Antifungal therapy of Candida biofilms: Past, present and future

Biofilm - Tập 5 - Trang 100126 - 2023
Olabayo H. Ajetunmobi1, Hamid Badali1, Jesus A. Romo1, Gordon Ramage2, Jose L. Lopez-Ribot1
1Department of Molecular Microbiology & Immunology, South Texas Center for Emerging Infectious Diseases, The University of Texas at San Antonio, San Antonio, TX, USA
2Glasgow Biofilm Research Network, School of Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, G12 8TA, UK

Tài liệu tham khảo

Brown, 2012, Hidden killers: human fungal infections, Sci Transl Med, 4, 165rv13, 10.1126/scitranslmed.3004404 Thomas-Ruddel, 2022, Risk factors for invasive Candida infection in critically ill patients: a systematic review and meta-analysis, Chest, 161, 345, 10.1016/j.chest.2021.08.081 Chakrabarti, 2020, Multidrug-resistant Candida auris: an epidemiological review, Expert Rev Anti Infect Ther, 18, 551, 10.1080/14787210.2020.1750368 Kean, 2020, Candida auris: a decade of understanding of an enigmatic pathogenic yeast, J Fungi (Basel)., 6 Silva, 2012, Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance, FEMS Microbiol Rev, 36, 288, 10.1111/j.1574-6976.2011.00278.x Koehler, 2019, Morbidity and mortality of candidaemia in Europe: an epidemiologic meta-analysis, Clin Microbiol Infect, 25, 1200, 10.1016/j.cmi.2019.04.024 Tsay, 2020, Burden of candidemia in the United States, 2017, Clin Infect Dis, 71, e449 Cuellar-Cruz, 2012, Candida species: new insights into biofilm formation, Future Microbiol, 7, 755, 10.2217/fmb.12.48 Wall, 2019, Candida albicans biofilm growth and dispersal: contributions to pathogenesis, Curr Opin Microbiol, 52, 1, 10.1016/j.mib.2019.04.001 Ramage, 2005, Candida biofilms: an update, Eukaryot Cell, 4, 633, 10.1128/EC.4.4.633-638.2005 Chandra, 2001, Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance, J Bacteriol, 183, 5385, 10.1128/JB.183.18.5385-5394.2001 Gulati, 2016, Candida albicans biofilms: development, regulation, and molecular mechanisms, Microb Infect, 18, 310, 10.1016/j.micinf.2016.01.002 Sherry, 2017, Biofilm-forming capability of highly virulent, multidrug-resistant Candida auris, Emerg Infect Dis, 23, 328, 10.3201/eid2302.161320 Uppuluri, 2018, Candida albicans dispersed cells are developmentally distinct from biofilm and planktonic cells, mBio, 9, 10.1128/mBio.01338-18 Uppuluri, 2010, Dispersion as an important step in the Candida albicans biofilm developmental cycle, PLoS Pathog, 6, 10.1371/journal.ppat.1000828 Nobile, 2006, Genetics and genomics of Candida albicans biofilm formation, Cell Microbiol, 8, 1382, 10.1111/j.1462-5822.2006.00761.x Nobile, 2012, A recently evolved transcriptional network controls biofilm development in Candida albicans, Cell, 148, 126, 10.1016/j.cell.2011.10.048 Nobile, 2006, Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo, PLoS Pathog, 2, e63, 10.1371/journal.ppat.0020063 Fox, 2015, An expanded regulatory network temporally controls Candida albicans biofilm formation, Mol Microbiol, 96, 1226, 10.1111/mmi.13002 Ramage, 2002, Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule, Appl Environ Microbiol, 68, 5459, 10.1128/AEM.68.11.5459-5463.2002 Pierce, 2013, Antifungal therapy with an emphasis on biofilms, Curr Opin Pharmacol, 13, 726, 10.1016/j.coph.2013.08.008 Ramage, 2001, Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms, Antimicrob Agents Chemother, 45, 2475, 10.1128/AAC.45.9.2475-2479.2001 Odds, 2003, Antifungal agents: mechanisms of action, Trends Microbiol, 11, 272, 10.1016/S0966-842X(03)00117-3 Ostrosky-Zeichner, 2010, An insight into the antifungal pipeline: selected new molecules and beyond, Nat Rev Drug Discov, 9, 719, 10.1038/nrd3074 Wall, 2020, Current antimycotics, new prospects, and future approaches to antifungal therapy, Antibiotics (Basel), 9 Kaur, 2023, Antifungal drug-resistance mechanisms in Candida biofilms, Curr Opin Microbiol, 71, 10.1016/j.mib.2022.102237 Ramage, 2012, Fungal biofilm resistance, Internet J Microbiol, 2012 Taff, 2013, Mechanisms of Candida biofilm drug resistance, Future Microbiol, 8, 1325, 10.2217/fmb.13.101 Ramage, 2006, Candida biofilms on implanted biomaterials: a clinically significant problem, FEMS Yeast Res, 6, 979, 10.1111/j.1567-1364.2006.00117.x Denning, 2002, Echinocandins: a new class of antifungal, J Antimicrob Chemother, 49, 889, 10.1093/jac/dkf045 Johnson, 2003, Caspofungin: first approved agent in a new class of antifungals, Expet Opin Pharmacother, 4, 807, 10.1517/14656566.4.5.807 Anderson, 2014, Amphotericin forms an extramembranous and fungicidal sterol sponge, Nat Chem Biol, 10, 400, 10.1038/nchembio.1496 Gray, 2012, Amphotericin primarily kills yeast by simply binding ergosterol, Proc Natl Acad Sci U S A, 109, 2234, 10.1073/pnas.1117280109 Kuhn, 2004, Candida biofilms: antifungal resistance and emerging therapeutic options, Curr Opin Invest Drugs, 5, 186 Perfect, 2017, The antifungal pipeline: a reality check, Nat Rev Drug Discov, 16, 603, 10.1038/nrd.2017.46 Wiederhold, 2022, Pharmacodynamics, mechanisms of action and resistance, and spectrum of activity of new antifungal agents, J Fungi (Basel)., 8 Bachmann, 2002, In vitro activity of caspofungin against Candida albicans biofilms, Antimicrob Agents Chemother, 46, 3591, 10.1128/AAC.46.11.3591-3596.2002 Marcos-Zambrano, 2016, Biofilm production and antibiofilm activity of echinocandins and liposomal amphotericin B in echinocandin-resistant yeast species, Antimicrob Agents Chemother, 60, 3579, 10.1128/AAC.03065-15 Hoenigl, 2021, The antifungal pipeline: fosmanogepix, ibrexafungerp, olorofim, opelconazole, and rezafungin, Drugs, 81, 1703, 10.1007/s40265-021-01611-0 Wiederhold, 2018, The antifungal arsenal: alternative drugs and future targets, Int J Antimicrob Agents, 51, 333, 10.1016/j.ijantimicag.2017.09.002 Zhao, 2016, CD101: a novel long-acting echinocandin, Cell Microbiol, 18, 1308, 10.1111/cmi.12640 Chandra, 2018, CD101, a novel echinocandin, possesses potent antibiofilm activity against early and mature Candida albicans biofilms, Antimicrob Agents Chemother, 62, 10.1128/AAC.01750-17 Jallow, 2021, Ibrexafungerp: a first-in-class oral triterpenoid glucan synthase inhibitor, J Fungi (Basel)., 7 Marcos-Zambrano, 2017, The novel oral glucan synthase inhibitor SCY-078 shows in vitro activity against sessile and planktonic Candida spp, J Antimicrob Chemother, 72, 1969, 10.1093/jac/dkx010 Larkin, 2017, The emerging pathogen Candida auris: growth phenotype, virulence factors, activity of antifungals, and effect of SCY-078, a novel glucan synthesis inhibitor, on growth morphology and biofilm formation, Antimicrob Agents Chemother, 61, 10.1128/AAC.02396-16 Berkow, 2018, Activity of novel antifungal compound APX001A against a large collection of Candida auris, J Antimicrob Chemother, 73, 3060, 10.1093/jac/dky302 Watanabe, 2012, E1210, a new broad-spectrum antifungal, suppresses Candida albicans hyphal growth through inhibition of glycosylphosphatidylinositol biosynthesis, Antimicrob Agents Chemother, 56, 960, 10.1128/AAC.00731-11 Warrilow, 2016, The investigational drug VT-1129 is a highly potent inhibitor of cryptococcus species CYP51 but only weakly inhibits the human enzyme, Antimicrob Agents Chemother, 60, 4530, 10.1128/AAC.00349-16 Rennane, 2021, Estimating the cost of industry investment in drug research and development: a review of methods and results, Inquiry, 58 Van Dijck, 2018, Methodologies for in vitro and in vivo evaluation of efficacy of antifungal and antibiofilm agents and surface coatings against fungal biofilms, Microb Cell, 5, 300, 10.15698/mic2018.07.638 Pierce, 2015, A novel small molecule inhibitor of Candida albicans biofilm formation, filamentation and virulence with low potential for the development of resistance, NPJ Biofilms Microbiomes, 1, 10.1038/npjbiofilms.2015.12 Romo, 2017, Development of anti-virulence approaches for candidiasis via a novel series of small-molecule inhibitors of Candida albicans filamentation, mBio, 8, 10.1128/mBio.01991-17 Romo, 2018, In vitro characterization of a biaryl amide anti-virulence compound targeting Candida albicans filamentation and biofilm formation, Front Cell Infect Microbiol, 8, 227, 10.3389/fcimb.2018.00227 Romo, 2019, Global transcriptomic analysis of the Candida albicans response to treatment with a novel inhibitor of filamentation, mSphere, 4, 10.1128/mSphere.00620-19 LaFleur, 2011, Novel high-throughput screen against Candida albicans identifies antifungal potentiators and agents effective against biofilms, J Antimicrob Chemother, 66, 820, 10.1093/jac/dkq530 De Cremer, 2015, Artemisinins, new miconazole potentiators resulting in increased activity against Candida albicans biofilms, Antimicrob Agents Chemother, 59, 421, 10.1128/AAC.04229-14 Zhang, 2020, A marine microbiome antifungal targets urgent-threat drug-resistant fungi, Science, 370, 974, 10.1126/science.abd6919 Zhao, 2021, Turbinmicin inhibits Candida biofilm growth by disrupting fungal vesicle-mediated trafficking, J Clin Invest, 131, 10.1172/JCI145123 Cruz, 2013, Enterococcus faecalis inhibits hyphal morphogenesis and virulence of Candida albicans, Infect Immun, 81, 189, 10.1128/IAI.00914-12 Brown, 2019, Antifungal activity of the Enterococcus faecalis peptide EntV requires protease cleavage and disulfide bond formation, mBio, 10, 10.1128/mBio.01334-19 Graham, 2017, Enterococcus faecalis bacteriocin EntV inhibits hyphal morphogenesis, biofilm formation, and virulence of Candida albicans, Proc Natl Acad Sci U S A, 114, 4507, 10.1073/pnas.1620432114 Cruz, 2022, Structural and functional analysis of EntV reveals a 12 amino acid fragment protective against fungal infections, Nat Commun, 13, 6047, 10.1038/s41467-022-33613-1 Ashburn, 2004, Drug repositioning: identifying and developing new uses for existing drugs, Nat Rev Drug Discov, 3, 673, 10.1038/nrd1468 Oprea, 2012, Drug repurposing: far beyond new targets for old drugs, AAPS J, 14, 759, 10.1208/s12248-012-9390-1 Butts, 2012, Antifungal drug discovery: something old and something new, PLoS Pathog, 8, 10.1371/journal.ppat.1002870 Donlin, 2022, Repurposing and optimization of drugs for discovery of novel antifungals, Drug Discov Today, 27, 2008, 10.1016/j.drudis.2022.04.021 Izadi, 2022, Drug repurposing against Candida auris: a systematic review, Mycoses, 65, 784, 10.1111/myc.13477 Wall, 2020, Screening repurposing libraries for identification of drugs with novel antifungal activity, Antimicrob Agents Chemother, 64, 10.1128/AAC.00924-20 Wall, 2018, Screening a repurposing library for inhibitors of multidrug-resistant Candida auris identifies ebselen as a repositionable candidate for antifungal drug development, Antimicrob Agents Chemother, 62, 10.1128/AAC.01084-18 Abduljalil, 2022, Screening the Tocriscreen bioactive compound library in search for inhibitors of Candida biofilm formation, APMIS, 130, 568, 10.1111/apm.13260 Mamouei, 2018, Alexidine dihydrochloride has broad-spectrum activities against diverse fungal pathogens, mSphere, 3, 10.1128/mSphere.00539-18 Siles, 2013, High-throughput screening of a collection of known pharmacologically active small compounds for identification of Candida albicans biofilm inhibitors, Antimicrob Agents Chemother, 57, 3681, 10.1128/AAC.00680-13 Sutar, 2022, Niclosamide-loaded nanoparticles disrupt Candida biofilms and protect mice from mucosal candidiasis, PLoS Biol, 20, 10.1371/journal.pbio.3001762 Wiederhold, 2017, Repurposing auranofin as an antifungal: in vitro activity against a variety of medically important fungi, Virulence, 8, 138, 10.1080/21505594.2016.1196301 Li, 2021, Recent developments on using nanomaterials to combat Candida albicans, Front Chem, 9, 10.3389/fchem.2021.813973 Lara, 2015, Effect of silver nanoparticles on Candida albicans biofilms: an ultrastructural study, J Nanobiotechnol, 13, 91, 10.1186/s12951-015-0147-8 Monteiro, 2011, Silver colloidal nanoparticles: antifungal effect against adhered cells and biofilms of Candida albicans and Candida glabrata, Biofouling, 27, 711, 10.1080/08927014.2011.599101 Lara, 2020, Inhibition of Candida auris biofilm formation on medical and environmental surfaces by silver nanoparticles, ACS Appl Mater Interfaces, 12, 21183, 10.1021/acsami.9b20708 Vazquez-Munoz, 2020, Silver nanoantibiotics display strong antifungal activity against the emergent multidrug-resistant yeast Candida auris under both planktonic and biofilm growing conditions, Front Microbiol, 11, 1673, 10.3389/fmicb.2020.01673 Vazquez-Munoz, 2014, Ultrastructural analysis of Candida albicans when exposed to silver nanoparticles, PLoS One, 9, 10.1371/journal.pone.0108876 Vazquez-Munoz, 2020, Bismuth nanoparticles obtained by a facile synthesis method exhibit antimicrobial activity against Staphylococcus aureus and Candida albicans, BMC Biomed Eng, 2, 11, 10.1186/s42490-020-00044-2 Vazquez-Munoz, 2020, Fast, facile synthesis method for BAL-mediated PVP-bismuth nanoparticles, MethodsX, 7, 10.1016/j.mex.2020.100894 Vazquez-Munoz, 2020, Bismuth nanoantibiotics display anticandidal activity and disrupt the biofilm and cell morphology of the emergent pathogenic yeast Candida auris, Antibiotics (Basel), 9 Anwar, 2022 Lara, 2018, Synergistic antifungal effect of chitosan-stabilized selenium nanoparticles synthesized by pulsed laser ablation in liquids against Candida albicans biofilms, Int J Nanomed, 13, 2697, 10.2147/IJN.S151285 Lara, 2020, Inhibition of mixed biofilms of Candida albicans and methicillin-resistant Staphylococcus aureus by positively charged silver nanoparticles and functionalized silicone elastomers, Pathogens, 9, 10.3390/pathogens9100784 Martins, 2012, Effect of exogenous administration of Candida albicans autoregulatory alcohols in a murine model of hematogenously disseminated candidiasis, J Basic Microbiol, 52, 487, 10.1002/jobm.201100158 Martins, 2012, Addition of DNase improves the in vitro activity of antifungal drugs against Candida albicans biofilms, Mycoses, 55, 80, 10.1111/j.1439-0507.2011.02047.x Parolin, 2022, Vaginal lactobacillus impair Candida dimorphic switching and biofilm formation, Microorganisms, 10, 10.3390/microorganisms10102091 Pusateri, 2009, Sensitivity of Candida albicans biofilm cells grown on denture acrylic to antifungal proteins and chlorhexidine, Arch Oral Biol, 54, 588, 10.1016/j.archoralbio.2009.01.016 Bezerra, 2022, Combined antibiofilm activity of synthetic peptides and antifungal drugs against Candida spp, Future Microbiol, 17, 1133, 10.2217/fmb-2022-0053 Haring, 2022, Combination of six individual derivatives of the pom-1 antibiofilm peptide doubles their efficacy against invasive and multi-resistant clinical isolates of the pathogenic yeast Candida albicans, Pharmaceutics, 14, 10.3390/pharmaceutics14071332 Robbins, 2011, Hsp90 governs dispersion and drug resistance of fungal biofilms, PLoS Pathog, 7, 10.1371/journal.ppat.1002257 Amorim, 2023, Photodynamic inactivation of different Candida species and inhibition of biofilm formation induced by water-soluble porphyrins, Photodiagnosis Photodyn Ther, 42, 10.1016/j.pdpdt.2023.103343 Bujdakova, 2016, Management of Candida biofilms: state of knowledge and new options for prevention and eradication, Future Microbiol, 11, 235, 10.2217/fmb.15.139 Junqueira, 2012, Photodynamic inactivation of biofilms formed by Candida spp., Trichosporon mucoides, and Kodamaea ohmeri by cationic nanoemulsion of zinc 2,9,16,23-tetrakis(phenylthio)-29H, 31H-phthalocyanine (ZnPc), Laser Med Sci, 27, 1205, 10.1007/s10103-012-1050-2 Pereira, 2011, Susceptibility of Candida albicans, Staphylococcus aureus, and Streptococcus mutans biofilms to photodynamic inactivation: an in vitro study, Laser Med Sci, 26, 341, 10.1007/s10103-010-0852-3 Cateau, 2008, In vitro efficacies of caspofungin or micafungin catheter lock solutions on Candida albicans biofilm growth, J Antimicrob Chemother, 62, 153, 10.1093/jac/dkn160 Bouza, 2014, The role of antifungals against Candida biofilm in catheter-related candidemia, Antibiotics (Basel), 4, 1, 10.3390/antibiotics4010001 Agarwalla, 2021, Persistent inhibition of Candida albicans biofilm and hyphae growth on titanium by graphene nanocoating, Dent Mater, 37, 370, 10.1016/j.dental.2020.11.028 Araujo, 2017, Portrait of Candida species biofilm regulatory network genes, Trends Microbiol, 25, 62, 10.1016/j.tim.2016.09.004 Uppuluri, 2011, Effect of fluconazole, amphotericin B and caspofungin against Candida albicans biofilms under conditions of flow and on biofilm dispersion, Antimicrob Agents Chemother, 10.1128/AAC.01701-10