Carbonic anhydrase activators

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1 Supuran CT. Structure and function of carbonic anhydrases. Biochem. J. 473(14), 2023–2032 (2016). • Updated review on the carbonic anhydrases (CAs), their structural and functional features.
  Medline CASGoogle Scholar
• 2 Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat. Rev. Drug Discov. 7(2), 168–181 (2008).
  Medline CASGoogle Scholar
• 3 Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J. Enzyme Inhib. Med. Chem. 31(3), 345–360 (2016). • All CA inhibition mechanisms, five of which known, reviewed.
  Medline CASGoogle Scholar
• 4 Xu Y, Feng L, Jeffrey PD, Shi Y, Morel FM. Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 452(7183), 56–61 (2008).
  Medline CASGoogle Scholar
• 5 Ferry JG. The gamma class of carbonic anhydrases. Biochim. Biophys. Acta 1804(2), 374–381 (2010).
  Medline CASGoogle Scholar
• 6 Macauley SR, Zimmerman SA, Apolinario EE et al. The archetype gamma-class carbonic anhydrase (Cam) contains iron when synthesized in vivo. Biochemistry 48(5), 817–819 (2009).
  Medline CASGoogle Scholar
• 7 Tripp BC, Bell CB 3rd, Cruz F, Krebs C, Ferry JG. A role for iron in an ancient carbonic anhydrase. J. Biol. Chem. 279(8), 6683–6687 (2004).
  Medline CASGoogle Scholar
• 8 Domsic JF, McKenna R. Sequestration of carbon dioxide by the hydrophobic pocket of the carbonic anhydrases. Biochim. Biophys. Acta 1804(2), 326–331 (2010).
  Medline CASGoogle Scholar
• 9 Tu CK, Silverman DN, Forsman C, Jonsson BH, Lindskog S. Role of histidine 64 in the catalytic mechanism of human carbonic anhydrase II studied with a site-specific mutant. Biochemistry 28(19), 7913–7918 (1989). •• Shows the role of His64 as proton shuttle.
  Medline CASGoogle Scholar
• 10 Briganti F, Mangani S, Orioli P, Scozzafava A, Vernaglione G, Supuran CT. Carbonic anhydrase activators: x-ray crystallographic and spectroscopic investigations for the interaction of isozymes I and II with histamine. Biochemistry 36(34), 10384–10392 (1997). •• First x-ray crystal structure of a CA–activator complex.
  Medline CASGoogle Scholar
• 11 Alterio V, Di Fiore A, D'Ambrosio K, Supuran CT, De Simone G. Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem. Rev. 112(8), 4421–4468 (2012).
  Medline CASGoogle Scholar
• 12 Supuran CT. Carbonic anhydrases: from biomedical applications of the inhibitors and activators to biotechnological use for CO₂ capture. J. Enzyme Inhib. Med. Chem. 28, 229–230 (2013).
  MedlineGoogle Scholar
• 13 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. 24, 4389–4396 (2014).
  Medline CASGoogle Scholar
• 14 Supuran CT. Diuretics: from classical carbonic anhydrase inhibitors to novel applications of the sulfonamides. Curr. Pharm. Des. 14(7), 641–648 (2008).
  Medline CASGoogle Scholar
• 15 Carta F, Supuran CT. Diuretics with carbonic anhydrase inhibitory action: a patent and literature review (2005–2013). Expert Opin. Ther. Pat. 23(6), 681–691 (2013).
  Medline CASGoogle Scholar
• 16 Masini E, Carta F, Scozzafava A, Supuran CT. Antiglaucoma carbonic anhydrase inhibitors: a patent review. Expert Opin. Ther. Pat. 23(6), 705–716 (2013).
  Medline CASGoogle Scholar
• 17 Supuran CT. Structure-based drug discovery of carbonic anhydrase inhibitors. J. Enzyme Inhib. Med. Chem. 27(6), 759–772 (2012).
  Medline CASGoogle Scholar
• 18 Scozzafava A, Supuran CT, Carta F. Antiobesity carbonic anhydrase inhibitors: a literature and patent review. Expert Opin. Ther. Pat. 23(6), 725–735 (2013).
  Medline CASGoogle Scholar
• 19 Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat. Rev. Drug Discov. 10(10), 767–777 (2011).
  Medline CASGoogle Scholar
• 20 Monti SM, Supuran CT, De Simone G. Anticancer carbonic anhydrase inhibitors: a patent review (2008–2013). Expert Opin. Ther. Pat. 23(6), 737–749 (2013).
  Medline CASGoogle Scholar
• 21 Supuran CT. Carbonic anhydrase inhibition and the management of hypoxic tumors. Metabolites 7, E48 (2017).
  MedlineGoogle Scholar
• 22 Carta F, Di Cesare Mannelli L, Pinard M et al. A class of sulfonamide carbonic anhydrase inhibitors with neuropathic pain modulating effects. Bioorg. Med. Chem. 23(8), 1828–1840 (2015).
  Medline CASGoogle Scholar
• 23 Supuran CT. Carbonic anhydrase inhibition and the management of neuropathic pain. Expert Rev. Neurother. 16(8), 961–968 (2016).
  Medline CASGoogle Scholar
• 24 Di Cesare Mannelli L, Micheli L, Carta F, Cozzi A, Ghelardini C, Supuran CT. Carbonic anhydrase inhibition for the management of cerebral ischemia: in vivo evaluation of sulfonamide and coumarin inhibitors. J. Enzyme Inhib. Med. Chem. 31(6), 894–899 (2016).
  Medline CASGoogle Scholar
• 25 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. 31(Suppl. 4), 60–63 (2016).
  Medline CASGoogle Scholar
• 26 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. 60(3), 1159–1170 (2017).
  Medline CASGoogle Scholar
• 27 Temperini C, Scozzafava A, Supuran CT. Carbonic anhydrase activation and the drug design. Curr. Pharm. Des. 14(7), 708–715 (2008).
  Medline CASGoogle Scholar
• 28 Isik S, Guler OO, Kockar F, Aydin M, Arslan O, Supuran CT. Saccharomyces cerevisiae β-carbonic anhydrase: inhibition and activation studies. Curr. Pharm. Des. 16(29), 3327–3336 (2010).
  Medline CASGoogle Scholar
• 29 Vullo D, De Luca V, Scozzafava A et al. 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. 22(20), 6324–6327 (2012).
  Medline CASGoogle Scholar
• 30 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. 18(23), 6194–6198 (2008).
  Medline CASGoogle Scholar
• 31 Leiner M. Das ferment kohlensäureanhydrase im tierkörper. Naturwissenschaften 28, 316–317 (1940).
  CASGoogle Scholar
• 32 Leiner M, Leiner G. Die aktivatoren der kohlensäureanhydrase. Naturwissenschaften 29, 195–197 (1941).
  CASGoogle Scholar
• 33 Leiner M, Leiner G. Die Messmethoden zur untersuchung der katalytischen wirksamkeit der kohlensäureanhydrase. Biochem. Z. 311, 119–145 (1941).
  Google Scholar
• 34 Main RE, Locke A. Activation of carbonic anhydrase by histamine. J. Biol. Chem. 140, LXXXI (1941).
  Google Scholar
• 35 Kiese M. Die aktivierung der kohlensäureanhydrase. Naturwissenschaften 29, 116–117 (1941).
  CASGoogle Scholar
• 36 Clark AM, Perrin DD. A re-investigation of the question of activators of carbonic anhydrase. Biochem. J. 48(4), 495–503 (1951).
  Medline CASGoogle Scholar
• 37 Ho C, Sturtevant JM. Activation of bovine carbonic anhydrase by ethylenediamine tetraacetic acid. Biochem. Biophys. Res. Commun. 3, 20–23 (1960).
  CASGoogle Scholar
• 38 Silverman DN, Backman L, Tu C. Role of hemoglobin in proton transfer to the active site of carbonic anhydrase. J. Biol. Chem. 254(8), 2588–2591 (1979).
  Medline CASGoogle Scholar
• 39 Supuran CT. Carbonic anhydrase activators. Part 4. A general mechanism of action for activators of isozymes I, II and III. Rev. Roum. Chim. 37, 411–421 (1992). •• Although published in a minor journal, the paper proposes the CA activation mechanism that was subsequently demonstrated by crystallography and other techniques.
  CASGoogle Scholar
• 40 Supuran CT, Balaban AT. Carbonic anhydrase activators. Part 8. pK_a–activation relationship in a series of amino acid derivatives activators of isozyme II. Rev. Roum. Chim. 39, 107–113 (1994).
  CASGoogle Scholar
• 41 Supuran CT, Claramunt RM, Lavandera JL, Elguero J. Carbonic anhydrase activators. XV. A kinetic study of the interaction of bovine isozyme II with pyrazoles, bis- and tris-azolyl-methanes. Biol. Pharm. Bull. 19(11), 1417–1422 (1996).
  Medline CASGoogle Scholar
• 42 Supuran CT, Balaban AT, Cabildo P, Claramunt RM, Lavandera JL, Elguero J. Carbonic anhydrase activators. VII. Isozyme II activation by bisazolyl-methanes, -ethanes and related azoles. Biol. Pharm. Bull. 16(12), 1236–1239 (1993).
  Medline CASGoogle Scholar
• 43 Briganti F, Scozzafava A, Supuran CT. Carbonic anhydrase activators. Part 19 spectroscopic and kinetic investigations for the interaction of isozymes I and II with primary amines. Met. Based Drugs. 4(4), 221–227 (1997).
  Medline CASGoogle Scholar
• 44 Nair SK, Christianson DW. Unexpected pH-dependent conformation of His-64, the proton shuttle of carbonic anhydrase II. J. Am. Chem. Soc. 113, 9455–9458 (1991). • Important crystallographic study on the orientation of His64 in the active site of CA II.
  CASGoogle Scholar
• 45 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 12(27), 7057–7066 (2006).
  Medline CASGoogle Scholar
• 46 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. 49(10), 3019–3027 (2006).
  Medline CASGoogle Scholar
• 47 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. 16(18), 8373–8378 (2008).
  Medline CASGoogle Scholar
• 48 Temperini C, Innocenti A, Scozzafava A, Mastrolorenzo A, Supuran CT. 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. 17(3), 628–635 (2007).
  Medline CASGoogle Scholar
• 49 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. 15(23), 5136–5141 (2005).
  Medline CASGoogle Scholar
• 50 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. 16(19), 5152–5156 (2006).
  Medline CASGoogle Scholar
• 51 Duda D, Tu C, Qian M et al. Structural and kinetic analysis of the chemical rescue of the proton transfer function of carbonic anhydrase II. Biochemistry 40(6), 1741–1748 (2001).
  Medline CASGoogle Scholar
• 52 Duda D, Govindasamy L, Agbandje-McKenna M, Tu C, Silverman DN, McKenna R. The refined atomic structure of carbonic anhydrase II at 1.05 A resolution: implications of chemical rescue of proton transfer. Acta Crystallogr. D Biol. Crystallogr. 59, 93–104 (2003).
  MedlineGoogle Scholar
• 53 Elder I, Tu C, Ming LJ, McKenna R, Silverman DN. Proton transfer from exogenous donors in catalysis by human carbonic anhydrase II. Arch. Biochem. Biophys. 437(1), 106–114 (2005).
  Medline CASGoogle Scholar
• 54 Aggarwal M, Kondeti B, Tu C, Maupin CM, Silverman DN, McKenna R. Structural insight into activity enhancement and inhibition of H64A carbonic anhydrase II by imidazoles. IUCrJ 1(Pt 2), 129–135 (2014).
  Medline CASGoogle Scholar
• 55 Maupin CM, Castillo N, Taraphder S et al. Chemical rescue of enzymes: proton transfer in mutants of human carbonic anhydrase II. J. Am. Chem. Soc. 133(16), 6223–6234 (2011).
  Medline CASGoogle Scholar
• 56 Vullo D, Nishimori I, Innocenti A, Scozzafava A, Supuran CT. Carbonic anhydrase activators: an activation study of the human mitochondrial isoforms VA and VB with amino acids and amines. Bioorg. Med. Chem. Lett. 17(5), 1336–1340 (2007).
  Medline CASGoogle Scholar
• 57 Pastorekova S, Vullo D, Nishimori I, Scozzafava A, Pastorek J, Supuran CT. Carbonic anhydrase activators: activation of the human tumor-associated isozymes IX and XII with amino acids and amines. Bioorg. Med. Chem. 16(7), 3530–3536 (2008).
  Medline CASGoogle Scholar
• 58 Nishimori I, Onishi S, Vullo D, Innocenti A, Scozzafava A, Supuran CT. Carbonic anhydrase activators. The first activation study of the human secretory isoform VI. Bioorg. Med. Chem. 15(15), 5351–5357 (2007).
  Medline CASGoogle Scholar
• 59 Parkkila S, Vullo D, Puccetti L, Parkkila AK, Scozzafava A, Supuran CT. Carbonic anhydrase activators: activation of isozyme XIII with amino acids and amines. Bioorg. Med. Chem. Lett. 16(15), 3955–3959 (2006).
  Medline CASGoogle Scholar
• 60 Vullo D, Innocenti A, Nishimori I, Scozzafava A, Kaila K, Supuran CT. Carbonic anhydrase activators: activation of the human isoforms VII (cytosolic) and XIV (transmembrane) with amino acids and amines. Bioorg. Med. Chem. Lett. 17(15), 4107–4112 (2007).
  Medline CASGoogle Scholar
• 61 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. 18(15), 4303–4307 (2008).
  Medline CASGoogle Scholar
• 62 Innocenti A, Hilvo M, Parkkila S, Scozzafava A, Supuran CT. Carbonic anhydrase activators. Activation of the membrane-associated isoform XV with amino acids and amines. Bioorg. Med. Chem. Lett. 19(13), 3430–3433 (2009).
  Medline CASGoogle Scholar
• 63 Clare BW, Supuran CT. Carbonic anhydrase activators. 3: structure–activity correlations for a series of isozyme II activators. J. Pharm. Sci. 83(6), 768–773 (1994).
  Medline CASGoogle Scholar
• 64 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. 38, 343–349 (1993).
  CASGoogle Scholar
• 65 Supuran CT, Barboiu M, Luca C, Pop E, Brewster ME, Dinculescu A. 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. 31, 597–606 (1996).
  CASGoogle Scholar
• 66 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. 32, 911–918 (1997).
  CASGoogle Scholar
• 67 Ilies M, Banciu MD, Ilies MA, Scozzafava A, Caproiu MT, Supuran CT. Carbonic anhydrase activators: design of high affinity isozymes I, II, and IV activators, incorporating tri-/tetrasubstituted-pyridinium-azole moieties. J. Med. Chem. 45, 504–510 (2002).
  Medline CASGoogle Scholar
• 68 Dave K, Scozzafava A, Vullo D, Supuran CT, Ilies MA. Pyridinium derivatives of histamine are potent activators of cytosolic carbonic anhydrase isoforms I, II and VII. Org. Biomol. Chem. 9(8), 2790–2800 (2011).
  Medline CASGoogle Scholar
• 69 Dave K, Ilies MA, Scozzafava A, Temperini C, Vullo D, Supuran CT. An inhibitor-like binding mode of a carbonic anhydrase activator within the active site of isoform II. Bioorg. Med. Chem. Lett. 21(9), 2764–2768 (2011). • Very interesting binding mode for a CA activator (CAA) as shown by kinetic and x-ray crystallographic studies.
  Medline CASGoogle Scholar
• 70 Scozzafava A, Supuran CT. Carbonic anhydrase activators – part 21. Novel activators of isozymes I, II and IV incorporating carboxamido and ureido histamine moieties. Eur. J. Med. Chem. 35(1), 31–39 (2000).
  Medline CASGoogle Scholar
• 71 Scozzafava A, Supuran CT. Carbonic anhydrase activators. Part 24. High affinity isozymes I, II and IV activators, derivatives of 4-(4-chlorophenylsulfonylureido-amino acyl)ethyl-1H-imidazole. Eur. J. Pharm. Sci. 10(1), 29–41 (2000).
  Medline CASGoogle Scholar
• 72 Supuran CT, Scozzafava A. Carbonic anhydrase activators: amino acyl/dipeptidyl histamine derivatives bind with high affinity to isozymes I, II and IV and act as efficient activators. Bioorg. Med. Chem. 7(12), 2915–2923 (1999).
  Medline CASGoogle Scholar
• 73 Briganti F, Scozzafava A, Supuran CT. Novel carbonic anhydrase isozymes I, II and IV activators incorporating sulfonyl-histamino moieties. Bioorg. Med. Chem. Lett. 9(14), 2043–2048 (1999).
  Medline CASGoogle Scholar
• 74 Supuran CT, Scozzafava A. Carbonic anhydrase activators: synthesis of high affinity isozymes I, II and IV activators, derivatives of 4-(arylsulfonylureido-amino acyl)ethyl-1H-imidazole. J. Enzyme Inhib. 15(5), 471–486 (2000).
  Medline CASGoogle Scholar
• 75 Scozzafava A, Iorga B, Supuran CT. Carbonic anhydrase activators: synthesis of high affinity isozymes I, II and IV activators, derivatives of 4-(4-tosylureido-amino acyl)ethyl-1H-imidazole (histamine derivatives). J. Enzyme Inhib. 15(2), 139–161 (2000).
  Medline CASGoogle Scholar
• 76 Saada MC, Vullo D, Montero JL, Scozzafava A, Winum JY, Supuran CT. Carbonic anhydrase I and II activation with mono- and dihalogenated histamine derivatives. Bioorg. Med. Chem. Lett. 21(16), 4884–4887 (2011).
  Medline CASGoogle Scholar
• 77 Saada MC, Vullo D, Montero JL, Scozzafava A, Supuran CT, Winum JY. Mono- and di-halogenated histamine, histidine and carnosine derivatives are potent carbonic anhydrase I, II, VII, XII and XIV activators. Bioorg. Med. Chem. 22(17), 4752–4758 (2014).
  Medline CASGoogle Scholar
• 78 Draghici B, Vullo D, Akocak S, Walker EA, Supuran CT, Ilies MA. Ethylene bis-imidazoles are highly potent and selective activators for isozymes VA and VII of carbonic anhydrase, with a potential nootropic effect. Chem. Commun. (Camb.) 50(45), 5980–5983 (2014).
  Medline CASGoogle Scholar
• 79 Le Duc Y, Licsandru E, Vullo D, Barboiu M, Supuran CT. Carbonic anhydrases activation with 3-amino-1H-1,2,4-triazole-1-carboxamides: discovery of subnanomolar isoform II activators. Bioorg. Med. Chem. 25(5), 1681–1686 (2017).
  MedlineGoogle Scholar
• 80 Licsandru E, Tanc M, Kocsis I, Barboiu M, Supuran CT. A class of carbonic anhydrase I – selective activators. J. Enzyme Inhib. Med. Chem. 32(1), 37–46 (2017).
  Medline CASGoogle Scholar
• 81 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. 12(8), 1177–1180 (2002).
  Medline CASGoogle Scholar
• 82 Scozzafava A, Supuran CT. Carbonic anhydrase activators: high affinity isozymes I, II, and IV activators, incorporating a beta-alanyl-histidine scaffold. J. Med. Chem. 45(2), 284–291 (2002).
  Medline CASGoogle Scholar
• 83 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. 19(9), 2440–2443 (2009).
  Medline CASGoogle Scholar
• 84 Saada MC, Montero JL, Vullo D, Scozzafava A, Winum JY, Supuran CT. Carbonic anhydrase activators: gold nanoparticles coated with derivatized histamine, histidine, and carnosine show enhanced activatory effects on several mammalian isoforms. J. Med. Chem. 54(5), 1170–1177 (2011).
  Medline CASGoogle Scholar
• 85 Zhang Y, Legrand YM, Petit E, Supuran CT, Barboiu M. Dynamic encapsulation and activation of carbonic anhydrase in multivalent dynameric host matrices. Chem. Commun. (Camb.) 52(21), 4053–4055 (2016).
  Medline CASGoogle Scholar
• 86 Abdelrahim MY, Tanc M, Winum JY, Supuran CT, Barboiu M. Dominant behaviours in the expression of human carbonic anhydrase hCA I activity. Chem. Commun. (Camb.) 50(59), 8043–8046 (2014).
  Medline CASGoogle Scholar
• 87 Maccallini C, Di Matteo M, Vullo D et al. Indazole, pyrazole, and oxazole derivatives targeting nitric oxide synthases and carbonic anhydrases. ChemMedChem 11(16), 1695–1699 (2016).
  Medline CASGoogle Scholar
• 88 Casini A, Caccia S, Scozzafava A, Supuran CT. Carbonic anhydrase activators. The selective serotonin reuptake inhibitors fluoxetine, sertraline and citalopram are strong activators of isozymes I and II. Bioorg. Med. Chem. Lett. 13(16), 2765–2768 (2003).
  Medline CASGoogle Scholar
• 89 Abdülkadir Coban T, Beydemir S, Gülcin I et al. Sildenafil is a strong activator of mammalian carbonic anhydrase isoforms I-XIV. Bioorg. Med. Chem. 17(16), 5791–5795 (2009).
  MedlineGoogle Scholar
• 90 Sugimoto A, Ikeda H, Tsukamoto H et al. Timolol activates the enzyme activities of human carbonic anhydrase I and II. Biol. Pharm. Bull. 33(2), 301–306 (2010). •• The only successful computational study ever reported for a CAA.
  Medline CASGoogle Scholar
• 91 Angeli A, Vaiano F, Mari F, Bertol E, Supuran CT. Psychoactive substances belonging to the amphetamine class potently activate brain carbonic anhydrase isoforms VA, VB, VII, and XII. J. Enzyme Inhib. Med. Chem. 32(1), 1253–1259 (2017). •• This work shows that many psychoactive substances show highly effective CA-activating effects against many isoforms present in the brain.
  Medline CASGoogle Scholar
• 92 Earnhardt JN, Wright SK, Qian M et al. Introduction of histidine analogs leads to enhanced proton transfer in carbonic anhydrase V. Arch. Biochem. Biophys. 361(2), 264–270 (1999).
  Medline CASGoogle Scholar
• 93 Elder I, Han S, Tu C et al. Activation of carbonic anhydrase II by active-site incorporation of histidine analogs. Arch. Biochem. Biophys. 421(2), 283–289 (2004).
  Medline CASGoogle Scholar
• 94 Shah GN, Bonapace G, Hu PY, Strisciuglio P, Sly WS. Carbonic anhydrase II deficiency syndrome (osteopetrosis with renal tubular acidosis and brain calcification): novel mutations in CA2 identified by direct sequencing expand the opportunity for genotype–phenotype correlation. Hum. Mutat. 24, 272 (2004).
  MedlineGoogle Scholar
• 95 Ogilvie JM, Ohlemiller KK, Shah GN et al. Carbonic anhydrase XIV deficiency produces a functional defect in the retinal light response. Proc. Natl Acad. Sci. USA 104(20), 8514–8519 (2007).
  Medline CASGoogle Scholar
• 96 Datta R, Shah GN, Rubbelke TS et al. Progressive renal injury from transgenic expression of human carbonic anhydrase IV folding mutants is enhanced by deficiency of p58IPK. Proc. Natl Acad. Sci. USA 107(14), 6448–6452 (2010).
  Medline CASGoogle Scholar
• 97 van Karnebeek CD, Sly WS, Ross CJ et al. Mitochondrial carbonic anhydrase VA deficiency resulting from CA5A alterations presents with hyperammonemia in early childhood. Am. J. Hum. Genet. 94(3), 453–461 (2014).
  Medline CASGoogle Scholar
• 98 Kendall AG, Tashian RE. Erythrocyte carbonic anhydrase I: inherited deficiency in humans. Science 197(4302), 471–472 (1977).
  Medline CASGoogle Scholar
• 99 Feldshtein M, Elkrinawi S, Yerushalmi B et al. Hyperchlorhidrosis caused by homozygous mutation in CA12, encoding carbonic anhydrase XII. Am. J. Hum. Genet. 87(5), 713–720 (2010).
  Medline CASGoogle Scholar
• 100 Almstedt K, Rafstedt T, Supuran CT, Carlsson U, Hammarström P. Small-molecule suppression of misfolding of mutated human carbonic anhydrase II linked to marble brain disease. Biochemistry 48(23), 5358–5364 (2009).
  Medline CASGoogle Scholar
• 101 Sun MK, Alkon DL. Carbonic anhydrase gating of attention: memory therapy and enhancement. Trends Pharmacol. Sci. 23(2), 83–89 (2002).
  Medline CASGoogle Scholar
• 102 Sun MK, Alkon DL. Pharmacological enhancement of synaptic efficacy, spatial learning, and memory through carbonic anhydrase activation in rats. J. Pharmacol. Exp. Ther. 297(3), 961–967 (2001).
  Medline CASGoogle Scholar
• 103 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 118, 148–156 (2017). • The mechanism by which the activators achieve the spatial learning and memory enhancement has been reported in this paper.
  Medline CASGoogle Scholar
• 104 Hipkiss AR. Could carnosine or related structures suppress Alzheimer's disease? J. Alzheimers Dis. 11(2), 229–240 (2007).
  Medline CASGoogle Scholar
• 105 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. 94(5), 495–509 (2014).
  Medline CASGoogle Scholar
• 106 Müller WE, Schröder HC, Schlossmacher U, Grebenjuk VA, Ushijima H, Wang X. Induction of carbonic anhydrase in SaOS-2 cells, exposed to bicarbonate and consequences for calcium phosphate crystal formation. Biomaterials 34(34), 8671–8680 (2013). •• Crucial observation regarding the role of the CAAs for inducing biomineralization and bone formation.
  Medline CASGoogle Scholar
• 107 Akocak S, Lolak N, Vullo D, Durgun M, Supuran CT. Synthesis and biological evaluation of histamine Schiff bases as carbonic anhydrase I, II, IV, VII, and IX activators. J. Enzyme Inhib. Med. Chem. 32(1), 1305–1312 (2017).
  Medline CASGoogle Scholar