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Polyamines inhibit carbonic anhydrases by anchoring to the zinc-coordinated water molecule.

Carta F, Temperini C, Innocenti A, Scozzafava A, Kaila K, Supuran CT
J Med Chem 53 5511-22 (2010)
Cited: 104 times
EuropePMC logo PMID: 20590092

Abstract

Carbonic anhydrases (CAs, EC 4.2.1.1) are inhibited by sulfonamides, phenols, and coumarins. Polyamines such as spermine, spermidine, and many synthetic congeners are described to constitute a novel class of CA inhibitors (CAIs), interacting with the different CA isozymes with efficiency from the low nanomolar to millimolar range. The main structure-activity relationship for these CAIs have been delineated: the length of the molecule, number of amine moieties, and their functionalization are the main parameters controlling activity. The X-ray crystal structure of the CA II-spermine adduct allowed understanding of the inhibition mechanism. Spermine anchors to the nonprotein zinc ligand through a network of hydrogen bonds. Its distal amine moiety makes hydrogen bonds with residues Thr200 and Pro201, which further stabilize the adduct. Spermine binds differently compared to sulfonamides, phenols, or coumarins, rendering possible to develop CAIs with a diverse inhibition mechanism, profile, and selectivity for various isoforms.

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Reviews citing this publication (20)

  1. Structure-based drug discovery of carbonic anhydrase inhibitors. Supuran CT. J Enzyme Inhib Med Chem 27 759-772 (2012)
  2. How many carbonic anhydrase inhibition mechanisms exist? Supuran CT. J Enzyme Inhib Med Chem 31 345-360 (2016)
  3. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Supuran CT. Expert Opin Drug Discov 12 61-88 (2017)
  4. Antiglaucoma carbonic anhydrase inhibitors: a patent review. Masini E, Carta F, Scozzafava A, Supuran CT. Expert Opin Ther Pat 23 705-716 (2013)
  5. Exploiting the hydrophobic and hydrophilic binding sites for designing carbonic anhydrase inhibitors. De Simone G, Alterio V, Supuran CT. Expert Opin Drug Discov 8 793-810 (2013)
  6. Acetazolamide for the treatment of idiopathic intracranial hypertension. Supuran CT. Expert Rev Neurother 15 851-856 (2015)
  7. Carbonic Anhydrase Inhibitors Targeting Metabolism and Tumor Microenvironment. Angeli A, Carta F, Nocentini A, Winum JY, Zalubovskis R, Akdemir A, Onnis V, Eldehna WM, Capasso C, Simone G, Monti SM, Carradori S, Donald WA, Dedhar S, Supuran CT. Metabolites 10 E412 (2020)
  8. Reconsidering anion inhibitors in the general context of drug design studies of modulators of activity of the classical enzyme carbonic anhydrase. Nocentini A, Angeli A, Carta F, Winum JY, Zalubovskis R, Carradori S, Capasso C, Donald WA, Supuran CT. J Enzyme Inhib Med Chem 36 561-580 (2021)
  9. Drug interaction considerations in the therapeutic use of carbonic anhydrase inhibitors. Supuran CT. Expert Opin Drug Metab Toxicol 12 423-431 (2016)
  10. Cancer Drug Development of Carbonic Anhydrase Inhibitors beyond the Active Site. Singh S, Lomelino CL, Mboge MY, Frost SC, McKenna R. Molecules 23 E1045 (2018)
  11. Carbonic anhydrase inhibition with natural products: novel chemotypes and inhibition mechanisms. Supuran CT. Mol Divers 15 305-316 (2011)
  12. Probing the surface of human carbonic anhydrase for clues towards the design of isoform specific inhibitors. Pinard MA, Mahon B, McKenna R. Biomed Res Int 2015 453543 (2015)
  13. Legionella pneumophila Carbonic Anhydrases: Underexplored Antibacterial Drug Targets. Supuran CT. Pathogens 5 E44 (2016)
  14. Phenols and Polyphenols as Carbonic Anhydrase Inhibitors. Karioti A, Carta F, Supuran CT. Molecules 21 E1649 (2016)
  15. Thermodynamic, kinetic, and structural parameterization of human carbonic anhydrase interactions toward enhanced inhibitor design. Linkuvienė V, Zubrienė A, Manakova E, Petrauskas V, Baranauskienė L, Zakšauskas A, Smirnov A, Gražulis S, Ladbury JE, Matulis D. Q Rev Biophys 51 e10 (2018)
  16. Novel approaches for designing drugs that interfere with pH regulation. Berrino E, Supuran CT. Expert Opin Drug Discov 14 231-248 (2019)
  17. Multicomponent chemistry in the synthesis of carbonic anhydrase inhibitors. Kalinin S, Supuran CT, Krasavin M. J Enzyme Inhib Med Chem 31 185-199 (2016)
  18. Carbonic Anhydrase Inhibitors from Marine Natural Products. Supuran CT. Mar Drugs 20 721 (2022)
  19. Research Progress and Potential Applications of Spermidine in Ocular Diseases. Han W, Li H, Chen B. Pharmaceutics 14 1500 (2022)
  20. Polyamines and α-Carbonic Anhydrases. Scozzafava A, Supuran CT, Carta F. Molecules 21 E1726 (2016)

Articles citing this publication (80)

  1. Dithiocarbamates strongly inhibit carbonic anhydrases and show antiglaucoma action in vivo. Carta F, Aggarwal M, Maresca A, Scozzafava A, McKenna R, Masini E, Supuran CT. J Med Chem 55 1721-1730 (2012)
  2. Selective hydrophobic pocket binding observed within the carbonic anhydrase II active site accommodate different 4-substituted-ureido-benzenesulfonamides and correlate to inhibitor potency. Pacchiano F, Aggarwal M, Avvaru BS, Robbins AH, Scozzafava A, McKenna R, Supuran CT. Chem Commun (Camb) 46 8371-8373 (2010)
  3. Dithiocarbamates: a new class of carbonic anhydrase inhibitors. Crystallographic and kinetic investigations. Carta F, Aggarwal M, Maresca A, Scozzafava A, McKenna R, Supuran CT. Chem Commun (Camb) 48 1868-1870 (2012)
  4. Synthesis and carbonic anhydrase inhibitory properties of sulfamides structurally related to dopamine. Aksu K, Nar M, Tanc M, Vullo D, Gülçin I, Göksu S, Tümer F, Supuran CT. Bioorg Med Chem 21 2925-2931 (2013)
  5. Kinetic and docking studies of phenol-based inhibitors of carbonic anhydrase isoforms I, II, IX and XII evidence a new binding mode within the enzyme active site. Durdagi S, Şentürk M, Ekinci D, Balaydın HT, Göksu S, Küfrevioğlu Öİ, Innocenti A, Scozzafava A, Supuran CT. Bioorg Med Chem 19 1381-1389 (2011)
  6. Carbonic anhydrase inhibitors: in vitro inhibition of α isoforms (hCA I, hCA II, bCA III, hCA IV) by flavonoids. Ekinci D, Karagoz L, Ekinci D, Senturk M, Supuran CT. J Enzyme Inhib Med Chem 28 283-288 (2013)
  7. Carbon- versus sulphur-based zinc binding groups for carbonic anhydrase inhibitors? Supuran CT. J Enzyme Inhib Med Chem 33 485-495 (2018)
  8. Out of the active site binding pocket for carbonic anhydrase inhibitors. D'Ambrosio K, Carradori S, Monti SM, Buonanno M, Secci D, Vullo D, Supuran CT, De Simone G. Chem Commun (Camb) 51 302-305 (2015)
  9. Novel coumarins and 2-thioxo-coumarins as inhibitors of the tumor-associated carbonic anhydrases IX and XII. Carta F, Maresca A, Scozzafava A, Supuran CT. Bioorg Med Chem 20 2266-2273 (2012)
  10. Coumarinyl-substituted sulfonamides strongly inhibit several human carbonic anhydrase isoforms: solution and crystallographic investigations. Wagner J, Avvaru BS, Robbins AH, Scozzafava A, Supuran CT, McKenna R. Bioorg Med Chem 18 4873-4878 (2010)
  11. A highly catalytically active γ-carbonic anhydrase from the pathogenic anaerobe Porphyromonas gingivalis and its inhibition profile with anions and small molecules. Del Prete S, Vullo D, De Luca V, Carginale V, Scozzafava A, Supuran CT, Capasso C. Bioorg Med Chem Lett 23 4067-4071 (2013)
  12. Biochemical characterization of the δ-carbonic anhydrase from the marine diatom Thalassiosira weissflogii, TweCA. Del Prete S, Vullo D, De Luca V, Supuran CT, Capasso C. J Enzyme Inhib Med Chem 29 906-911 (2014)
  13. Anion inhibition studies of two new β-carbonic anhydrases from the bacterial pathogen Legionella pneumophila. Nishimori I, Vullo D, Minakuchi T, Scozzafava A, Osman SM, AlOthman Z, Capasso C, Supuran CT. Bioorg Med Chem Lett 24 1127-1132 (2014)
  14. Conformational variability of different sulfonamide inhibitors with thienyl-acetamido moieties attributes to differential binding in the active site of cytosolic human carbonic anhydrase isoforms. Biswas S, Aggarwal M, Güzel Ö, Scozzafava A, McKenna R, Supuran CT. Bioorg Med Chem 19 3732-3738 (2011)
  15. Discovery of New Potential Anti-Infective Compounds Based on Carbonic Anhydrase Inhibitors by Rational Target-Focused Repurposing Approaches. Annunziato G, Angeli A, D'Alba F, Bruno A, Pieroni M, Vullo D, De Luca V, Capasso C, Supuran CT, Costantino G. ChemMedChem 11 1904-1914 (2016)
  16. Protonography, a technique applicable for the analysis of η-carbonic anhydrase activity. Del Prete S, De Luca V, Supuran CT, Capasso C. J Enzyme Inhib Med Chem 30 920-924 (2015)
  17. Biochemical characterization of the γ-carbonic anhydrase from the oral pathogen Porphyromonas gingivalis, PgiCA. Del Prete S, De Luca V, Vullo D, Scozzafava A, Carginale V, Supuran CT, Capasso C. J Enzyme Inhib Med Chem 29 532-537 (2014)
  18. 7-Substituted-sulfocoumarins are isoform-selective, potent carbonic anhydrase II inhibitors. Tanc M, Carta F, Bozdag M, Scozzafava A, Supuran CT. Bioorg Med Chem 21 4502-4510 (2013)
  19. Salen and tetrahydrosalen derivatives act as effective inhibitors of the tumor-associated carbonic anhydrase XII--a new scaffold for designing isoform-selective inhibitors. Carradori S, De Monte C, D'Ascenzio M, Secci D, Celik G, Ceruso M, Vullo D, Scozzafava A, Supuran CT. Bioorg Med Chem Lett 23 6759-6763 (2013)
  20. Inhibition studies of quinazoline-sulfonamide derivatives against the γ-CA (PgiCA) from the pathogenic bacterium, Porphyromonas gingivalis. Alafeefy AM, Ceruso M, Al-Tamimi AM, Del Prete S, Supuran CT, Capasso C. J Enzyme Inhib Med Chem 30 592-596 (2015)
  21. 7-Aryl-triazolyl-substituted sulfocoumarins are potent, selective inhibitors of the tumor-associated carbonic anhydrase IX and XII. Nocentini A, Ceruso M, Carta F, Supuran CT. J Enzyme Inhib Med Chem 31 1226-1233 (2016)
  22. Mono-/dihydroxybenzoic acid esters and phenol pyridinium derivatives as inhibitors of the mammalian carbonic anhydrase isoforms I, II, VII, IX, XII and XIV. Carta F, Vullo D, Maresca A, Scozzafava A, Supuran CT. Bioorg Med Chem 21 1564-1569 (2013)
  23. Advances in Anti-Cancer Drug Development Targeting Carbonic Anhydrase IX and XII. Mboge MY, McKenna R, Frost SC. Top Anticancer Res 5 3-42 (2015)
  24. Inhibition of mammalian carbonic anhydrases I-XIV with grayanotoxin III: solution and in silico studies. Durdagi S, Scozzafava G, Vullo D, Sahin H, Kolayli S, Supuran CT. J Enzyme Inhib Med Chem 29 469-475 (2014)
  25. Computational investigation of the selectivity of salen and tetrahydrosalen compounds towards the tumor-associated hCA XII isozyme. Akdemir A, De Monte C, Carradori S, Supuran CT. J Enzyme Inhib Med Chem 30 114-118 (2015)
  26. Dithiocarbamates effectively inhibit the β-carbonic anhydrase from the dandruff-producing fungus Malassezia globosa. Vullo D, Del Prete S, Nocentini A, Osman SM, AlOthman Z, Capasso C, Bozdag M, Carta F, Gratteri P, Supuran CT. Bioorg Med Chem 25 1260-1265 (2017)
  27. Synthesis and crystallographic analysis of new sulfonamides incorporating NO-donating moieties with potent antiglaucoma action. Mincione F, Benedini F, Biondi S, Cecchi A, Temperini C, Formicola G, Pacileo I, Scozzafava A, Masini E, Supuran CT. Bioorg Med Chem Lett 21 3216-3221 (2011)
  28. Synthesis of a new series of dithiocarbamates with effective human carbonic anhydrase inhibitory activity and antiglaucoma action. Bozdag M, Carta F, Vullo D, Akdemir A, Isik S, Lanzi C, Scozzafava A, Masini E, Supuran CT. Bioorg Med Chem 23 2368-2376 (2015)
  29. Inhibition of α-class cytosolic human carbonic anhydrases I, II, IX and XII, and β-class fungal enzymes by carboxylic acids and their derivatives: new isoform-I selective nanomolar inhibitors. Sechi M, Innocenti A, Pala N, Rogolino D, Carcelli M, Scozzafava A, Supuran CT. Bioorg Med Chem Lett 22 5801-5806 (2012)
  30. Anion inhibition studies of two α-carbonic anhydrases from Lotus japonicus, LjCAA1 and LjCAA2. Vullo D, Flemetakis E, Scozzafava A, Capasso C, Supuran CT. J Inorg Biochem 136 67-72 (2014)
  31. Natural product polyamines that inhibit human carbonic anhydrases. Davis RA, Vullo D, Supuran CT, Poulsen SA. Biomed Res Int 2014 374079 (2014)
  32. Synthesis of aminocyanopyrazoles via a multi-component reaction and anti-carbonic anhydrase inhibitory activity of their sulfamide derivatives against cytosolic and transmembrane isoforms. Allouche F, Chabchoub F, Carta F, Supuran CT. J Enzyme Inhib Med Chem 28 343-349 (2013)
  33. 5-Substituted-(1,2,3-triazol-4-yl)thiophene-2-sulfonamides strongly inhibit human carbonic anhydrases I, II, IX and XII: solution and X-ray crystallographic studies. Leitans J, Sprudza A, Tanc M, Vozny I, Zalubovskis R, Tars K, Supuran CT. Bioorg Med Chem 21 5130-5138 (2013)
  34. 6-Substituted 1,2-benzoxathiine-2,2-dioxides are isoform-selective inhibitors of human carbonic anhydrases IX, XII and VA. Tanc M, Carta F, Scozzafava A, Supuran CT. Org Biomol Chem 13 77-80 (2015)
  35. 7-Amino-3,4-dihydro-1H-quinolin-2-one, a compound similar to the substituted coumarins, inhibits α-carbonic anhydrases without hydrolysis of the lactam ring. Vullo D, Isik S, Bozdag M, Carta F, Supuran CT. J Enzyme Inhib Med Chem 30 773-777 (2015)
  36. Exploring carbonic anhydrase inhibition with multimeric coumarins displayed on a fullerene scaffold. Abellán-Flos M, Tanç M, Supuran CT, Vincent SP. Org Biomol Chem 13 7445-7451 (2015)
  37. N-Substituted and ring opened saccharin derivatives selectively inhibit transmembrane, tumor-associated carbonic anhydrases IX and XII. Ivanova J, Carta F, Vullo D, Leitans J, Kazaks A, Tars K, Žalubovskis R, Supuran CT. Bioorg Med Chem 25 3583-3589 (2017)
  38. Attachment of carbohydrates to methoxyaryl moieties leads to highly selective inhibitors of the cancer associated carbonic anhydrase isoforms IX and XII. Riafrecha LE, Rodríguez OM, Vullo D, Supuran CT, Colinas PA. Bioorg Med Chem 22 5308-5314 (2014)
  39. Crystal structure of the human carbonic anhydrase II adduct with 1-(4-sulfamoylphenyl-ethyl)-2,4,6-triphenylpyridinium perchlorate, a membrane-impermeant, isoform selective inhibitor. Alterio V, Esposito D, Monti SM, Supuran CT, De Simone G. J Enzyme Inhib Med Chem 33 151-157 (2018)
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  43. Effect of Fermentation, Drying and Roasting on Biogenic Amines and Other Biocompounds in Colombian Criollo Cocoa Beans and Shells. Delgado-Ospina J, Di Mattia CD, Paparella A, Mastrocola D, Martuscelli M, Chaves-Lopez C. Foods 9 E520 (2020)
  44. Synthesis and carbonic anhydrase inhibitory properties of amino acid - coumarin/quinolinone conjugates incorporating glycine, alanine and phenylalanine moieties. Küçükbay FZ, Küçükbay H, Tanc M, Supuran CT. J Enzyme Inhib Med Chem 31 1198-1202 (2016)
  45. Interactions of natural polyamines with mammalian proteins. Schuster I, Bernhardt R. Biomol Concepts 2 79-94 (2011)
  46. Sulfocoumarin-, Coumarin-, 4-Sulfamoylphenyl-Bearing Indazole-3-carboxamide Hybrids: Synthesis and Selective Inhibition of Tumor-Associated Carbonic Anhydrase Isozymes IX and XII. Angapelly S, Sri Ramya PV, Angeli A, Supuran CT, Arifuddin M. ChemMedChem 12 1578-1584 (2017)
  47. Sulphonamide inhibition studies of the β-carbonic anhydrase from the bacterial pathogen Clostridium perfringens. Vullo D, Kumar RSS, Scozzafava A, Ferry JG, Supuran CT. J Enzyme Inhib Med Chem 33 31-36 (2018)
  48. Synthesis of sulfonamides incorporating piperazinyl-ureido moieties and their carbonic anhydrase I, II, IX and XII inhibitory activity. Congiu C, Onnis V, Deplano A, Balboni G, Dedeoglu N, Supuran CT. Bioorg Med Chem Lett 25 3850-3853 (2015)
  49. Superacid synthesized tertiary benzenesulfonamides and benzofuzed sultams act as selective hCA IX inhibitors: toward understanding a new mode of inhibition by tertiary sulfonamides. Métayer B, Martin-Mingot A, Vullo D, Supuran CT, Thibaudeau S. Org Biomol Chem 11 7540-7549 (2013)
  50. 5-Substituted-benzylsulfanyl-thiophene-2-sulfonamides with effective carbonic anhydrase inhibitory activity: Solution and crystallographic investigations. Ivanova J, Balode A, Žalubovskis R, Leitans J, Kazaks A, Vullo D, Tars K, Supuran CT. Bioorg Med Chem 25 857-863 (2017)
  51. Coumarins and other fused bicyclic heterocycles with selective tumor-associated carbonic anhydrase isoforms inhibitory activity. Bozdag M, Alafeefy AM, Altamimi AM, Vullo D, Carta F, Supuran CT. Bioorg Med Chem 25 677-683 (2017)
  52. Sulfamide derivatives with selective carbonic anhydrase VII inhibitory action. Villalba ML, Palestro P, Ceruso M, Gonzalez Funes JL, Talevi A, Bruno Blanch L, Supuran CT, Gavernet L. Bioorg Med Chem 24 894-901 (2016)
  53. Sulfonamide inhibition studies of the β carbonic anhydrase from Drosophila melanogaster. Syrjänen L, Parkkila S, Scozzafava A, Supuran CT. Bioorg Med Chem Lett 24 2797-2801 (2014)
  54. Synthesis of novel acridine bis-sulfonamides with effective inhibitory activity against the carbonic anhydrase isoforms I, II, IX and XII. Esirden İ, Ulus R, Aday B, Tanç M, Supuran CT, Kaya M. Bioorg Med Chem 23 6573-6580 (2015)
  55. Dendrimers incorporating benzenesulfonamide moieties strongly inhibit carbonic anhydrase isoforms I-XIV. Carta F, Osman SM, Vullo D, AlOthman Z, Supuran CT. Org Biomol Chem 13 6453-6457 (2015)
  56. Natural product hybrid and its superacid synthesized analogues: dodoneine and its derivatives show selective inhibition of carbonic anhydrase isoforms I, III, XIII and XIV. Carreyre H, Coustard JM, Carré G, Vandebrouck C, Bescond J, Ouédraogo M, Marrot J, Vullo D, Supuran CT, Thibaudeau S. Bioorg Med Chem 21 3790-3794 (2013)
  57. Quantitative Characterization of the Interaction Space of the Mammalian Carbonic Anhydrase Isoforms I, II, VII, IX, XII, and XIV and their Inhibitors, Using the Proteochemometric Approach. Rasti B, Karimi-Jafari MH, Ghasemi JB. Chem Biol Drug Des 88 341-353 (2016)
  58. A failed tentative to design a super carbonic anhydrase having the biochemical properties of the most thermostable CA (SspCA) and the fastest (SazCA) enzymes. De Luca V, Del Prete S, Carginale V, Vullo D, Supuran CT, Capasso C. J Enzyme Inhib Med Chem 30 989-994 (2015)
  59. An update on anticancer drug development and delivery targeting carbonic anhydrase IX. Kazokaitė J, Aspatwar A, Parkkila S, Matulis D. PeerJ 5 e4068 (2017)
  60. Heterologous expression and biochemical characterisation of the recombinant β-carbonic anhydrase (MpaCA) from the warm-blooded vertebrate pathogen malassezia pachydermatis. De Luca V, Angeli A, Mazzone V, Adelfio C, Carginale V, Scaloni A, Carta F, Selleri S, Supuran CT, Capasso C. J Enzyme Inhib Med Chem 37 62-68 (2022)
  61. May Sulfonamide Inhibitors of Carbonic Anhydrases from Mammaliicoccus sciuri Prevent Antimicrobial Resistance Due to Gene Transfer to Other Harmful Staphylococci? De Luca V, Giovannuzzi S, Supuran CT, Capasso C. Int J Mol Sci 23 13827 (2022)
  62. Hydroxylamine-O-sulfonamide is a versatile lead compound for the development of carbonic anhydrase inhibitors. Di Fiore A, Vergara A, Caterino M, Alterio V, Monti SM, Ombouma J, Dumy P, Vullo D, Supuran CT, Winum JY, De Simone G. Chem Commun (Camb) 51 11519-11522 (2015)
  63. Salicylaldoxime derivatives as new leads for the development of carbonic anhydrase inhibitors. Tuccinardi T, Bertini S, Granchi C, Ortore G, Macchia M, Minutolo F, Martinelli A, Supuran CT. Bioorg Med Chem 21 1511-1515 (2013)
  64. Synthesis, characterization and carbonic anhydrase inhibitory activity of novel benzothiazole derivatives. Küçükbay FZ, Buğday N, Küçükbay H, Tanc M, Supuran CT. J Enzyme Inhib Med Chem 31 1221-1225 (2016)
  65. Interview A Key Opinion Leader interview: insight into the research and career of Prof. Claudiu T Supuran. Supuran CT, Palmer C. Expert Opin Ther Pat 25 501-505 (2015)
  66. Proteochemometric Modeling of the Interaction Space of Carbonic Anhydrase and its Inhibitors: An Assessment of Structure-based and Sequence-based Descriptors. Rasti B, Namazi M, Karimi-Jafari MH, Ghasemi JB. Mol Inform 36 (2017)
  67. Synthesis and evaluation of sulfonamide-bearing thiazole as carbonic anhydrase isoforms hCA I and hCA II. Kılıcaslan S, Arslan M, Ruya Z, Bilen Ç, Ergün A, Gençer N, Arslan O. J Enzyme Inhib Med Chem 31 1300-1305 (2016)
  68. Biochemical, structural, and computational studies of a γ-carbonic anhydrase from the pathogenic bacterium Burkholderia pseudomallei. Di Fiore A, De Luca V, Langella E, Nocentini A, Buonanno M, Monti SM, Supuran CT, Capasso C, De Simone G. Comput Struct Biotechnol J 20 4185-4194 (2022)
  69. Inhibitory Effects of Sulfonamide Derivatives on the β-Carbonic Anhydrase (MpaCA) from Malassezia pachydermatis, a Commensal, Pathogenic Fungus Present in Domestic Animals. De Luca V, Angeli A, Mazzone V, Adelfio C, Carta F, Selleri S, Carginale V, Scaloni A, Supuran CT, Capasso C. Int J Mol Sci 22 12601 (2021)
  70. Synthesis and characterization of a proton transfer salt between 2,6-pyridinedicarboxylic acid and 2-aminobenzothiazole, and its complexes and their inhibition studies on carbonic anhydrase isoenzymes. İlkimen H, Yenikaya C, Sarı M, Bülbül M, Tunca E, Dal H. J Enzyme Inhib Med Chem 29 353-361 (2014)
  71. Synthesis and evaluation of N-heteroarylsubstituted triazolosulfonamides as carbonic anhydrase inhibitors. Balci A, Arslan M, Nixha AR, Bilen C, Ergun A, Gençer N. J Enzyme Inhib Med Chem 30 377-382 (2015)
  72. 2-Amino-3-cyanopyridine derivatives as carbonic anhydrase inhibitors. Ayvaz S, Çankaya M, Atasever A, Altuntas A. J Enzyme Inhib Med Chem 28 305-310 (2013)
  73. Mutation of active site residues Asn67 to Ile, Gln92 to Val and Leu204 to Ser in human carbonic anhydrase II: influences on the catalytic activity and affinity for inhibitors. Turkoglu S, Maresca A, Alper M, Kockar F, Işık S, Sinan S, Ozensoy O, Arslan O, Supuran CT. Bioorg Med Chem 20 2208-2213 (2012)
  74. Probing the chemical interaction space governed by 4-aminosubstituted benzenesulfonamides and carbonic anhydrase isoforms. Rasti B, Heravi YE. Res Pharm Sci 13 192-204 (2018)
  75. Synthesis and Biological Evaluation of Novel Aromatic Imide-Polyamine Conjugates. Li M, Wang Y, Zhang J, Xie S, Wang C, Wu Y. Molecules 21 E1637 (2016)
  76. Synthesis of saccharin-glycoconjugates targeting carbonic anhydrase using a one-pot cyclization/deprotection strategy. Murray AB, Quadri M, Li H, McKenna R, Horenstein NA. Carbohydr Res 476 65-70 (2019)
  77. Editorial Molecular targets of spermidine: implications for cancer suppression. Zimmermann A, Hofer SJ, Madeo F. Cell Stress 7 50-58 (2023)
  78. Sulfonamide inhibition studies of the α-carbonic anhydrase from the gammaproteobacterium Thiomicrospira crunogena XCL-2, TcruCA. Vullo D, Bhatt A, Mahon BP, McKenna R, Supuran CT. Bioorg Med Chem Lett 26 401-405 (2016)
  79. Synthesis and biological evaluation of new 3-substituted coumarin derivatives as selective inhibitors of human carbonic anhydrase IX and XII. Mahammad Ghouse S, Bahatam K, Angeli A, Pawar G, Chinchilli KK, Yaddanapudi VM, Mohammed A, Supuran CT, Nanduri S. J Enzyme Inhib Med Chem 38 2185760 (2023)
  80. Synthesis and carbonic anhydrase inhibitory properties of new spiroindoline-substituted sulphonamide compounds. Güleç Ö, Arslan M, Gencer N, Ergun A, Bilen C, Arslan O. Arch Physiol Biochem 123 306-312 (2017)


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