{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,11]],"date-time":"2026-10-11T06:21:05Z","timestamp":1791699665548,"version":"4.3.4"},"reference-count":126,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2021,4,21]],"date-time":"2021-04-21T00:00:00Z","timestamp":1618963200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003407","name":"Ministero dell\u2019Istruzione, dell\u2019Universit\u00e0 e della Ricerca","doi-asserted-by":"publisher","award":["FISR2019_04819 BacCAD"],"award-info":[{"award-number":["FISR2019_04819 BacCAD"]}],"id":[{"id":"10.13039\/501100003407","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Carbon dioxide (CO2), a vital molecule of the carbon cycle, is a critical component in living organisms\u2019 metabolism, performing functions that lead to the building of compounds fundamental for the life cycle. In all living organisms, the CO2\/bicarbonate (HCO3\u2212) balancing is governed by a superfamily of enzymes, known as carbonic anhydrases (CAs, EC 4.2.1.1). CAs catalyze the pivotal physiological reaction, consisting of the reversible hydration of the CO2 to HCO3\u2212 and protons. Opportunistic and pathogenic fungi can sense the environmental CO2 levels, which influence their virulence or environmental subsistence traits. The fungal CO2-sensing is directly stimulated by HCO3\u2212 produced in a CA-dependent manner, which directly activates adenylyl cyclase (AC) involved in the fungal spore formation. The interference with CA activity may impair fungal growth and virulence, making this approach interesting for designing antifungal drugs with a novel mechanism of action: the inhibition of CAs linked to the CO2\/HCO3\u2212\/pH chemosensing and signaling. This review reports that sulfonamides and their bioisosteres as well as inorganic anions can inhibit in vitro the \u03b2- and \u03b1-CAs from the fungi, suggesting how CAs may be considered as a novel \u201cpathogen protein\u201d target of many opportunistic, pathogenic fungi.<\/jats:p>","DOI":"10.3390\/ijms22094324","type":"journal-article","created":{"date-parts":[[2021,4,21]],"date-time":"2021-04-21T12:47:07Z","timestamp":1619009227000},"page":"4324","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":50,"title":["A Highlight on the Inhibition of Fungal Carbonic Anhydrases as Drug Targets for the Antifungal Armamentarium"],"prefix":"10.3390","volume":"22","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4262-0323","authenticated-orcid":false,"given":"Claudiu T.","family":"Supuran","sequence":"first","affiliation":[{"name":"Section of Pharmaceutical and Nutraceutical Sciences, Department of Neurofarba, University of Florence, Via U. Schiff 6, Sesto Fiorentino, 50019 Florence, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3314-2411","authenticated-orcid":false,"given":"Clemente","family":"Capasso","sequence":"additional","affiliation":[{"name":"Institute of Biosciences and Bioresources, CNR, Via Pietro Castellino 111, 80131 Napoli, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,4,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"18866","DOI":"10.1073\/pnas.0702737104","article-title":"Contributions to accelerating atmospheric CO2 growth from economic activity, carbon intensity, and efficiency of natural sinks","volume":"104","author":"Canadell","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1098\/rstb.2003.1428","article-title":"Tropical forests and the global carbon cycle: Impacts of atmospheric carbon dioxide, climate change and rate of deforestation","volume":"359","author":"Cramer","year":"2004","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1084","DOI":"10.1126\/science.1224304","article-title":"Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2","volume":"337","author":"Cheng","year":"2012","journal-title":"Science"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"R934","DOI":"10.1016\/j.cub.2005.10.064","article-title":"Fungal CO2 sensing: A breath of fresh air","volume":"15","author":"Mitchell","year":"2005","journal-title":"Curr. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1080\/21505594.2019.1688753","article-title":"Antivirulence and avirulence genes in human pathogenic fungi","volume":"10","author":"Hube","year":"2019","journal-title":"Virulence"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1055\/s-0040-1701215","article-title":"Invasive Candidiasis","volume":"41","year":"2020","journal-title":"Semin. Respir. Crit. Care Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1055\/s-0039-3401990","article-title":"Invasive Pulmonary Aspergillosis","volume":"41","author":"Ledoux","year":"2020","journal-title":"Semin. Respir. Crit. Care Med."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1055\/s-0039-3401992","article-title":"Mucormycosis","volume":"41","author":"Reid","year":"2020","journal-title":"Semin. Respir. Crit. Care Med."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1055\/s-0039-3400280","article-title":"Cryptococcosis","volume":"41","author":"Zavala","year":"2020","journal-title":"Semin. Respir. Crit. Care Med."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1002\/(SICI)1097-0061(199805)14:7<623::AID-YEA264>3.0.CO;2-D","article-title":"Bicarbonate-mediated social communication stimulates meiosis and sporulation of Saccharomyces cerevisiae","volume":"14","author":"Ohkuni","year":"1998","journal-title":"Yeast"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1854","DOI":"10.1083\/jcb.100.6.1854","article-title":"Outer plaque assembly and spore encapsulation are defective during sporulation of adenylate cyclase-deficient mutants of Saccharomyces cerevisiae","volume":"100","author":"Uno","year":"1985","journal-title":"J. Cell Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"42","DOI":"10.3389\/fphys.2014.00042","article-title":"Role of the bicarbonate-responsive soluble adenylyl cyclase in pH sensing and metabolic regulation","volume":"5","author":"Chang","year":"2014","journal-title":"Front. Physiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2021","DOI":"10.1016\/j.cub.2005.10.040","article-title":"Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence","volume":"15","author":"Klengel","year":"2005","journal-title":"Curr. Biol."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Chadwick, B.J., and Lin, X. (2020). On the History and Applications of Congenic Strains in Cryptococcus Research. Pathogens, 9.","DOI":"10.3390\/pathogens9090750"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"3206","DOI":"10.1101\/gad.11.23.3206","article-title":"Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP","volume":"11","author":"Alspaugh","year":"1997","journal-title":"Genes Dev."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1126\/science.289.5479.625","article-title":"Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor","volume":"289","author":"Chen","year":"2000","journal-title":"Science"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1172\/JCI112000","article-title":"Virulence of Cryptococcus neoformans. Regulation of capsule synthesis by carbon dioxide","volume":"76","author":"Granger","year":"1985","journal-title":"J. Clin. Investig."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2112","DOI":"10.3390\/s110202112","article-title":"Physiological sensing of carbon dioxide\/bicarbonate\/pH via cyclic nucleotide signaling","volume":"11","author":"Buck","year":"2011","journal-title":"Sensors"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1111\/j.1574-6976.2001.tb00582.x","article-title":"Conserved cAMP signaling cascades regulate fungal development and virulence","volume":"25","author":"Heitman","year":"2001","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2013","DOI":"10.1016\/j.cub.2005.09.047","article-title":"Carbonic anhydrase and CO2 sensing during Cryptococcus neoformans growth, differentiation, and virulence","volume":"15","author":"Bahn","year":"2005","journal-title":"Curr. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"313","DOI":"10.2174\/1389203720666190722152415","article-title":"Virulence Factors in Candida species","volume":"21","author":"Staniszewska","year":"2020","journal-title":"Curr. Protein Pept. Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"442","DOI":"10.3389\/fmicb.2019.00442","article-title":"Nutrient and Stress Sensing in Pathogenic Yeasts","volume":"10","author":"Rutherford","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1128\/microbiolspec.FUNK-0014-2016","article-title":"Fungi that Infect Humans","volume":"5","author":"Kohler","year":"2017","journal-title":"Microbiol. Spectr."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Guzel-Akdemir, O., Carradori, S., Grande, R., Demir-Yazici, K., Angeli, A., Supuran, C.T., and Akdemir, A. (2020). Development of Thiazolidinones as Fungal Carbonic Anhydrase Inhibitors. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21082960"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1904","DOI":"10.1002\/cmdc.201600180","article-title":"Discovery of New Potential Anti-Infective Compounds Based on Carbonic Anhydrase Inhibitors by Rational Target-Focused Repurposing Approaches","volume":"11","author":"Annunziato","year":"2016","journal-title":"ChemMedChem"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"689","DOI":"10.3109\/14756366.2015.1059333","article-title":"A magnificent enzyme superfamily: Carbonic anhydrases, their purification and characterization","volume":"31","author":"Capasso","year":"2016","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1115","DOI":"10.1016\/j.bmc.2016.01.037","article-title":"Sulfonamide inhibition studies of the beta-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae","volume":"24","author":"Vullo","year":"2016","journal-title":"Bioorg. Med. Chem."},{"key":"ref_28","first-page":"1","article-title":"Cloning, expression and purification of the complete domain of the eta-carbonic anhydrase from Plasmodium falciparum","volume":"31","author":"Supuran","year":"2016","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2359","DOI":"10.2174\/1568026616666160413135522","article-title":"An Overview of the Carbonic Anhydrases from Two Pathogens of the Oral Cavity: Streptococcus mutans and Porphyromonas gingivalis","volume":"16","author":"Capasso","year":"2016","journal-title":"Curr. Top. Med. Chem."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"325","DOI":"10.3109\/14756366.2014.910202","article-title":"An overview of the alpha-, beta- and gamma-carbonic anhydrases from Bacteria: Can bacterial carbonic anhydrases shed new light on evolution of bacteria?","volume":"30","author":"Capasso","year":"2015","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Supuran, C.T., and Capasso, C. (2017). An Overview of the Bacterial Carbonic Anhydrases. Metabolites, 7.","DOI":"10.3390\/metabo7040056"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2023","DOI":"10.1042\/BCJ20160115","article-title":"Structure and function of carbonic anhydrases","volume":"473","author":"Supuran","year":"2016","journal-title":"Biochem. J."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1007\/978-94-007-7359-2_15","article-title":"Carbonic anhydrase inhibitors drug design","volume":"75","author":"McKenna","year":"2014","journal-title":"Subcell Biochem."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1038\/nrd3554","article-title":"Interfering with pH regulation in tumours as a therapeutic strategy","volume":"10","author":"Neri","year":"2011","journal-title":"Nat. Rev. Drug Discov."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1038\/nrd2467","article-title":"Carbonic anhydrases: Novel therapeutic applications for inhibitors and activators","volume":"7","author":"Supuran","year":"2008","journal-title":"Nat. Rev. Drug. Discov."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"603","DOI":"10.2174\/138161208783877884","article-title":"Carbonic anhydrases\u2014An overview","volume":"14","author":"Supuran","year":"2008","journal-title":"Curr. Pharm. Des."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1080\/13543776.2018.1497161","article-title":"Biomedical applications of prokaryotic carbonic anhydrases","volume":"28","author":"Supuran","year":"2018","journal-title":"Expert Opin. Ther. Pat."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Supuran, C.T., and Capasso, C. (2017). Carbonic Anhydrase from Porphyromonas Gingivalis as a Drug Target. Pathogens, 6.","DOI":"10.3390\/pathogens6030030"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2130","DOI":"10.2174\/0929867321666141012174921","article-title":"An Overview of the Selectivity and Efficiency of the Bacterial Carbonic Anhydrase Inhibitors","volume":"22","author":"Capasso","year":"2015","journal-title":"Curr. Med. Chem."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1080\/14756366.2018.1559840","article-title":"Phaeodactylum tricornutum as a model organism for testing the membrane penetrability of sulphonamide carbonic anhydrase inhibitors","volume":"34","author":"Rogato","year":"2019","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1080\/14756366.2019.1571273","article-title":"Inhibition of alpha-, beta-, gamma-, delta-, zeta- and eta-class carbonic anhydrases from bacteria, fungi, algae, diatoms and protozoans with famotidine","volume":"34","author":"Angeli","year":"2019","journal-title":"J Enzym. Inhib. Med. Chem."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1194","DOI":"10.1080\/14756366.2018.1490733","article-title":"Inhibition of alpha-, beta-, gamma-, and delta-carbonic anhydrases from bacteria and diatoms with N\u2019-aryl-N-hydroxy-ureas","volume":"33","author":"Berrino","year":"2018","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.bioorg.2018.06.002","article-title":"The first activation studies of the eta-carbonic anhydrase from the malaria parasite Plasmodium falciparum with amines and amino acids","volume":"80","author":"Angeli","year":"2018","journal-title":"Bioorg. Chem."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1128\/EC.5.1.103-111.2006","article-title":"Cryptococcus neoformans senses CO2 through the carbonic anhydrase Can2 and the adenylyl cyclase Cac1","volume":"5","author":"Mogensen","year":"2006","journal-title":"Eukaryot Cell"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1207","DOI":"10.1016\/j.jmb.2008.11.037","article-title":"Structure and inhibition of the CO2-sensing carbonic anhydrase Can2 from the pathogenic fungus Cryptococcus neoformans","volume":"385","author":"Schlicker","year":"2009","journal-title":"J. Mol. Biol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1158","DOI":"10.1016\/j.bmc.2008.12.035","article-title":"Carbonic anhydrase inhibitors: Inhibition of the beta-class enzyme from the yeast Saccharomyces cerevisiae with sulfonamides and sulfamates","volume":"17","author":"Isik","year":"2009","journal-title":"Bioorg. Med. Chem."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"6327","DOI":"10.1016\/j.bmcl.2008.10.100","article-title":"Carbonic anhydrase inhibitors. Inhibition of the beta-class enzyme from the yeast Saccharomyces cerevisiae with anions","volume":"18","author":"Isik","year":"2008","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1042","DOI":"10.1016\/j.febslet.2011.03.001","article-title":"Structure of a dimeric fungal alpha-type carbonic anhydrase","volume":"585","author":"Borchert","year":"2011","journal-title":"FEBS Lett."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1759","DOI":"10.1111\/febs.12738","article-title":"Crystal structures of two tetrameric beta-carbonic anhydrases from the filamentous ascomycete Sordaria macrospora","volume":"281","author":"Lehneck","year":"2014","journal-title":"FEBS J."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"107700","DOI":"10.1016\/j.jsb.2021.107700","article-title":"Structural insights into novel mechanisms of inhibition of the major beta-carbonic anhydrase CafB from the pathogenic fungus Aspergillus fumigatus","volume":"213","author":"Kim","year":"2021","journal-title":"J. Struct. Biol."},{"key":"ref_51","first-page":"831","article-title":"Crystal Structure of beta-Carbonic Anhydrase CafA from the Fungal Pathogen Aspergillus fumigatus","volume":"43","author":"Kim","year":"2020","journal-title":"Mol. Cells"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"4993","DOI":"10.1074\/jbc.M510756200","article-title":"Structural mechanics of the pH-dependent activity of beta-carbonic anhydrase from Mycobacterium tuberculosis","volume":"281","author":"Covarrubias","year":"2006","journal-title":"J. Biol. Chem."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"3513","DOI":"10.1021\/jm300203r","article-title":"Molecular cloning, characterization, and inhibition studies of a beta-carbonic anhydrase from Malassezia globosa, a potential antidandruff target","volume":"55","author":"Hewitson","year":"2012","journal-title":"J. Med. Chem."},{"key":"ref_54","first-page":"e60175","article-title":"Infecting Mice with Malassezia spp. to Study the Fungus-Host Interaction","volume":"153","author":"Sparber","year":"2019","journal-title":"J. Vis. Exp."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"9540","DOI":"10.1021\/acs.jmedchem.0c00734","article-title":"Optimization of Acetazolamide-Based Scaffold as Potent Inhibitors of Vancomycin-Resistant Enterococcus","volume":"63","author":"Kaur","year":"2020","journal-title":"J. Med. Chem."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1093\/jac\/17.6.689","article-title":"Domagk and the development of the sulphonamides","volume":"17","author":"Otten","year":"1986","journal-title":"J. Antimicrob. Chem."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"379","DOI":"10.3109\/14756366.2013.787422","article-title":"Sulfa and trimethoprim-like drugs\u2014Antimetabolites acting as carbonic anhydrase, dihydropteroate synthase and dihydrofolate reductase inhibitors","volume":"29","author":"Capasso","year":"2014","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"490","DOI":"10.1038\/nsb0697-490","article-title":"Crystal structure of the anti-bacterial sulfonamide drug target dihydropteroate synthase","volume":"4","author":"Achari","year":"1997","journal-title":"Nat. Struct. Biol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1080\/14737175.2016.1193009","article-title":"Carbonic anhydrase inhibition and the management of neuropathic pain","volume":"16","author":"Supuran","year":"2016","journal-title":"Expert Rev. Neurother."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1517\/17425255.2016.1154534","article-title":"Drug interaction considerations in the therapeutic use of carbonic anhydrase inhibitors","volume":"12","author":"Supuran","year":"2016","journal-title":"Expert Opin. Drug Metab. Toxicol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1080\/17460441.2017.1253677","article-title":"Advances in structure-based drug discovery of carbonic anhydrase inhibitors","volume":"12","author":"Supuran","year":"2017","journal-title":"Expert Opin. Drug Discov."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"345","DOI":"10.3109\/14756366.2015.1122001","article-title":"How many carbonic anhydrase inhibition mechanisms exist?","volume":"31","author":"Supuran","year":"2016","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1016\/j.bmc.2014.12.009","article-title":"Sulfonamide inhibition studies of the eta-class carbonic anhydrase from the malaria pathogen Plasmodium falciparum","volume":"23","author":"Vullo","year":"2015","journal-title":"Bioorg. Med. Chem."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"3550","DOI":"10.1016\/j.bmcl.2015.06.079","article-title":"Sulfonamide inhibition studies of the gamma-carbonic anhydrase from the Antarctic bacterium Pseudoalteromonas haloplanktis","volume":"25","author":"Vullo","year":"2015","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1728","DOI":"10.1016\/j.bmc.2015.02.045","article-title":"Sulfonamide inhibition studies of the gamma-carbonic anhydrase from the Antarctic cyanobacterium Nostoc commune","volume":"23","author":"Vullo","year":"2015","journal-title":"Bioorg. Med. Chem."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"2291","DOI":"10.1016\/j.bmcl.2015.04.037","article-title":"Sulfonamide inhibition study of the beta-class carbonic anhydrase from the caries producing pathogen Streptococcus mutans","volume":"25","author":"Dedeoglu","year":"2015","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"592","DOI":"10.3109\/14756366.2014.957202","article-title":"Inhibition studies of quinazoline-sulfonamide derivatives against the gamma-CA (PgiCA) from the pathogenic bacterium, Porphyromonas gingivalis","volume":"30","author":"Alafeefy","year":"2015","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"52","DOI":"10.3109\/14756366.2013.877897","article-title":"Inhibition of human carbonic anhydrase isozymes I, II, IX and XII with a new series of sulfonamides incorporating aroylhydrazone-, [1,2,4]triazolo [3,4-b][1,3,4]thiadiazinyl- or 2-(cyanophenylmethylene)-1,3,4-thiadiazol-3(2H)-yl moieties","volume":"30","author":"Alafeefy","year":"2015","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1080\/14756366.2016.1187143","article-title":"A substituted sulfonamide and its Co (II), Cu (II), and Zn (II) complexes as potential antifungal agents","volume":"31","author":"Diaz","year":"2016","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1941","DOI":"10.1016\/j.bmcl.2016.01.072","article-title":"Comparison of the sulfonamide inhibition profiles of the alpha-, beta- and gamma-carbonic anhydrases from the pathogenic bacterium Vibrio cholerae","volume":"26","author":"Vullo","year":"2016","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"4184","DOI":"10.1016\/j.bmcl.2016.07.060","article-title":"Cloning, expression, purification and sulfonamide inhibition profile of the complete domain of the eta-carbonic anhydrase from Plasmodium falciparum","volume":"26","author":"Vullo","year":"2016","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"3043","DOI":"10.1016\/j.bmc.2016.05.016","article-title":"Synthesis of 4-(thiazol-2-ylamino)-benzenesulfonamides with carbonic anhydrase I, II and IX inhibitory activity and cytotoxic effects against breast cancer cell lines","volume":"24","author":"Amin","year":"2016","journal-title":"Bioorg. Med. Chem."},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Supuran, C.T. (2016). Legionella pneumophila Carbonic Anhydrases: Underexplored Antibacterial Drug Targets. Pathogens, 5.","DOI":"10.3390\/pathogens5020044"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"2939","DOI":"10.1016\/j.bmc.2014.04.006","article-title":"Sulfonamide inhibition studies of two beta-carbonic anhydrases from the bacterial pathogen Legionella pneumophila","volume":"22","author":"Nishimori","year":"2014","journal-title":"Bioorg. Med. Chem."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"6706","DOI":"10.1016\/j.bmcl.2013.10.037","article-title":"Anion inhibition studies of a beta-carbonic anhydrase from Clostridium perfringens","volume":"23","author":"Vullo","year":"2013","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"3300","DOI":"10.2174\/138161210793429814","article-title":"The beta-carbonic anhydrases from Mycobacterium tuberculosis as drug targets","volume":"16","author":"Nishimori","year":"2010","journal-title":"Curr. Pharm. Des."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"6649","DOI":"10.1016\/j.bmcl.2009.10.009","article-title":"Carbonic anhydrase inhibitors. Characterization and inhibition studies of the most active beta-carbonic anhydrase from Mycobacterium tuberculosis, Rv3588c","volume":"19","author":"Carta","year":"2009","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Supuran, C.T. (2017). Special Issue: Sulfonamides. Molecules, 22.","DOI":"10.3390\/molecules22101642"},{"key":"ref_79","unstructured":"Nguyen, K., and Ahlawat, R. (2020). Famotidine. StatPearls, StatPearls Publishing."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"423","DOI":"10.3389\/fonc.2018.00423","article-title":"Updates in the Clinical Development of Epacadostat and Other Indoleamine 2,3-Dioxygenase 1 Inhibitors (IDO1) for Human Cancers","volume":"8","author":"Komiya","year":"2018","journal-title":"Front. Oncol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"6794","DOI":"10.1016\/j.bmc.2015.10.006","article-title":"Poly(amidoamine) dendrimers show carbonic anhydrase inhibitory activity against alpha-, beta-, gamma- and eta-class enzymes","volume":"23","author":"Carta","year":"2015","journal-title":"Bioorg. Med. Chem."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1648","DOI":"10.1016\/j.bmc.2016.02.036","article-title":"Isatin analogs as novel inhibitors of Candida spp. beta-carbonic anhydrase enzymes","volume":"24","author":"Akdemir","year":"2016","journal-title":"Bioorg. Med. Chem."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"3691","DOI":"10.1007\/s00253-020-10504-3","article-title":"Sordaria macrospora: 25 years as a model organism for studying the molecular mechanisms of fruiting body development","volume":"104","author":"Teichert","year":"2020","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1099\/mic.0.032581-0","article-title":"Carbonic anhydrases in fungi","volume":"156","author":"Elleuche","year":"2010","journal-title":"Microbiology"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1111\/exd.12684","article-title":"Characterization of the major bacterial-fungal populations colonizing dandruff scalps in Shanghai, China, shows microbial disequilibrium","volume":"24","author":"Wang","year":"2015","journal-title":"Exp. Dermatol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1016\/j.jinorgbio.2011.11.017","article-title":"(In)organic anions as carbonic anhydrase inhibitors","volume":"111","author":"Supuran","year":"2012","journal-title":"J. Inorg. Biochem."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1194","DOI":"10.1021\/acsmedchemlett.7b00369","article-title":"Benzoxaboroles as Efficient Inhibitors of the beta-Carbonic Anhydrases from Pathogenic Fungi: Activity and Modeling Study","volume":"8","author":"Nocentini","year":"2017","journal-title":"ACS Med. Chem. Lett."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"1064","DOI":"10.1080\/14756366.2017.1355307","article-title":"Inhibition of the beta-carbonic anhydrase from the dandruff-producing fungus Malassezia globosa with monothiocarbamates","volume":"32","author":"Nocentini","year":"2017","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"1721","DOI":"10.1021\/jm300031j","article-title":"Dithiocarbamates strongly inhibit carbonic anhydrases and show antiglaucoma action in vivo","volume":"55","author":"Carta","year":"2012","journal-title":"J. Med. Chem."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"1868","DOI":"10.1039\/c2cc16395k","article-title":"Dithiocarbamates: A new class of carbonic anhydrase inhibitors. Crystallographic and kinetic investigations","volume":"48","author":"Carta","year":"2012","journal-title":"Chem. Commun."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"859","DOI":"10.1016\/j.bmcl.2011.12.033","article-title":"Dithiocarbamates are strong inhibitors of the beta-class fungal carbonic anhydrases from Cryptococcus neoformans, Candida albicans and Candida glabrata","volume":"22","author":"Monti","year":"2012","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"407","DOI":"10.3109\/14756366.2011.641015","article-title":"Dithiocarbamates strongly inhibit the beta-class carbonic anhydrases from Mycobacterium tuberculosis","volume":"28","author":"Maresca","year":"2013","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_93","first-page":"55","article-title":"Arylsulfonyl-N,N-dialkyl-dithiocarbamates as tumor cell growth inhibitors: Novel agents targeting beta-tubulin?","volume":"16","author":"Scozzafava","year":"2001","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"1887","DOI":"10.1016\/S0960-894X(00)00375-9","article-title":"Arylsulfonyl-N,N-diethyl-dithiocarbamates: A novel class of antitumor agents","volume":"10","author":"Scozzafava","year":"2000","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"1548","DOI":"10.1016\/j.bmcl.2010.01.081","article-title":"Carbonic anhydrase inhibitors. Inhibition of transmembrane isoforms IX, XII, and XIV with less investigated anions including trithiocarbonate and dithiocarbamate","volume":"20","author":"Innocenti","year":"2010","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"759","DOI":"10.3109\/14756366.2012.672983","article-title":"Structure-based drug discovery of carbonic anhydrase inhibitors","volume":"27","author":"Supuran","year":"2012","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"2065","DOI":"10.1021\/bc100288c","article-title":"Bishydrazide glycoconjugates for lectin recognition and capture of bacterial pathogens","volume":"21","author":"Adak","year":"2010","journal-title":"Bioconjug. Chem."},{"key":"ref_98","doi-asserted-by":"crossref","unstructured":"Lomelino, C.L., Supuran, C.T., and McKenna, R. (2016). Non-Classical Inhibition of Carbonic Anhydrase. Int. J. Mol. Sci., 17.","DOI":"10.3390\/ijms17071150"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0027-5107(00)00036-1","article-title":"Yeast as an honorary mammal","volume":"451","author":"Resnick","year":"2000","journal-title":"Mutat. Res."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"23477","DOI":"10.1074\/jbc.M110.125153","article-title":"A systems biology approach to dissection of the effects of small bicyclic peptidomimetics on a panel of Saccharomyces cerevisiae mutants","volume":"285","author":"Stefanini","year":"2010","journal-title":"J. Biol. Chem."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"3570","DOI":"10.1016\/j.bmcl.2013.04.028","article-title":"Carbonic anhydrase inhibitors. Benzenesulfonamides incorporating cyanoacrylamide moieties strongly inhibit Saccharomyces cerevisiae beta-carbonic anhydrase","volume":"23","author":"Alafeefy","year":"2013","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"3327","DOI":"10.2174\/138161210793429878","article-title":"Saccharomyces cerevisiae beta-carbonic anhydrase: Inhibition and activation studies","volume":"16","author":"Isik","year":"2010","journal-title":"Curr. Pharm. Des."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"132","DOI":"10.3109\/14756366.2015.1010529","article-title":"Dithiocarbamates with potent inhibitory activity against the Saccharomyces cerevisiae beta-carbonic anhydrase","volume":"31","author":"Bozdag","year":"2016","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"495","DOI":"10.3109\/14756366.2013.806497","article-title":"Carbonic anhydrase inhibitors. Phenols incorporating 2- or 3-pyridyl-ethenylcarbonyl and tertiary amine moieties strongly inhibit Saccharomyces cerevisiae beta-carbonic anhydrase","volume":"29","author":"Bilginer","year":"2014","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1128\/CMR.12.1.80","article-title":"Candida glabrata: Review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans","volume":"12","author":"Fidel","year":"1999","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"4802","DOI":"10.1016\/j.bmcl.2009.06.048","article-title":"Carbonic anhydrase inhibitors. Inhibition of the beta-class enzyme from the pathogenic yeast Candida glabrata with anions","volume":"19","author":"Innocenti","year":"2009","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"2925","DOI":"10.1016\/j.bmc.2013.03.077","article-title":"Synthesis and carbonic anhydrase inhibitory properties of sulfamides structurally related to dopamine","volume":"21","author":"Aksu","year":"2013","journal-title":"Bioorg. Med. Chem."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1007\/s00294-009-0238-x","article-title":"Evolution of carbonic anhydrases in fungi","volume":"55","author":"Elleuche","year":"2009","journal-title":"Curr. Genet."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"10299","DOI":"10.1074\/jbc.M009182200","article-title":"Crystal structure of the \u201ccab\u201d-type beta class carbonic anhydrase from the archaeon Methanobacterium thermoautotrophicum","volume":"276","author":"Strop","year":"2001","journal-title":"J. Biol. Chem."},{"key":"ref_110","doi-asserted-by":"crossref","unstructured":"Vullo, D., Lehneck, R., Donald, W.A., Poggeler, S., and Supuran, C.T. (2020). Anion Inhibition Studies of the beta-Class Carbonic Anhydrase CAS3 from the Filamentous Ascomycete Sordaria macrospora. Metabolites, 10.","DOI":"10.3390\/metabo10030093"},{"key":"ref_111","doi-asserted-by":"crossref","unstructured":"Vullo, D., Lehneck, R., Donald, W.A., Poggeler, S., and Supuran, C.T. (2020). Sulfonamide Inhibition Studies of the beta-Class Carbonic Anhydrase CAS3 from the Filamentous Ascomycete Sordaria macrospora. Molecules, 25.","DOI":"10.3390\/molecules25051036"},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1080\/14756366.2018.1425687","article-title":"Sulfonamide inhibition studies of two beta-carbonic anhydrases from the ascomycete fungus Sordaria macrospora, CAS1 and CAS2","volume":"33","author":"Vullo","year":"2018","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1111\/myc.12276","article-title":"Presence, species distribution, and density of Malassezia yeast in patients with seborrhoeic dermatitis\u2014A community-based case-control study and review of literature","volume":"58","author":"Barac","year":"2015","journal-title":"Mycoses"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1128\/CMR.00021-11","article-title":"The Malassezia genus in skin and systemic diseases","volume":"25","author":"Gaitanis","year":"2012","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"12647","DOI":"10.1074\/jbc.M113.547034","article-title":"Chemical organization of the cell wall polysaccharide core of Malassezia restricta","volume":"289","author":"Stalhberger","year":"2014","journal-title":"J. Biol. Chem."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.mib.2017.10.024","article-title":"Host-microbe interactions: Malassezia and human skin","volume":"40","author":"Grice","year":"2017","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1046\/j.1467-2494.2000.00024.x","article-title":"The antidandruff efficacy of a shampoo containing piroctone olamine and salicylic acid in comparison to that of a zinc pyrithione shampoo","volume":"22","author":"Loden","year":"2000","journal-title":"Int. J. Cosmet. Sci."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1111\/j.1365-2133.2011.10570.x","article-title":"Malassezia, dandruff and seborrhoeic dermatitis: An overview","volume":"165","author":"Hay","year":"2011","journal-title":"Br. J. Dermatol."},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"5194","DOI":"10.1016\/j.bmcl.2015.09.068","article-title":"Anion inhibition studies of the dandruff-producing fungus Malassezia globosa beta-carbonic anhydrase MgCA","volume":"25","author":"Vullo","year":"2015","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_120","doi-asserted-by":"crossref","unstructured":"Del Prete, S., Angeli, A., Ghobril, C., Hitce, J., Clavaud, C., Marat, X., Supuran, C.T., and Capasso, C. (2020). Sulfonamide Inhibition Profile of the beta-Carbonic Anhydrase from Malassezia restricta, An Opportunistic Pathogen Triggering Scalp Conditions. Metabolites, 10.","DOI":"10.3390\/metabo10010039"},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"1260","DOI":"10.1016\/j.bmc.2016.12.040","article-title":"Dithiocarbamates effectively inhibit the beta-carbonic anhydrase from the dandruff-producing fungus Malassezia globosa","volume":"25","author":"Vullo","year":"2017","journal-title":"Bioorg. Med. Chem."},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"2577","DOI":"10.1016\/j.bmc.2017.03.026","article-title":"Inhibition of Malassezia globosa carbonic anhydrase with phenols","volume":"25","author":"Bua","year":"2017","journal-title":"Bioorg. Med. Chem."},{"key":"ref_123","doi-asserted-by":"crossref","unstructured":"Paloukopoulou, C., Govari, S., Soulioti, A., Stefanis, I., Angeli, A., Matheeussen, A., Capasso, C., Cos, P., Supuran, C.T., and Karioti, A. (2021). Phenols from Origanum dictamnus L. and Thymus vulgaris L. and their activity against Malassezia globosa carbonic anhydrase. Nat. Prod. Res., 1\u20137.","DOI":"10.1080\/14786419.2021.1880406"},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1080\/14756366.2019.1681987","article-title":"Phosphonamidates are the first phosphorus-based zinc binding motif to show inhibition of beta-class carbonic anhydrases from bacteria, fungi, and protozoa","volume":"35","author":"Alissa","year":"2020","journal-title":"J. Enzym. Inhib. Med. Chem."},{"key":"ref_125","doi-asserted-by":"crossref","unstructured":"Del Prete, S., Vullo, D., Ghobril, C., Hitce, J., Clavaud, C., Marat, X., Capasso, C., and Supuran, C.T. (2019). Cloning, Purification, and Characterization of a beta-Carbonic Anhydrase from Malassezia restricta, an Opportunistic Pathogen Involved in Dandruff and Seborrheic Dermatitis. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20102447"},{"key":"ref_126","doi-asserted-by":"crossref","unstructured":"Prete, S.D., Angeli, A., Ghobril, C., Hitce, J., Clavaud, C., Marat, X., Supuran, C.T., and Capasso, C. (2019). Anion Inhibition Profile of the beta-Carbonic Anhydrase from the Opportunist Pathogenic Fungus Malassezia Restricta Involved in Dandruff and Seborrheic Dermatitis. 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