, M.A.; Cutler, J.E. Candida albicans mannan extract-protein conjugates induce a protective immune response against experimental candidiasis. J. Infect. Dis., 1999, 179(6), 1477-1484.
[http://dx.doi.org/10.1086/314779] [PMID: 10228070]
[121]
Bistoni, F.; Vecchiarelli, A.; Cenci, E.; Puccetti, P.; Marconi, P.; Cassone, A. Evidence for macrophage-mediated protection against lethal Candida albicans infection. Infect. Immun., 1986, 51(2), 668-674.
[PMID: 3943907]
[122]
Pietrella, D.; Rachini, A.; Torosantucci, A.; Chiani, P.; Brown, A.J.; Bistoni, F.; Costantino, P.; Mosci, P.; d’Enfert, C.; Rappuoli, R.; Cassone, A.; Vecchiarelli, A. A β-glucan-conjugate vaccine and anti-β-glucan antibodies are effective against murine vaginal candidiasis as assessed by a novel in vivo imaging technique. Vaccine, 2010, 28(7), 1717-1725.
[http://dx.doi.org/10.1016/j.vaccine.2009.12.021] [PMID: 20038431]
[123]
Graybill, J.R.; Bocanegra, R.; Luther, M. Antifungal combination therapy with granulocyte colony-stimulating factor and fluconazole in experimental disseminated candidiasis. Eur. J. Clin. Microbiol. Infect. Dis., 1995, 14(8), 700-703.
[http://dx.doi.org/10.1007/BF01690878] [PMID: 8565989]
[124]
Kullberg, B-J.; van ’t Wout, J.W.; Hoogstraten, C.; van Furth, R. Recombinant interferon-γ enhances resistance to acute disseminated Candida albicans infection in mice. J. Infect. Dis., 1993, 168(2), 436-443.
[http://dx.doi.org/10.1093/infdis/168.2.436] [PMID: 8335982]
[125]
Dua, K.; Malyla, V.; Singhvi, G.; Wadhwa, R.; Krishna, R.V.; Shukla, S.D.; Shastri, M.D.; Chellappan, D.K.; Maurya, P.K.; Satija, S.; Mehta, M.; Gulati, M.; Hansbro, N.; Collet, T.; Awasthi, R.; Gupta, G.; Hsu, A.; Hansbro, P.M. Increasing complexity and interactions of oxidative stress in chronic respiratory diseases: An emerging need for novel drug delivery systems. Chem. Biol. Interact., 2019, 299, 168-178.
[http://dx.doi.org/10.1016/j.cbi.2018.12.009] [PMID: 30553721]
[126]
Dua, K.; Hansbro, N.G.; Foster, P.S.; Hansbro, P.M. MicroRNAs as therapeutics for future drug delivery systems in treatment of lung diseases. Drug Deliv. Transl. Res., 2017, 7(1), 168-178.
[http://dx.doi.org/10.1007/s13346-016-0343-6] [PMID: 27848224]
[127]
Dua, K.; Rapalli, V.K.; Shukla, S.D.; Singhvi, G.; Shastri, M.D.; Chellappan, D.K.; Satija, S.; Mehta, M.; Gulati, M.; Pinto, T.J.A.; Gupta, G.; Hansbro, P.M. Multi-drug resistant Mycobacterium tuberculosis & oxidative stress complexity: Emerging need for novel drug delivery approaches. Biomed. Pharmacother., 2018, 107, 1218-1229.
[http://dx.doi.org/10.1016/j.biopha.2018.08.101] [PMID: 30257336]
[128]
Pinto Reis, C.; Vasques Roque, L.; Baptista, M.; Rijo, P. Innovative formulation of nystatin particulate systems in toothpaste for candidiasis treatment. Pharm. Dev. Technol., 2016, 21(3), 282-287.
[http://dx.doi.org/10.3109/10837450.2014.999783] [PMID: 25567611]
[129]
Balamurugan, J.; Vijayalakshmi, P. Preparation and evaluation of floating extended release matrix tablet using combination of polymethacrylates and polyethylene oxide polymers. Int. J. Pharm. Pharm. Sci., 2014, 6(8), 584-592.
[130]
Salunkhe, S.S.; Bhatia, N.M.; Bhatia, M.S. Implications of formulation design on lipid-based nanostructured carrier system for drug delivery to brain. Drug Deliv., 2016, 23(4), 1306-1316.
[PMID: 25080227]
[131]
Fernández Campos, F.; Calpena Campmany, A.C.; Rodríguez Delgado, G.; López Serrano, O.; Clares Naveros, B. Development and characterization of a novel nystatin-loaded nanoemulsion for the buccal treatment of candidosis: ultrastructural effects and release studies. J. Pharm. Sci., 2012, 101(10), 3739-3752.
[http://dx.doi.org/10.1002/jps.23249] [PMID: 22777575]
[132]
El-Ridy, M.S.; Abdelbary, A.; Essam, T.; El-Salam, R.M.; Kassem, A.A. Niosomes as a potential drug delivery system for increasing the efficacy and safety of nystatin. Drug Dev. Ind. Pharm., 2011, 37(12), 1491-1508.
[http://dx.doi.org/10.3109/03639045.2011.587431] [PMID: 21707323]
[133]
Khan, M.A.; Syed, F.M.; Nasti, H.T.; Saima Dagger, K.; Haq, W.; Shehbaz, A.; Owais, M. Use of tuftsin bearing nystatin liposomes against an isolate of Candida albicans showing less in vivo susceptibility to amphotericin B. J. Drug Target., 2003, 11(2), 93-99.
[http://dx.doi.org/10.1080/1061186031000119093] [PMID: 12881195]
[134]
Desai, K.G.H.; Kumar, T.M. Preparation and evaluation of a novel buccal adhesive system. AAPS PharmSciTech, 2004, 5(3)e35
[http://dx.doi.org/10.1208/pt050335] [PMID: 15760069]
[135]
Al-Quadeib, B.T.; Radwan, M.A.; Siller, L.; Horrocks, B.; Wright, M.C. Stealth Amphotericin B nanoparticles for oral drug delivery: In vitro optimization. Saudi Pharm. J., 2015, 23(3), 290-302.
[http://dx.doi.org/10.1016/j.jsps.2014.11.004] [PMID: 26106277]
[136]
Hussain, A.; Singh, V.K.; Singh, O.P.; Shafaat, K.; Kumar, S.; Ahmad, F.J. Formulation and optimization of nanoemulsion using antifungal lipid and surfactant for accentuated topical delivery of Amphotericin B. Drug Deliv., 2016, 23(8), 3101-3110.
[http://dx.doi.org/10.3109/10717544.2016.1153747] [PMID: 27854145]
[137]
Patel, P.A.; Patravale, V.B. AmbiOnp: solid lipid nanoparticles of amphotericin B for oral administration. J. Biomed. Nanotechnol., 2011, 7(5), 632-639.
[http://dx.doi.org/10.1166/jbn.2011.1332] [PMID: 22195480]
[138]
Moen, M.D.; Lyseng-Williamson, K.A.; Scott, L.J. Liposomal amphotericin B: a review of its use as empirical therapy in febrile neutropenia and in the treatment of invasive fungal infections. Drugs, 2009, 69(3), 361-392.
[http://dx.doi.org/10.2165/00003495-200969030-00010] [PMID: 19275278]
[139]
Patel, S.K.; Shah, D.R.; Tiwari, S. Bioadhesive films containing fluconazole for mucocutaneous candidiasis. Indian J. Pharm. Sci., 2015, 77(1), 55-61.
[http://dx.doi.org/10.4103/0250-474X.151601] [PMID: 25767319]
[140]
Kumar, J.R.K.; Muralidharan, S.; Dhanaraj, S.A. Development and in vitro evalution of guar gum based fluconazole in situ gel for oral thrush. J. Pharm. Sci. Rev. Res., 2012, 4(12), 2009.
[141]
Jaiswal, P.; Gidwani, B.; Vyas, A. Nanostructured lipid carriers and their current application in targeted drug delivery. Artif. Cells Nanomed. Biotechnol., 2016, 44(1), 27-40.
[http://dx.doi.org/10.3109/21691401.2014.909822] [PMID: 24813223]
[142]
Bhalaria, M.; Naik, S.; Misra, A. Ethosomes: a novel delivery system for antifungal drugs in the treatment of topical fungal diseases. Indian J. Exp. Biol., 2009, 47(5), 368-375.
[143]
Maiti, S.; Dey, P.; Kaity, S.; Ray, S.; Maji, S.; Sa, B. Investigation on processing variables for the preparation of fluconazole-loaded ethyl cellulose microspheres by modified multiple emulsion technique. AAPS PharmSciTech, 2009, 10(3), 703-715.
[http://dx.doi.org/10.1208/s12249-009-9257-7] [PMID: 19479386]
[144]
Shahzadi, I.; Masood, M.I.; Chowdhary, F.; Anjum, A.A.; Nawaz, M.A.; Maqsood, I.; Zaman, M.Q. Microemulsion formulation for topical delivery of miconazole nitrate. Int. J. Pharm. Sci. Rev. Res., 2014, 24(2), 30-36.
[145]
Lambert, E.; Janjic, J.M. Multiple linear regression applied to predicting droplet size of complex perfluorocarbon nanoemulsions for biomedical applications. Pharm. Dev. Technol., 2019, 24(6), 700-710.
[http://dx.doi.org/10.1080/10837450.2019.1578372] [PMID: 30724654]
[146]
Chauhan, P.; Tyagi, B.K. Herbal novel drug delivery systems and transfersomes. J. Drug Deliv. Ther., 2018, 8(3), 162-168.
[http://dx.doi.org/10.22270/jddt.v8i3.1772]
[147]
An efficacy and safety study of APX001 in non-neutropenic patients with candidemia. Available from: clinicaltrials.gov/ct2/show/NCT03604705 (Accessed on February 15, 2019).
[148]
A Study to Evaluate the Efficacy and Safety of Oral VT-1161 in Patients With Acute Vaginal candidiasis (Yeast Infection). Available from: clinicaltrials.gov/ct2/show/record/NCT01891331 (Accessed February 15, 2019).
[149]
Oral SCY-078 vs. standard-of-care following IV echinocandin in the treatment of invasive candidiasis. Available from: clinicaltrials.gov/ct2/show/NCT02244606?term=NCT02244606&rank=1 (Accessed on February 16, 2019).
[150]
Open-label study to evaluate the efficacy and safety of scy-078 in patients with candidiasis caused by Candida auris (CARES). Available from: clinicaltrials.gov/ct2/show/NCT03363841 [Accessed on February 16, 2019].
[151]
CD101 compared to caspofungin followed by oral step down in subjects with candidemia and/or invasive candidiasis-bridging extension (STRIVE). Available from: clinicaltrials.gov/ct2/results?cond=&term=NCT02734862 (Accessed on February 16, 2019).
[152]
A study to evaluate oral vt-1161 in the treatment of patients with recurrent vaginal candidiasis (yeast infection). Available from: clinicaltrials.gov/ct2/show/NCT02267382 (Accessed on February 16, 2019).
[153]
Safety and efficacy of oral encochleated amphotericin b (CAMB/MAT2203) in the treatment of vulvovaginal candidiasis (VVC). Available from: clinicaltrials.gov/ct2/show/NCT02971007 (Accessed on February 16, 2019)
[154]
CAMB/MAT2203 in patients with mucocutaneous candidiasis (CAMB). Available from: clinicaltrials.gov/ct2/show/NCT02629419 (Accessed on February 16, 2019)
[155]
Efficacy and safety of oral encochleated amphotericin b (CAMB) in the treatment of fluconazole-resistant vulvovaginal candidiasis. Available from: clinicaltrials.gov/ct2/show/NCT03167957 (Accessed on February 16, 2019)
[156]
CelAgace™ orarinse solution for treatment of candidiasis. Available from: clinicaltrials.gov/ct2/show/study/NCT03250923 (Accessed on February 16, 2019).
[157]
A comparative clinical trial to evaluate the safety and clinical equivalence of clotrimazole troche/lozenges USP, 10mg (unique pharmaceutical laboratories, India) with clotrimazole troche 10mg (roxane laboratories inc., usa) in subjects with oropharyngeal candidiasis. (TPC). Available from: clinicaltrials.gov/ct2/show/NCT02635438 (Accessed on February 16, 2019).
[158]
Patients with vulvovaginal candidiasis (EPP-AFG-VVC). Available from: clinicaltrials.gov/ct2/show/NCT03024502 (Accessed February 16, 2019).
[159]
The safety and efficacy of intravenous anidulafungin as a treatment for azole-refractory mucosal candidiasis (FRMC). Available from: clinicaltrials.gov/ct2/show/NCT00041704 (Accessed on February 16, 2019).
[160]
Study to compare the efficacy and safety of micafungin versus conventional amphotericin b for the treatment of neonatal candidiasis (MAGIC-2). Available from: clinicaltrials.gov/ct2/show/NCT00815516 (Accessed February 16, 2019).
[161]
Gentian violet vs. Available from: clinicaltrials.gov/ct2/show/NCT01427738 (Accessed on February 16, 2019).


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 19
ISSUE: 28
Year: 2019
Page: [2593 - 2609]
Pages: 17
DOI: 10.2174/1568026619666191026105308
Price: $65

Article Metrics

PDF: 23
HTML: 5