The first activation study of the β-carbonic anhydrases from the pathogenic bacteria Brucella suis and Francisella tularensis with amines and amino acids

References

• a) El-Sayed A, Awad W. Brucellosis: evolution and expected comeback. Int J Vet Sci Med 2018;6(Suppl):S31–S5;
   PubMed Web of Science ®Google Scholar
  b) Dadar M, Shahali Y, Whatmore AM. Human brucellosis caused by raw dairy products: a review on the occurrence, major risk factors and prevention. Int J Food Microbiol 2019;292:39–47;
   PubMed Web of Science ®Google Scholar
  c) Tuon FF, Gondolfo RB, Cerchiari N. Human-to-human transmission of Brucella - a systematic review. Trop Med Int Health 2017;22:539–46.
   PubMed Web of Science ®Google Scholar
• a) Hull NC, Schumaker BA. Comparisons of brucellosis between human and veterinary medicine. Infect Ecol Epidemiol 2018;8:1500846;
   PubMedGoogle Scholar
  b) Cross AR, Baldwin VM, Roy S, et al. Zoonoses under our noses. Microbes Infect 2019;21:10–9;
   PubMed Web of Science ®Google Scholar
  c) Köhler S, Ouahrani-Bettache S, Winum JY. Brucella suis carbonic anhydrases and their inhibitors: towards alternative antibiotics? J Enzyme Inhib Med Chem 2017;32:683–7.
   PubMed Web of Science ®Google Scholar
• a) Hirschmann JV. From squirrels to biological weapons: the early history of tularemia. Am J Med Sci 2018;356:319–28;
   PubMed Web of Science ®Google Scholar
  b) Pilo P. Phylogenetic lineages of Francisella tularensis in animals. Front Cell Infect Microbiol 2018;8:258.
   Google Scholar
• a) Faber M, Heuner K, Jacob D, Grunow R. Tularemia in Germany-a re-emerging zoonosis. Front Cell Infect Microbiol 2018;8:40;
   PubMed Web of Science ®Google Scholar
  b) Caspar Y, Maurin M. Francisella tularensis susceptibility to antibiotics: a comprehensive review of the data obtained in vitro and in animal models. Front Cell Infect Microbiol 2017;7:122.
   PubMed Web of Science ®Google Scholar
• a) Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016;473:2023–32;
   PubMed Web of Science ®Google Scholar
  b) Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov 2017;12:61–88;
   PubMed Web of Science ®Google Scholar
  c) Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81;
   PubMed Web of Science ®Google Scholar
  d) Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011;10:767–77;
   PubMed Web of Science ®Google Scholar
  e) 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.
   PubMedGoogle Scholar
• a) Capasso C, Supuran CT. An overview of the alpha-, beta-and gamma-carbonic anhydrases from Bacteria: can bacterial carbonic anhydrases shed new light on evolution of bacteria? J Enzyme Inhib Med Chem 2015;30:325–32;
   PubMed Web of Science ®Google Scholar
  b) Del Prete S, Vullo D, Fisher GM, et al. Discovery of a new family of carbonic anhydrases in the malaria pathogen Plasmodium falciparum–the η-carbonic anhydrases. Bioorg Med Chem Lett 2014;24:4389–96;
   PubMed Web of Science ®Google Scholar
  c) Supuran CT. Structure-based drug discovery of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2012;27:759–72;
   PubMed Web of Science ®Google Scholar
  d) Ozensoy Guler O, Capasso C, Supuran CT. A magnificent enzyme superfamily: carbonic anhydrases, their purification and characterization. J Enzyme Inhib Med Chem 2016;31:689–94.
   PubMed Web of Science ®Google Scholar
• 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;
   PubMed Web of Science ®Google Scholar
  b) Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60;
   PubMed Web of Science ®Google Scholar
  c) Alterio V, Di 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;
   PubMed Web of Science ®Google Scholar
  d) 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.
   PubMed Web of Science ®Google Scholar
• a) Supuran CT. Carbonic anhydrase activators. Future Med Chem 2018;10:561–73;
   PubMed Web of Science ®Google Scholar
  b) Tanini D, Capperucci A, Supuran CT, Angeli A. Sulfur, selenium and tellurium containing amines act as effective carbonic anhydrase activators. Bioorg Chem 2019;87:516–22;
   PubMed Web of Science ®Google Scholar
  c) Rami M, Winum JY, Supuran CT, et al. (Hetero)aryl substituted thiazol-2,4-yl scaffold as human carbonic anhydrase I, II, VII and XIV activators. J Enzyme Inhib Med Chem 2019;34:224–9.
   PubMed Web of Science ®Google Scholar
• a) Briganti F., Mangani S., Orioli P., et al., Carbonic anhydrase activators: x-ray crystallographic and spectroscopic investigations for the interaction of isozymes I and II with histamine. Biochemistry 1997;36:10384–92;
   PubMed Web of Science ®Google Scholar
  b) Clare B.W., Supuran C.T., Carbonic anhydrase activators. 3: structure-activity correlations for a series of isozyme II activators. J Pharm Sci 1994;83:768–73;
   PubMed Web of Science ®Google Scholar
  c) Ilies M, Scozzafava A, Supuran CT. Carbonic anhydrase activators. In: Supuran CT, Scozzafava A, Conway J, eds. Carbonic anhydrase – its inhibitors and activators. Boca Raton: CRC Press; 2004:317–52;
   Google Scholar
  d) Bhatt A, Mondal UK, Supuran CT, et al. Crystal structure of carbonic anhydrase II in complex with an activating ligand: implications in neuronal function. Mol Neurobiol 2018;55:7431–7.
   PubMed Web of Science ®Google Scholar
• a) Akocak S, Lolak N, Vullo D, et al. Synthesis and biological evaluation of histamine Schiff bases as carbonic anhydrase I, II, IV, VII, and IX activators. J Enzyme Inhib Med Chem 2017;32:1305–12;
   PubMed Web of Science ®Google Scholar
  b) Angeli A, Vaiano F, Mari F, et al. Psychoactive substances belonging to the amphetamine class potently activate brain carbonic anhydrase isoforms VA, VB, VII, and XII. J Enzyme Inhib Med Chem 2017;32:1253–9;
   PubMed Web of Science ®Google Scholar
  c) Licsandru E, Tanc M, Kocsis I, Barboiu M, Supuran CT. A class of carbonic anhydrase I - selective activators. J Enzyme Inhib Med Chem 2017;32:37–46;
   PubMed Web of Science ®Google Scholar
  d) Akocak S, Lolak N, Bua S, et al. α-Carbonic anhydrases are strongly activated by spinaceamine derivatives. Bioorg Med Chem 2019;27:800–4.
   PubMed Web of Science ®Google Scholar
• a) 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;
   PubMed Web of Science ®Google Scholar
  b) Pacchiano F, Aggarwal M, Avvaru BS, et al. Selective hydrophobic pocket binding observed within the carbonic anhydrase II active site accommodate different 4-substituted-ureido-benzenesulfonamides and correlate to inhibitor potency. Chem Commun (Camb) 2010;46:8371–3;
   PubMed Web of Science ®Google Scholar
  c) Carta F, Scozzafava A, Supuran CT. Sulfonamides: a patent review (2008–2012). Expert OpinTher Pat 2012;22:747–58;
   PubMed Web of Science ®Google Scholar
  d) Briganti F, Pierattelli R, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. Part 37. Novel classes of carbonic anhydrase inhibitors and their interaction with the native and cobalt-substituted enzyme: kinetic and spectroscopic investigations. Eur J Med Chem 1996;31:1001–10;
   Web of Science ®Google Scholar
  e) Supuran CT, Clare BW. Carbonic anhydrase inhibitors. Part 57. Quantum chemical QSAR of a group of 1,3,4-thiadiazole and 1,3,4-thiadiazoline disulfonamides with carbonic anhydrase inhibitory properties. Eur J Med Chem 1999;34:41–50.
   Web of Science ®Google Scholar
• a) Perfetto R, Del Prete S, Vullo D, et al. Cloning, expression and purification of the α-carbonic anhydrase from the mantle of the Mediterranean mussel, Mytilusg alloprovincialis. J Enzyme Inhib Med Chem 2017;32:1029–35;
   PubMed Web of Science ®Google Scholar
  b) Abdoli M, Angeli A, Bozdag M, et al. Synthesis and carbonic anhydrase I, II, VII, and IX inhibition studies with a series of benzo[d]thiazole-5- and 6-sulfonamides. J Enzyme Inhib Med Chem 2017;32:1071–8;
   PubMed Web of Science ®Google Scholar
  c) 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;
   PubMed Web of Science ®Google Scholar
  d) 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.
   PubMed Web of Science ®Google Scholar
• a) Supuran CT, Capasso C. Carbonic anhydrase from Porphyromonas gingivalis as a drug target. Pathogens 2017;6:E30;
   PubMed Web of Science ®Google Scholar
  b) Capasso C, Supuran CT. Inhibition of bacterial carbonic anhydrases as a novel approach to escape drug resistance. Curr Top Med Chem 2017;17:1237–48;
   PubMed Web of Science ®Google Scholar
  c) Supuran CT, Capasso C. New light on bacterial carbonic anhydrases phylogeny based on the analysis of signal peptide sequences. J Enzyme Inhib Med Chem 2016;31:1254–60;
   PubMed Web of Science ®Google Scholar
  d) Vullo D, Del Prete S, Di Fonzo P, et al. Comparison of the sulfonamide inhibition profiles of the β- and γ-carbonic anhydrases from the pathogenic bacterium Burkholderia pseudomallei. Molecules 2017;22:421–435;
   PubMed Web of Science ®Google Scholar
  e) Prete SD, Vullo D, di Fonzo P, et al. Sulfonamide inhibition profile of the γ-carbonic anhydrase identified in the genome of the pathogenic bacterium Burkholderia pseudomallei the etiological agent responsible of melioidosis. Bioorg Med Chem Lett 2017;27:490–5.
   PubMed Web of Science ®Google Scholar
• a) Supuran CT. Applications of carbonic anhydrases inhibitors in renal and central nervous system diseases. Expert Opin Ther Pat 2018;28:713–21;
   PubMed Web of Science ®Google Scholar
  b) Supuran CT. Carbonic anhydrase inhibitors and their potential in a range of therapeutic areas. Expert Opin Ther Pat 2018;28:709–12;
   PubMed Web of Science ®Google Scholar
  c) Monti SM, Supuran CT, De Simone G. Anticancer carbonic anhydrase inhibitors: a patent review (2008 - 2013). Expert Opin Ther Pat 2013;23:737–49;
   PubMed Web of Science ®Google Scholar
  d) Pastorekova S, Casini A, Scozzafava A, et al. Carbonic anhydrase inhibitors: the first selective, membrane-impermeant inhibitors targeting the tumor-associated isozyme IX. Bioorg Med Chem Lett 2004;14:869–73.
   PubMed Web of Science ®Google Scholar
• a) Scozzafava A, Supuran CT, Carta F. Antiobesity carbonic anhydrase inhibitors: a literature and patent review. Expert Opin Ther Pat 2013;23:725–35;
   PubMed Web of Science ®Google Scholar
  b) Supuran CT. Carbonic anhydrase inhibition and the management of hypoxic tumors. Metabolites 2017;7:E48;
   PubMed Web of Science ®Google Scholar
  c) Supuran CT. Carbonic anhydrase inhibitors in the treatment and prophylaxis of obesity. Expert Opin Ther Pat 2003;13:1545–50;
   Web of Science ®Google Scholar
  d) Winum JY, Temperini C, El Cheikh K, et al. Carbonic anhydrase inhibitors: clash with Ala65 as a means for designing inhibitors with low affinity for the ubiquitous isozyme II, exemplified by the crystal structure of the topiramate sulfamide analogue. J Med Chem 2006;49:7024–31;
   PubMed Web of Science ®Google Scholar
  e) Rehman SU, Chohan ZH, Gulnaz F, Supuran CT. In-vitro antibacterial, antifungal and cytotoxic activities of some coumarins and their metal complexes. J Enzyme Inhib Med Chem 2005;20:333–40.
   PubMed Web of Science ®Google Scholar
• a) Supuran CT. Carbonic anhydrase inhibition and the management of neuropathic pain. Expert Rev Neurother 2016;16:961–8;
   PubMed Web of Science ®Google Scholar
  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.
   PubMed Web of Science ®Google Scholar
• a) 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(suppl 4):60–3;
   PubMed Web of Science ®Google Scholar
  b) Bua S, Di Cesare Mannelli L, Vullo D, et al. Design and synthesis of novel nonsteroidal anti-inflammatory drugs and carbonic anhydrase inhibitors hybrids (NSAIDs-CAIs) for the treatment of rheumatoid arthritis. J Med Chem 2017;60:1159–70.
   PubMed Web of Science ®Google Scholar
• a) Del Prete S, Vullo D, Osman SM, et al. Anion inhibitors of the β-carbonic anhydrase from the pathogenic bacterium responsible of tularemia, Francisella tularensis. Bioorg Med Chem 2017;25:4800–4;
   PubMed Web of Science ®Google Scholar
  b) Del Prete S, Vullo D, Osman SM, et al. Sulfonamide inhibition profiles of the β-carbonic anhydrase from the pathogenic bacterium Francisella tularensis responsible of the febrile illness tularemia. Bioorg Med Chem 2017;25:3555–61;
   PubMed Web of Science ®Google Scholar
  c) Joseph P, Turtaut F, Ouahrani-Bettache S, et al. Cloning, characterization, and inhibition studies of a beta-carbonic anhydrase from Brucella suis. J Med Chem 2010;53:2277–85;
   PubMed Web of Science ®Google Scholar
  d) Joseph P, Ouahrani-Bettache S, Montero JL, et al. A new β-carbonic anhydrase from Brucella suis, its cloning, characterization, and inhibition with sulfonamides and sulfamates, leading to impaired pathogen growth. Bioorg Med Chem 2011;19:1172–8.
   PubMed Web of Science ®Google Scholar
• a) Angeli A, Del Prete S, Donald WA, et al. The γ-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae is potently activated by amines and amino acids. Bioorg Chem 2018;77:1–5;
   PubMed Web of Science ®Google Scholar
  b) Angeli A, Del Prete S, Osman SM, et al. Activation studies with amines and amino acids of the β-carbonic anhydrase encoded by the Rv3273 gene from the pathogenic bacterium Mycobacterium tuberculosis. J Enzyme Inhib Med Chem 2018;33:364–9;
   PubMed Web of Science ®Google Scholar
  c) Angeli A, Del Prete S, Osman SM, et al. Activation studies of the α- and β-carbonic anhydrases from the pathogenic bacterium Vibrio cholerae with amines and amino acids. J Enzyme Inhib Med Chem 2018;33:227–33;
   PubMed Web of Science ®Google Scholar
  d) Vullo D, Del Prete S, Osman SM, et al. Comparison of the amine/amino acid activation profiles of the β- and γ-carbonic anhydrases from the pathogenic bacterium Burkholderia pseudomallei. J Enzyme Inhib Med Chem 2018;33:25–30;
   PubMed Web of Science ®Google Scholar
  e) Vullo D, Del Prete S, Osman SM, et al. Burkholderia pseudomallei γ-carbonic anhydrase is strongly activated by amino acids and amines. Bioorg Med Chem Lett 2016;27:77–80.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• a) Temperini C, Scozzafava A, Supuran CT. Carbonic anhydrase activation and the drug design. Curr Pharm Des 2008;14:708–715;
   PubMed Web of Science ®Google Scholar
  b) Isik S, Guler OO, Kockar F, et al. Saccharomyces cerevisiae β-carbonic anhydrase: inhibition and activation studies. Curr Pharm Des 2010;16:3327–36.
   PubMed Web of Science ®Google Scholar
• a) Temperini C, Scozzafava A, Vullo D, Supuran CT. Carbonic anhydrase activators. Activation of isozymes I, II, IV, VA, VII, and XIV with l- and d-histidine and crystallographic analysis of their adducts with isoform II: engineering proton-transfer processes within the active site of an enzyme. Chemistry 2006;12:7057–66;
   PubMed Web of Science ®Google Scholar
  b) Temperini C, Scozzafava A, Vullo D, Supuran CT. Carbonic anhydrase activators. Activation of isoforms I, II, IV, VA, VII, and XIV with L- and D-phenylalanine and crystallographic analysis of their adducts with isozyme II: stereospecific recognition within the active site of an enzyme and its consequences for the drug design. J Med Chem 2006;49:3019–27;
   PubMed Web of Science ®Google Scholar
  c) Temperini C, Innocenti A, Scozzafava A, Supuran CT. Carbonic anhydrase activators: kinetic and X-ray crystallographic study for the interaction of D- and L-tryptophan with the mammalian isoforms I-XIV. Bioorg Med Chem 2008;16:8373–8.
   PubMed Web of Science ®Google Scholar
• a) Temperini C, Innocenti A, Scozzafava A, et al. Carbonic anhydrase activators: L-Adrenaline plugs the active site entrance of isozyme II, activating better isoforms I, IV, VA, VII, and XIV. Bioorg Med Chem Lett 2007;17:628–35;
   PubMed Web of Science ®Google Scholar
  b) Temperini C, Scozzafava A, Puccetti L, Supuran CT. Carbonic anhydrase activators: X-ray crystal structure of the adduct of human isozyme II with L-histidine as a platform for the design of stronger activators. Bioorg Med Chem Lett 2005;15:5136–41;
   PubMed Web of Science ®Google Scholar
  c) Temperini C, Scozzafava A, Supuran CT. Carbonic anhydrase activators: the first X-ray crystallographic study of an adduct of isoform I. Bioorg Med Chem Lett 2006;16:5152–6.
   PubMed Web of Science ®Google Scholar
• a) Vullo D, Nishimori I, Innocenti A, et al. Carbonic anhydrase activators: an activation study of the human mitochondrial isoforms VA and VB with amino acids and amines. Bioorg Med Chem Lett 2007;17:1336–40;
   PubMed Web of Science ®Google Scholar
  b) Pastorekova S, Vullo D, Nishimori I, et al. Carbonic anhydrase activators: activation of the human tumor-associated isozymes IX and XII with amino acids and amines. Bioorg Med Chem 2008;16:3530–6;
   PubMed Web of Science ®Google Scholar
  c) Nishimori I, Onishi S, Vullo D, et al. Carbonic anhydrase activators. The first activation study of the human secretory isoform VI. Bioorg Med Chem 2007;15:5351–7.
   PubMed Web of Science ®Google Scholar
• a) Parkkila S, Vullo D, Puccetti L, et al. Carbonic anhydrase activators: activation of isozyme XIII with amino acids and amines. Bioorg Med Chem Lett 2006;16:3955–9;
   PubMed Web of Science ®Google Scholar
  b) Vullo D, Innocenti A, Nishimori I, et al. Carbonic anhydrase activators: activation of the human isoforms VII (cytosolic) and XIV (transmembrane) with amino acids and amines. Bioorg Med Chem Lett 2007;17:4107–12;
   PubMed Web of Science ®Google Scholar
  c) Vullo D, Nishimori I, Scozzafava A, Supuran CT. Carbonic anhydrase activators: activation of the human cytosolic isozyme III and membrane-associated isoform IV with amino acids and amines. Bioorg Med Chem Lett 2008;18:4303–7.
   PubMed Web of Science ®Google Scholar
• a) Innocenti A, Hilvo M, Parkkila S, et al. Carbonic anhydrase activators. Activation of the membrane-associated isoform XV with amino acids and amines. Bioorg Med Chem Lett 2009;19:3430–3;
   PubMed Web of Science ®Google Scholar
  b) Supuran CT, Dinculescu A, Balaban AT. Carbonic anhydrase activators. Part 5. CA II activation by 2,4,6-trisubstituted pyridinium cations with 1-(ω-aminoalkyl) side chains. Rev Roum Chim 1993;38:343–9;
   Web of Science ®Google Scholar
  c) Supuran CT, Barboiu M, Luca C, et al. Carbonic anhydrase activators. Part 14. Synthesis of mono- and bis- pyridinium salt derivatives of 2-amino-5-(2-aminoethyl)- and 2-amino-5-(3-aminopropyl)-1,3,4-thiadiazole, and their interaction with isozyme II. Eur J Med Chem 1996;31:597–606;
   Web of Science ®Google Scholar
  d) Ilies MA, Banciu MD, Ilies M, et al. Carbonic anhydrase activators. Part 17. Synthesis and activation study of a series of 1-(1,2,4-triazole-(1H)-3-yl)-2,4,6-trisubstituted-pyridinium salts against isozymes I, II and IV. Eur J Med Chem 1997;32:911–8.
   Web of Science ®Google Scholar
• a) Ilies M, Banciu MD, Ilies MA, et al. Carbonic anhydrase activators: design of high affinity isozymes I, II, and IV activators, incorporating tri-/tetrasubstituted-pyridinium-azole moieties. J Med Chem 2002;45:504–10;
   PubMed Web of Science ®Google Scholar
  b) Dave K, Scozzafava A, Vullo D, et al. Pyridinium derivatives of histamine are potent activators of cytosolic carbonic anhydrase isoforms I, II and VII. Org Biomol Chem 2011;9:2790–800;
   PubMed Web of Science ®Google Scholar
  c) Dave K, Ilies MA, Scozzafava A, et al. An inhibitor-like binding mode of a carbonic anhydrase activator within the active site of isoform II. Bioorg Med Chem Lett 2011;21:2764–8.
   PubMed Web of Science ®Google Scholar
• a) Scozzafava A, Supuran CT. Carbonic anhydrase activators: human isozyme II is strongly activated by oligopeptides incorporating the carboxyterminal sequence of the bicarbonate anion exchanger AE1. Bioorg Med Chem Lett 2002;12:1177–80;
   PubMed Web of Science ®Google Scholar
  b) Scozzafava A, Supuran CT. Carbonic anhydrase activators: high affinity isozymes I, II, and IV activators, incorporating a beta-alanyl-histidine scaffold. J Med Chem 2002;45:284–91;
   PubMed Web of Science ®Google Scholar
  c) Abdo MR, Vullo D, Saada MC, et al. Carbonic anhydrase activators: activation of human isozymes I, II and IX with phenylsulfonylhydrazido l-histidine derivatives. Bioorg Med Chem Lett 2009;19:2440–3;
   PubMed Web of Science ®Google Scholar
  d) Saada MC, Montero JL, Vullo D, et al. Carbonic anhydrase activators: gold nanoparticles coated with derivatized histamine, histidine, and carnosine show enhanced activatory effects on several mammalian isoforms. J Med Chem 2011;54:1170–7;
   PubMed Web of Science ®Google Scholar
  e) Zhang Y, Legrand YM, Petit E, et al. Dynamic encapsulation and activation of carbonic anhydrase in multivalent dynameric host matrices. Chem Commun (Camb) 2016;52:4053–5.
   PubMed Web of Science ®Google Scholar
• a) Vullo D, De Luca V, Scozzafava A, Carginale V, Rossi M, Supuran CT, Capasso C. The first activation study of a bacterial carbonic anhydrase (CA). The thermostable α-CA from Sulfurihydrogenibium yellowstonense YO3AOP1 is highly activated by amino acids and amines. Bioorg Med Chem Lett 2012;22:6324–7;
   PubMed Web of Science ®Google Scholar
  b) Innocenti A, Zimmerman SA, Scozzafava A, Ferry JG, Supuran CT. Carbonic anhydrase activators: activation of the archaeal beta-class (Cab) and gamma-class (Cam) carbonic anhydrases with amino acids and amines. Bioorg Med Chem Lett 2008;18:6194–8;
   PubMed Web of Science ®Google Scholar
  c) Vullo D, Del Prete S, Osman SM, et al. Comparison of the amine/amino acid activation profiles of the β- and γ-carbonic anhydrases from the pathogenic bacterium Burkholderia pseudomallei. J Enzyme Inhib Med Chem 2018;33:25–30;
   PubMed Web of Science ®Google Scholar
  d) Vullo D, Del Prete S, Osman SM, et al. Burkholderia pseudomallei γ-carbonic anhydrase is strongly activated by amino acids and amines. Bioorg Med Chem Lett 2017;27:77–80;
   PubMed Web of Science ®Google Scholar
  e) Angeli A, Del Prete S, Osman SM, et al. Activation studies of the γ-carbonic anhydrases from the antartic marine bacteria Pseudoalteromonas haloplanktis and Colwellia psychrerythraea with amino acids and amines. Marine Drugs 2019;17:238–47;
   Web of Science ®Google Scholar
  f) Angeli A, Del Prete S, Alasmary FAS, et al. The first activation studies of the η-carbonic anhydrase from the malaria parasite Plasmodium falciparum with amines and amino acids. Bioorg Chem 2018;80:94–8.
   PubMed Web of Science ®Google Scholar
• a) Canto de Souza L, Provensi G, Vullo D, et al. Carbonic anhydrase activation enhances object recognition memory in mice through phosphorylation of the extracellular signal-regulated kinase in the cortex and the hippocampus. Neuropharmacology 2017;118:148–56;
   PubMed Web of Science ®Google Scholar
  b) Wang X, Schröder HC, Schlossmacher U, et al. Modulation of the initial mineralization process of SaOS-2 cells by carbonic anhydrase activators and polyphosphate. Calcif Tissue Int 2014;94:495–509;
   PubMed Web of Science ®Google Scholar
  c) Sanku RKK, John JS, Ilies MA, Walker EA. Potential learning and memory disruptors and enhancers in a simple, 1-day operant task in mice. Behav Pharmacol 2018;29:482–92.
   PubMed Web of Science ®Google Scholar
• a) Monti SM, Meccariello A, Ceruso M, et al. Inhibition studies of Brucella suis β-carbonic anhydrases with a series of 4-substituted pyridine-3-sulphonamides. J Enzyme Inhib Med Chem 2018;33:255–9;
   PubMed Web of Science ®Google Scholar
  b) Ombouma J, Vullo D, Köhler S, et al. N-glycosyl-N-hydroxysulfamides as potent inhibitors of Brucella suis carbonic anhydrases. J Enzyme Inhib Med Chem 2015;30:1010–2.
   PubMed Web of Science ®Google Scholar
• a) Riafrecha LE, Vullo D, Ouahrani-Bettache S, et al. Inhibition of β-carbonic anhydrases from Brucella suis with C-cinnamoyl glycosides incorporating the phenol moiety. J Enzyme Inhib Med Chem 2015;30:1017–20;
   PubMed Web of Science ®Google Scholar
  b) Riafrecha LE, Vullo D, Supuran CT, Colinas PA. C-glycosides incorporating the 6-methoxy-2-naphthyl moiety are selective inhibitors of fungal and bacterial carbonic anhydrases. J Enzyme Inhib Med Chem 2015;30:857–61;
   PubMed Web of Science ®Google Scholar
  c) Maresca A, Scozzafava A, Köhler S, et al. Inhibition of beta-carbonic anhydrases from the bacterial pathogen Brucella suis with inorganic anions. J Inorg Biochem 2012;110:36–9.
   PubMed Web of Science ®Google Scholar
• a) Supuran CT. Bacterial carbonic anhydrases as drug targets: toward novel antibiotics? Front Pharmacol 2011;2:34;
   PubMed Web of Science ®Google Scholar
  b) Supuran CT. Inhibition of bacterial carbonic anhydrases and zinc proteases: from orphan targets to innovative new antibiotic drugs. Curr Med Chem 2012;19:831–44.
   PubMed Web of Science ®Google Scholar
• a) Stefanucci A, Angeli A, Dimmito MP, et al. Activation of β- and γ-carbonic anhydrases from pathogenic bacteria with tripeptides. J Enzyme Inhib Med Chem 2018;33:945–50;
   PubMed Web of Science ®Google Scholar
  b) Angeli A, Buonanno M, Donald WA, et al. The zinc - but not cadmium - containing ζ-carbonic from the diatom Thalassiosira weissflogii is potently activated by amines and amino acids. Bioorg Chem 2018;80:261–5;
   PubMed Web of Science ®Google Scholar
  c) Angeli A, Donald WA, Parkkila S, Supuran CT. Activation studies with amines and amino acids of the β-carbonic anhydrase from the pathogenic protozoan Leishmania donovani chagasi. Bioorg Chem 2018;78:406–10;
   PubMed Web of Science ®Google Scholar
  d) Angeli A, Del Prete S, Donald WA, et al. The γ-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae is potently activated by amines and amino acids. Bioorg Chem 2018;77:1–5.
   PubMed Web of Science ®Google Scholar
• Nguyen GTH, Tran TN, Podgorski MN, et al. Nanoscale ion emitters in native mass spectrometry for measuring ligand-protein binding affinities. ACS Cent Sci 2019;5:308–18.
   PubMed Web of Science ®Google Scholar