1,040
Views
10
CrossRef citations to date
0
Altmetric
Short Communication

Sulfonamide inhibition studies of two β-carbonic anhydrases from the ascomycete fungus Sordaria macrospora, CAS1 and CAS2

, , &
Pages 390-396 | Received 27 Dec 2017, Accepted 05 Jan 2018, Published online: 24 Jan 2018

References

  • (a) Zickler D, Espagne E. Sordaria, a model system to uncover links between meiotic pairing and recombination. Semin Cell Dev Biol 2016;54:149–57. (b) Teichert I, Nowrousian M, Pöggeler S, Kück U. The filamentous fungus Sordaria macrospora as a genetic model to study fruiting body development. Adv Genet 2014;87:199–244.
  • Lehneck R, Neumann P, Vullo D, et al. Crystal structures of two tetrameric β-carbonic anhydrases from the filamentous ascomycete Sordaria macrospora. FEBS J 2014;281:1759–72.
  • (a) Elleuche S, Pöggeler S. Evolution of carbonic anhydrases in fungi. Curr Genet 2009;55:211–22. (b) Elleuche S, Pöggeler S. Carbonic anhydrases in fungi. Microbiology 2010;1:23–9. (c) Lehneck R, Pöggeler S. Fungal carbonic anhydrases and their inhibition. Top Med Chem 2017;22:95–110. (d) Lehneck R, Pöggeler S. A matter of structure: structural comparison of fungal carbonic anhydrases. Appl Microbiol Biotechnol 2014;98:8433–41.
  • (a) Hall RA, De Sordi L, MacCallum DM, et al. CO2 acts as a signalling molecule in populations of the fungal pathogen Candida albicans. PLoS Pathog 2010;6:e1001193. (b) Cottier F, Leewattanapasuk W, Kemp LR, et al. Carbonic anhydrase regulation and CO2 sensing in the fungal pathogen Candida glabrata involves a novel Rca1p ortholog. Bioorg Med Chem 2013;2:1549–54. (c) Mogensen EG, Janbon G, Chaloupka J, et al. Cryptococcus neoformans senses CO2 through the carbonic anhydrase Can2 and the adenylyl cyclase Cac1. Eukaryot Cell 2006;5:103–11.
  • (a) Elleuche S, Pöggeler S. Beta-carbonic anhydrases play a role in fruiting body development and ascospore germination in the filamentous fungus Sordaria macrospora. PLoS One 2009;4:e5177. (b) Aguilera J, Van Dijken JP, De Winde JH, Pronk JT. Carbonic anhydrase (Nce103p): an essential biosynthetic enzyme for growth of Saccharomyces cerevisiae at atmospheric carbon dioxide pressure. Biochem J 2005;391:311–16.
  • Li YP, Tang X, Wu W, et al. The ctnG gene encodes carbonic anhydrase involved in mycotoxin citrinin biosynthesis from Monascus aurantiacus. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 2015;32:577–83.
  • (a) Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016;4:2023–32. (b) Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60. (c) Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81.
  • (a) Supuran CT. Carbonic anhydrases: from biomedical applications of the inhibitors and activators to biotechnological use for CO2 capture. J Enzyme Inhib Med Chem 2013;28:229–30. (b) Fabrizi F, Mincione F, Somma T, et al. A new approach to antiglaucoma drugs: carbonic anhydrase inhibitors with or without NO donating moieties. Mechanism of action and preliminary pharmacology. J Enzyme Inhib Med Chem 2012;27:138–47. (c) Capasso C, Supuran CT. Bacterial, fungal and protozoan carbonic anhydrases as drug targets. Expert Opin Ther Targets 2015;19:1689–704.
  • (a) Supuran CT. Structure-based drug discovery of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2012;27:759–72. (b) Scozzafava A, Menabuoni L, Mincione F, Supuran CT. Carbonic anhydrase inhibitors. A general approach for the preparation of water-soluble sulfonamides incorporating polyamino-polycarboxylate tails and of their metal complexes possessing long-lasting, topical intraocular pressure-lowering properties. J Med Chem 2002;45:1466–76. (c) Alterio VD, Fiore A, D’Ambrosio K, et al. Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem Rev 2012;112:4421–68.
  • (a) Masini E, Carta F, Scozzafava A, Supuran CT. Antiglaucoma carbonic anhydrase inhibitors: a patent review. Expert Opin Ther Pat 2013;23:705–16. (b) Puccetti L, Fasolis G, Vullo D, et al. Carbonic anhydrase inhibitors. Inhibition of cytosolic/tumor-associated carbonic anhydrase isozymes I, II, IX, and XII with Schiff's bases incorporating chromone and aromatic sulfonamide moieties, and their zinc complexes. Bioorg Med Chem Lett 2005;15:3096–101. (c) Scozzafava A, Menabuoni L, Mincione F, et al. Carbonic anhydrase inhibitors: perfluoroalkyl/aryl-substituted derivatives of aromatic/heterocyclic sulfonamides as topical intraocular pressure-lowering agents with prolonged duration of action. J Med Chem 2000;43:4542–51. (d) Supuran CT, Mincione F, Scozzafava A, et al. Carbonic anhydrase inhibitors—part 52. Metal complexes of heterocyclic sulfonamides: a new class of strong topical intraocular pressure-lowering agents in rabbits. Eur J Med Chem 1998;33:247–54.
  • (a) Innocenti A, Mühlschlegel FA, Hall RA, et al. Carbonic anhydrase inhibitors: inhibition of the beta-class enzymes from the fungal pathogens Candida albicans and Cryptococcus neoformans with simple anions. Bioorg Med Chem Lett 2008;18:5066–70. (b) Innocenti A, Hall RA, Schlicker C, et al. Carbonic anhydrase inhibitors. Inhibition of the beta-class enzymes from the fungal pathogens Candida albicans and Cryptococcus neoformans with aliphatic and aromatic carboxylates. Bioorg Med Chem 2009;17:2654–7.
  • (a) Innocenti A, Hall RA, Schlicker C, et al. Carbonic anhydrase inhibitors. Inhibition and homology modeling studies of the fungal beta-carbonic anhydrase from Candida albicans with sulfonamides. Bioorg Med Chem 2009;1:4503–9. (b) Carta F, Innocenti A, Hall RA, et al. Carbonic anhydrase inhibitors. Inhibition of the β-class enzymes from the fungal pathogens Candida albicans and Cryptococcus neoformans with branched aliphatic/aromatic carboxylates and their derivatives. Bioorg Med Chem Lett 2011;2:2521–6. (c) Rami M, Innocenti A, Montero JL, et al. Synthesis of rhodamine B-benzenesulfonamide conjugates and their inhibitory activity against human α- and bacterial/fungal β-carbonic anhydrases. Bioorg Med Chem Lett 2011;21:5210–13.
  • (a) Innocenti A, Leewattanapasuk W, Mühlschlegel FA, et al. Carbonic anhydrase inhibitors. Inhibition of the beta-class enzyme from the pathogenic yeast Candida glabrata with anions. Bioorg Med Chem Lett 2009;1:4802–5. (b) Monti SM, Maresca A, Viparelli F, et al. Dithiocarbamates are strong inhibitors of the beta-class fungal carbonic anhydrases from Cryptococcus neoformans, Candida albicans and Candida glabrata. Bioorg Med Chem Lett 2012;22:859–62. (c) Vullo D, Leewattanapasuk W, Mühlschlegel FA, et al. Carbonic anhydrase inhibitors: inhibition of the β-class enzyme from the pathogenic yeast Candida glabrata with sulfonamides, sulfamates and sulfamides. Bioorg Med Chem Lett 2013;23:2647–52.
  • (a) Innocenti A, Leewattanapasuk W, Manole G, et al. Carbonic anhydrase activators: activation of the beta-carbonic anhydrase from the pathogenic yeast Candida glabrata with amines and amino acids. Bioorg Med Chem Lett 2010;2:1701–4. (b) Supuran CT. Bortezomib inhibits bacterial and fungal β-carbonic anhydrases. Bioorg Med Chem 2016;24:4406–9.
  • (a) Schlicker C, Hall RA, Vullo D, et al. Structure and inhibition of the CO2-sensing carbonic anhydrase Can2 from the pathogenic fungus Cryptococcus neoformans. J Mol Biol 2009;385:1207–20. (b) Innocenti A, Winum JY, Hall RA, et al. Carbonic anhydrase inhibitors. Inhibition of the fungal beta-carbonic anhydrases from Candida albicans and Cryptococcus neoformans with boronic acids. Bioorg Med Chem Lett 2009;19:2642–5. (c) Davis RA, Hofmann A, Osman A, et al. Natural product-based phenols as novel probes for mycobacterial and fungal carbonic anhydrases. J Med Chem 2011;54:1682–92. (c) Akdemir A, Güzel-Akdemir Ö, Karalı N, Supuran CT. Isatin analogs as novel inhibitors of Candida spp. β-carbonic anhydrase enzymes. Bioorg Med Chem 2016;24:1648–52.
  • (a) Innocenti A, Hall RA, Scozzafava A, et al. Carbonic anhydrase activators: activation of the beta-carbonic anhydrases from the pathogenic fungi Candida albicans and Cryptococcus neoformans with amines and amino acids. Bioorg Med Chem 2010;1:1034–7. (b) Güzel O, Maresca A, Hall RA, et al. Carbonic anhydrase inhibitors. The beta-carbonic anhydrases from the fungal pathogens Cryptococcus neoformans and Candida albicans are strongly inhibited by substituted-phenyl-1H-indole-5-sulfonamides. Bioorg Med Chem Lett 2010;2:2508–11. (c) Nocentini A, Cadoni R, Del Prete S, et al. Benzoxaboroles as efficient inhibitors of the β-carbonic anhydrases from pathogenicf: activity and modeling study. ACS Med Chem Lett 2017;8:1194–8.
  • (a) Hewitson KS, Vullo D, Scozzafava A, et al. Molecular cloning, characterization, and inhibition studies of a β-carbonic anhydrase from Malassezia globosa, a potential antidandruff target. J Med Chem 2012;55:3513–20. (b) Del Prete S, Vullo D, Osman SM, et al. Anion inhibition studies of the dandruff-producing fungus Malassezia globosa β-carbonic anhydrase MgCA. Bioorg Med Chem Lett 2015;25:5194–8. (c) Vullo D, Del Prete S, Nocentini A, et al. Dithiocarbamates effectively inhibit the β-carbonic anhydrase from the dandruff-producing fungus Malassezia globosa. Bioorg Med Chem 2017;25:1260–5. (d) Nocentini A, Vullo D, Del Prete S, et al. Inhibition of the β-carbonic anhydrase from the dandruff-producing fungus Malassezia globosa with monothiocarbamates. J Enzyme Inhib Med Chem 2017;32:1064–70.
  • (a) Singh S, Supuran CT. In silico modeling of β-carbonic anhydrase inhibitors from the fungus Malassezia globosa as antidandruff agents. J Enzyme Inhib Med Chem 2016;31:417–24. (b) Del Prete S, De Luca V, Vullo D, et al. A new procedure for the cloning, expression and purification of the β-carbonic anhydrase from the pathogenic yeast Malassezia globosa, an anti-dandruff drug target. J Enzyme Inhib Med Chem 2016;31:1156–61. (c) Vullo D, Del Prete S, Capasso C, Supuran CT. Carbonic anhydrase activators: activation of the β-carbonic anhydrase from Malassezia globosa with amines and amino acids. Bioorg Med Chem Lett 2016;26:1381–5. (d) Entezari Heravi Y, Bua S, Nocentini A, et al. Inhibition of Malassezia globosa carbonic anhydrase with phenols. Bioorg Med Chem 2017;25:2577–82. (e) Angiolella L, Carradori S, Maccallini C, et al. Targeting Malassezia species for novel synthetic and natural antidandruff agents. Curr Med Chem 2017;24:2392–412.
  • (a) Isik S, Kockar F, Arslan O, et al. Carbonic anhydrase inhibitors. Inhibition of the beta-class enzyme from the yeast Saccharomyces cerevisiae with anions. Bioorg Med Chem Lett 2008;1:6327–231. (b) Isik S, Kockar F, Aydin M, et al. Carbonic anhydrase inhibitors: inhibition of the beta-class enzyme from the yeast Saccharomyces cerevisiae with sulfonamides and sulfamates. Bioorg Med Chem 2009;1:1158–63. (c) Isik S, Kockar F, Aydin M, et al. Carbonic anhydrase activators: activation of the beta-carbonic anhydrase Nce103 from the yeast Saccharomyces cerevisiae with amines and amino acids. Bioorg Med Chem Lett 2009;1:1662–5. (d) Isik S, Guler OO, Kockar F, et al. Saccharomyces cerevisiae β-carbonic anhydrase: inhibition and activation studies. Curr Pharm Des 2010;1:3327–36. (e) Bozdag M, Carta F, Vullo D, et al. Dithiocarbamates with potent inhibitory activity against the Saccharomyces cerevisiae β-carbonic anhydrase. J Enzyme Inhib Med Chem 2016;3:132–6. (f) Bilginer S, Unluer E, Gul HI, et al. Carbonic anhydrase inhibitors. Phenols incorporating 2- or 3-pyridyl-ethenylcarbonyl and tertiary amine moieties strongly inhibit Saccharomyces cerevisiae β-carbonic anhydrase. J Enzyme Inhib Med Chem 2014;29:495–9.
  • (a) Cuesta-Seijo JA, Borchert MS, Navarro-Poulsen JC, et al. Structure of a dimeric fungal α-type carbonic anhydrase. FEBS Lett 2011;5:1042–8. (b) Tobal JM, Balieiro ME. Role of carbonic anhydrases in pathogenic micro-organisms: a focus on Aspergillus fumigatus. J Med Microbiol 2014;6:15–27. (c) Lehenck R, Elleche S, Pöggeler S. The filamentous ascomycete Sordaria macrospora can survive in ambient air without carbonic anhydrases. Mol Microbiol 2014;92:931–44.
  • De Simone G, Supuran CT. (In)organic anions as carbonic anhydrase inhibitors. J Inorg Biochem 2012;111:117–29.
  • Carta F, Scozzafava A, Supuran CT. Sulfonamides: a patent review (2008–2012). Expert Opin Ther Pat 2012;22:747–58.
  • (a) Supuran CT, Vullo D, Manole G, et al. Designing of novel carbonic anhydrase inhibitors and activators. Curr Med Chem Cardiovasc Hematol Agents 2004;2:49–68. (b) De Simone G, Langella E, Esposito D, et al. Insights into the binding mode of sulphamates and sulphamides to hCA II: crystallographic studies and binding free energy calculations. J Enzyme Inhib Med Chem 2017;32:1002–11.
  • (a) Carta F, Supuran CT. Diuretics with carbonic anhydrase inhibitory action: a patent and literature review (2005–2013). Expert Opin Ther Pat 2013;23:681–91. (b) Scozzafava A, Supuran CT, Carta F. Antiobesity carbonic anhydrase inhibitors: a literature and patent review. Expert Opin Ther Pat 2013;23:725–35. (c) Abbate F, Winum JY, Potter BV, et al. Carbonic anhydrase inhibitors: X-ray crystallographic structure of the adduct of human isozyme II with EMATE, a dual inhibitor of carbonic anhydrases and steroid sulfatase. Bioorg Med Chem Lett 2004;14:231–4.
  • (a) Supuran CT. Carbonic anhydrase inhibition and the management of neuropathic pain. Expert Rev Neurother 2016;16:961–8. (b) Di Cesare Mannelli L, Micheli L, Carta F, et al. Carbonic anhydrase inhibition for the management of cerebral ischemia: in vivo evaluation of sulfonamide and coumarin inhibitors. J Enzyme Inhib Med Chem 2016;31:894–9. (c) Margheri F, Ceruso M, Carta F, et al. Overexpression of the transmembrane carbonic anhydrase isoforms IX and XII in the inflamed synovium. J Enzyme Inhib Med Chem 2016;31:60–3.
  • Khalifah RG. The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. J Biol Chem 1971;246:2561–73.