The history and rationale of using carbonic anhydrase inhibitors in the treatment of peptic ulcers. In memoriam Ioan Puşcaş (1932–2015)

References

• Davenport HW. In memoriam: the carbonic anhydrase theory of gastric acid secretion. Gastroenterology 1946;7:374
   PubMed Web of Science ®Google Scholar
• Davenport HW. The early days of carbonic anhydrase. Ann NY Acad Sci 1984;429:3–4
   Web of Science ®Google Scholar
• Sebastian A. A dictionary of the history of medicine. New York-London: The Parthenon Publishing Group; 1999: 172,368,608
   Google Scholar
• Keilin D, Mann T. Carbonic anhydrase. Nature 1939;144:442–3
   Google Scholar
• Sneader W. Drug discovery. A history. Chichester: John Wiley and Sons Ltd; 2005
   Google Scholar
• Roblin RO, Clapp JW. The preparation of heterocyclic sulfonamides. J Am Chem Soc 1950;11:4890–2
   Web of Science ®Google Scholar
• Maren TH. Carbonic anhydrase: chemistry, physiology and inhibition. Physiol Rev 1967;47:595–781
   PubMed Web of Science ®Google Scholar
• Swensson ER. A comparative approach to carbonic anhydrase: the work of Thomas H. Maren. Comp Biochem Physiol A Mol Integr Physiol 2003;1236:229–41
   Web of Science ®Google Scholar
• Forster RE. Remarks on the discovery of carbonic anhydrase. In: Chegwidden WR, Carter NF, Edwards YH, eds. The carbonic anhydrases. New Horizons. Basel: Birkhauser Verlag; 2000:1–11
   Google Scholar
• Van Slyke DD, Hawkins JA. Studies on gas and electrolyte equilibrium in blood. XVI. The evolution of carbon dioxide from blood and buffer solutions. J Biol Chem 1930;87:265–79
   Google Scholar
• Meldrum NU, Roughton FJW. Carbonic anhydrase. Its preparation and properties. J Physiol (London) 1933;80:113–42
   Google Scholar
• Davenport HW, Fisher RB. The mechanism of the secretion of acid and chloride by the gastric mucosa. Am J Physiol 1940;131:165–75
   Google Scholar
• Davenport HW. A history of gastric secretion and digestion, experimental studies to 1975. New York-Oxford: Oxford University Press; 1992
   Google Scholar
• Hollander F. The composition of pure gastric juice. Am J Dig Dis 1934;1:319–29
   Google Scholar
• Teorell T. On the primary acidity of the gastric juice. J Physiol (London) 1940;97:308–15
   Google Scholar
• Davenport HW. The inhibition of carbonic anhydrase and of gastric acid secretion by thiocyanate. Am J Physiol 1940;129:505–14
   Google Scholar
• Puşcaş I, Chiu A, Buzás G, et al. Elucidation of the mechanism of gastric acid secretion. Rev Med Interne 1980;32:233–47
   Google Scholar
• Puşcaş I. Histamine and calcium interaction in the process of gastric acid secretion in humans. Rev Med Interne 1979;312:549–54
   Google Scholar
• Dobrescu D. A propos de l’action de l’histamine sur l’anhydrase carbonique. CR Seances Soc Biol Fil 1966;160:220–2
   PubMedGoogle Scholar
• Salganik RI, Arqutinskaya SV, Bersimbaev RI. The stimulating action of gastric pentapeptide, histamine and cyclic adenosine 3′,5′-monophosphate on carbonic anhydrase in rat stomach. Experientia 1972;28:1191–1
   PubMedGoogle Scholar
• Vinik AI, Heldsinger AA. Cytochemical quantification of physiologic regulation of oxyntic cell carbonic anhydrase. Ann NY Acad Sci 1984;429:592–6
   PubMed Web of Science ®Google Scholar
• Puşcaş I, Coltău M, Baican M, Domuţa G. Omeprazole has a dual mechanism of action: it inhibits both H+K+ATPase and gastric mucosa carbonic anhydrase enzyme in humans (in vitro and in vivo experiments). J Pharmacol Exp Ther 1999;290:530–4
   PubMed Web of Science ®Google Scholar
• Saada MC, Vulloo D, Montero JL, et al. Carbonic anhydrase I and II activation with mono- and dihalogenated histamine. Bioorg Med Chem Lett 2011;21:4884–7
   PubMed Web of Science ®Google Scholar
• Janowitz HD, Colcher H, Hollander F. Inhibition of gastric secretion in dogs by carbonic anhydrase inhibitor 2-acetyl-amino-1,3,4-thiadiazole-5-sulfonamide. Am J Physiol 1952;171:325–30
   PubMed Web of Science ®Google Scholar
• Janowitz HD, Dreiling DA, Roblin HL, Hollander F. Inhibition of the formation of hydrochloric acid in the human stomach by diamox: the role of carbonic anhydrase in gastric acid secretion. Gastroenterology 1957;33:378–81
   PubMed Web of Science ®Google Scholar
• Lindner AE, Cohen N, Berkowitz J, Janowitz HD. A note on the oral dose of acetazolamide required to inhibit acid secretion in man. Gastroenterology 1964;46:273–5
   PubMed Web of Science ®Google Scholar
• Poller L. The effect of acetazolamide, an inhibitor of carbonic anhydrase, on gastric secretion. Br J Pharmacol 1956;11:263–5
   Web of Science ®Google Scholar
• Cheli R, Dodero M. The effect of acetazolamide on gastric secretion in normal subjects and in patients of chronic gastritis confirmed by biopsy. Minerva Gastroenterol 1956;2:120–2
   PubMedGoogle Scholar
• Gailitis RJ, Schreiber W. Carbonic anhydrase inhibition in the management of symptomatic peptic ulcers. Clinical studies with diamox on 125 patients. Am J Dig Dis 1960;5:473–8
   PubMedGoogle Scholar
• Gothe KM. Senkung der Magensaftaziditat durch gezielte Schadigung der saurebildenden Zellen.Behandlungsversuche bei peptischen Magen- und Darmerkrankungen. Med Welt 1963;46:2363–7
   PubMedGoogle Scholar
• Puşcaş I. Inhibition of gastric acid secretion by acetazolamide. Doctoral Thesis, Medical and Pharmaceutical Institute, Timişoara; 1971
   Google Scholar
• Puşcaş I. Treatment of gastroduodenal ulcers with carbonic anhydrase inhibitors. Ann NY Acad Sci 1984;423:587–91
   Web of Science ®Google Scholar
• Puşcaş I, Buzás G. Treatment of duodenal ulcers with ethoxzolamide, an inhibitor of gastric mucosa carbonic anhydrase. Int J Pharmacol Ther Toxicol 1986;24:97–899
   PubMed Web of Science ®Google Scholar
• Puşcaş I. Carbonic anhydrase inhibitors in the treatment of gastric and duodenal ulcers. In: Szabó S, Mózsik Gy, eds. New pharmacology of ulcer disease. New York: Elsevier Publishing Co.;1987: 164–79
   Google Scholar
• Supuran CT. Bacterial carbonic anhydrases as drug targets: towards novel antibiotics? Front Pharmacol 2011;2:34
   PubMed Web of Science ®Google Scholar
• 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
• Chirica LC, Petersson C, Huirtig M, et al. Expression nand localization of alpha- and beta-carbonic anhydrase in Helicobacter pylori. Biochim Biophys Acta 2002;1601:192–9
   PubMed Web of Science ®Google Scholar
• Nishimori I, Minakuchi T, Morimoto K, et al. Carbonic anhydrase inhibitors: DNA cloning and inhibition studies of the alpha-carbonic anhydrase from Helicobacter pylori, a new target for developing sulfonamide and sulfamate gastric drugs. J Med Chem 2006;49:2117–26
   PubMed Web of Science ®Google Scholar
• Nishimori I, Vullo D, Minakuchi T, et al. Carbonic anhydrase inhibitors: cloning and sulfonamide inhibition studies of a carboxyterminal truncated alpha-carbonic anhydrase from Helicobacter pylori. Bioorg Med Chem Lett 2006;16:2182–8
   PubMed Web of Science ®Google Scholar
• Nishimori I, Minakuchi T, Kohsaki T, et al. Carbonic anhydrase inhibitors: the beta-carbonic anhydrase from Helicobacter pylori is a new target for sulfonamide and sulfamate inhibitors. Bioorg Med Chem Lett 2007;17:3585–94
   PubMed Web of Science ®Google Scholar
• Nishimori I, Onishi S, Takeuchi H, Supuran CT. The α- and β-classes carbonic anhydrases from Helicobacter pylori as novel drug targets. Curr Pharm Des 2008;14:622–30
   PubMed Web of Science ®Google Scholar
• Supuran CT. Novel targets against Helicobacter pylori: a bioinformatic approach. Future Microbiol 2007;2:111–14
   Web of Science ®Google Scholar
• Maresca A, Vullo D, Scozzafava A, Supuran CT. Inhibition of the alpha- and beta-carbonic anhydrases from the gastric pathogen Helicobacter pylori with anions. J Enzyme Inhib Med Chem 2013;28:388–91
   PubMed Web of Science ®Google Scholar
• Nishimori I, Takeuchi H, Supuran CT. Inhibition of beta- and alpha-CAs from Helicobacter pylori as potential novel gastric drugs. In: Supuran CT, Winum JY, eds. Drug design of zinc-enzyme inhibitors: functional, structural, and disease applications. Hoboken: Wiley; 2009:359–74
   Google Scholar
• Supuran CT, Scozzafava A. Carbonic anhydrases as targets for medicinal chemistry. Bioorg Med Chem 2007;15:4336–50
   PubMed Web of Science ®Google Scholar
• 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
• 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
• Supuran CT. Carbonic anhydrases: from biomedical applications of the inhibitors and activators to biotechnologic use for CO2 capture. J Enzyme Inhib Med Chem 2013;28:229–30
   PubMed Web of Science ®Google Scholar
• Smith KS, Jakubzick C, Whittam TS, Ferry JG. Carbonic anhydrase is an ancient enzyme widespread in prokaryotes. Proc Natl Acad Sci USA 1999;96:15184–9
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibitors. Bioorg Med Chem Lett 2010;20:3467–74
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Singh S, Supuran CT. 3D-QSAR CoMFA studies on sulfonamide inhibitors of the Rv3588c β-carbonic anhydrase from Mycobacterium tuberculosis and design of not yet synthesized new molecules. J Enzyme Inhib Med Chem 2014;29:449–55
   PubMed Web of Science ®Google Scholar
• 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
• 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
• Capasso C, Supuran CT. Sulfa and trimethoprim-like drugs-antimetabolites acting as carbonic anhydrase, dihydropteroate synthase and dihydrofolate reductase inhibitors. J Enzyme Inhib Med Chem 2014;29:379–87
   PubMed Web of Science ®Google Scholar
• Carta F, Scozzafava A, Supuran CT. Sulfonamides (RSO2NH2): a patent review 2008–2012. Expert Opin Ther Pat 2012;22:747–58
   PubMed Web of Science ®Google Scholar
• Supuran CT, Maresca A, Gregáň F, Remko M. Three new aromatic sulfonamide inhibitors of carbonic anhydrases I, II, IV and XII. J Enzyme Inhib Med Chem 2013;28:289–93
   PubMed Web of Science ®Google Scholar
• Stähler FN, Ganter L, Lederer K, et al. Mutational analysis of the Helicobacter pylori carbonic anhydrases. FEMS Immunol Med Microbiol 2005;44:183–9
   PubMed Web of Science ®Google Scholar
• Marcus EA, Moshfegh AP, Sachs G, Scott DR. The periplasmic α-carbonic anhydrase activity of Helicobacter pylori is essential for acid acclimation. J Bacteriol 2005;187:729–38
   PubMed Web of Science ®Google Scholar
• Sachs G, Weeks DL, Wen Y, et al. Acid acclimation by Helicobacter pylori. Physiology (Bethesda) 2005;20:429–38
   PubMed Web of Science ®Google Scholar
• Shahidzadeh R, Opekun A, Shiotani A, Graham DY. Effect of the carbonic anhydrase inhibitor, acetazolamide, on Helicobacter pylori infection in vivo: a pilot study. Helicobacter 2005;10:136–8
   PubMed Web of Science ®Google Scholar
• Modak JK, Liu YC, Machuca MA, et al. Structural basis for the inhibition of Helicobacter pylori α-carbonic anhydrase by sulfonamides. PLoS One 2015;10:e0127149
   PubMed Web of Science ®Google Scholar