Discovery of novel drugs for Chagas disease: is carbonic anhydrase a target for antiprotozoal drugs?

References

• WHO. Neglected tropical diseases. 2021 [cited 2022 Feb 15]. Available from: https://www.who.int/news-room/questions-and-answers/item/neglected-tropical-diseases
   Google Scholar
• Horn D. A profile of research on the parasitic trypanosomatids and the diseases they cause. Buscaglia CA, editor. PLoS Negl Trop Dis. 2022;16(1):e0010040.
   PubMedGoogle Scholar
• Gomes C, Almeida AB, Rosa AC, et al. American trypanosomiasis and Chagas disease: sexual transmission. Inter J Infect Dis. 2019;81:81–84.
   PubMed Web of Science ®Google Scholar
• Vermelho AB, Rodrigues GC, Supuran CT. Why hasn’t there been more progress in new Chagas disease drug discovery? Expert Opin Drug Discov. 2020;15(2):145–158.
   PubMed Web of Science ®Google Scholar
• Zheng C, Quintero O, Revere EK, et al. Chagas disease in the New York city metropolitan area. Open Forum Infect Dis. 2020;7(5):ofaa156.
   PubMed Web of Science ®Google Scholar
• Zaidel EJ, Forsyth CJ, Novick G, et al. COVID-19: implications for people with Chagas disease. Glob Heart. 2020;15(1):69.
   PubMed Web of Science ®Google Scholar
• Alonso-Padilla J, Abril M, Alarcón de Noya B, et al. Target product profile for a test for the early assessment of treatment efficacy in Chagas disease patients: an expert consensus. Santiago H da C, editor. PLoS Negl Trop Dis. 2020;14(4):e0008035.
   PubMed Web of Science ®Google Scholar
• Cortes-Serra N, Losada-Galvan I, Pinazo M-J, et al. State-of-the-art in host-derived biomarkers of Chagas disease prognosis and early evaluation of anti-Trypanosoma cruzi treatment response. Biochim Biophys Acta (BBA) - Mol Basis Dis. 2020;1866(7):165758.
   PubMed Web of Science ®Google Scholar
• Echeverría LE, Marcus R, Novick G, et al. WHF IASC roadmap on Chagas disease. Glob Heart. 2020;15(1):26.
   PubMed Web of Science ®Google Scholar
• Lidani KCF, Andrade FA, Bavia L, et al. Chagas disease: from discovery to a worldwide health problem. Front Public Health. 2019;7:166 .
   PubMed Web of Science ®Google Scholar
• Martín-Escolano J, Medina-Carmona E, Martín-Escolano R. Chagas disease: current view of an ancient and global chemotherapy challenge. ACS Infect Dis. 2020;6(11):2830–2843.
   PubMed Web of Science ®Google Scholar
• Ruiz-Lancheros E, Chatelain E, Ndao M. Chagas disease treatment efficacy biomarkers: myths and realities. In: Altcheh JM, Freilij H, editors. Chagas disease [Internet]. Cham: Springer International Publishing; 2019. p. 323–349 [cited 2022 Jan 31] . Available from: http://link.springer.com/10.1007/978-3-030-00054-7_16
   Google Scholar
• de Souza ALADAG, Mesquita CT. Chagas disease - past and future. Int J Cardiovasc Sci. 2020;33(6):601–603.
   Google Scholar
• Vermelho AB, Cardoso V, Mansoldo FRP, et al. Chagas disease: drug development and parasite targets. Berlin (Heidelberg): Springer Berlin Heidelberg; 2022 [cited 2022 Feb 15]. Available from: https://link.springer.com/10.1007/7355_2021_143
   Google Scholar
• Beltran-Hortelano I, Alcolea V, Font M, et al. Examination of multiple Trypanosoma cruzi targets in a new drug discovery approach for Chagas disease. Bioorg Med Chem. 2022;58:116577. • A complete review about Trypanosoma cruzi targets.
   PubMed Web of Science ®Google Scholar
• Imran M, Khan SA, Alshammari MK, et al. Discovery, development, inventions and patent review of fexinidazole: the first all-oral therapy for human African trypanosomiasis. Pharmaceuticals. 2022;15(2):128.
   Web of Science ®Google Scholar
• Mansoldo FRP, Carta F, Angeli A, et al. Chagas disease: perspectives on the past and present and challenges in drug discovery. Molecules. 2020;25(22):5483.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Emerging role of carbonic anhydrase inhibitors. Clin Sci. 2021;135(10):1233–1249.
   PubMed Web of Science ®Google Scholar
• Vermelho AB, Capaci GR, Rodrigues IA, et al. Carbonic anhydrases from Trypanosoma and Leishmania as anti-protozoan drug targets. Bioorg Med Chem. 2017;25(5):1543–1555.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Osman SM, Rodrigues IA, et al. Appraisal of anti-protozoan activity of nitroaromatic benzenesulfonamides inhibiting carbonic anhydrases from Trypanosoma cruzi and Leishmania donovani. J Enzyme Inhib Med Chem. 2019;34(1):1164–1171.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Inhibition of carbonic anhydrase from Trypanosoma cruzi for the management of Chagas disease: an underexplored therapeutic opportunity. Future Med Chem. 2016;8(3):311–324. • An important review about carbonic anhydrase in Trypanosoma cruzi
   PubMed Web of Science ®Google Scholar
• Angeli A, Carta F, Nocentini A, et al. Carbonic anhydrase inhibitors targeting metabolism and tumor microenvironment. Metabolites. 2020;10(10):412.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. Bacterial, fungal and protozoan carbonic anhydrases as drug targets. Expert Opin Ther Targets. 2015;19(12):1689–1704.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Structure and function of carbonic anhydrases. Biochem J. 2016;473(14):2023–2032.
   PubMedGoogle Scholar
• Aspatwar A, Barker H, Tolvanen M, et al. Carbonic anhydrases from pathogens. Carbonic anhydrases [Internet]. Elsevier; 2019. p. 449–475. cited 2022 Jan 31. Available from: https://linkinghub.elsevier.com/retrieve/pii/B9780128164761000204
   Google Scholar
• Mishra CB, Tiwari M, Supuran CT. Progress in the development of human carbonic anhydrase inhibitors and their pharmacological applications: where are we today? Med Res Rev. 2020;40(6):2485–2565.
   PubMed Web of Science ®Google Scholar
• Bonardi A, Nocentini A, Bua S, et al. Sulfonamide inhibitors of human carbonic anhydrases designed through a three-tails approach: improving Ligand/Isoform matching and selectivity of action. J Med Chem. 2020;63(13):7422–7444.
   PubMed Web of Science ®Google Scholar
• Llanos MA, Sbaraglini ML, Villalba ML, et al. A structure-based approach towards the identification of novel antichagasic compounds: Trypanosoma cruzi carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem. 2020;35(1):21–30.
   PubMed Web of Science ®Google Scholar
• Pan P, Vermelho AB, Capaci Rodrigues G, et al. Cloning, characterization, and sulfonamide and thiol inhibition studies of an α-carbonic anhydrase from Trypanosoma cruzi, the causative agent of Chagas disease. J Med Chem. 2013;56(4):1761–1771 •• Discovery of an α-carbonic anhydrase in Trypanosoma cruzi .
   PubMed Web of Science ®Google Scholar
• Bhattacharya A, Corbeil A, Do Monte-Neto RL, et al. Of drugs and trypanosomatids: new tools and knowledge to reduce bottlenecks in drug discovery. Genes (Basel). 2020;11(7):722.
   PubMed Web of Science ®Google Scholar
• D’Ambrosio K, Supuran CT, De Simone G. Are carbonic anhydrases suitable targets to fight protozoan parasitic diseases? CMC. 2019;25(39):5266–5278.
   Google Scholar
• Urbański LJ, Angeli A, Mykuliak VV, et al. Biochemical and structural characterization of beta-carbonic anhydrase from the parasite Trichomonas vaginalis. J Mol Med. 2022;100(1):115–124.
   PubMed Web of Science ®Google Scholar
• Ceruso M, Carta F, Osman SM, et al. Inhibition studies of bacterial, fungal and protozoan β-class carbonic anhydrases with Schiff bases incorporating sulfonamide moieties. Bioorg Med Chem. 2015;23(15):4181–4187.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Di Fiore A, Parkkila S, et al. Beta-carbonic anhydrase 1 from Trichomonas vaginalis as new antiprotozoan drug target. Berlin (Heidelberg): Springer Berlin Heidelberg. p. 1–14.
   Google Scholar
• Syrjänen L, Vermelho AB, de Almeida Rodrigues I, et al. Cloning, characterization, and inhibition studies of a β-carbonic anhydrase from Leishmania donovani chagasi, the protozoan parasite responsible for leishmaniasis. J Med Chem. 2013;56(18):7372–7381.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Capasso C. Protozoan Carbonic Anhydrases. In: Supuran CT, Capasso C, editors. Zinc enzyme inhibitors [Internet]. Cham: Springer International Publishing; 2016. p. 111–133. cited 2022 Jan 9. Available from: http://link.springer.com/10.1007/7355_2016_11
   Google Scholar
• 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(18):4389–4396.
   PubMed Web of Science ®Google Scholar
• Hirakawa Y, Senda M, Fukuda K, et al. Characterization of a novel type of carbonic anhydrase that acts without metal cofactors. BMC Biol. 2021;19(1):105.
   PubMed Web of Science ®Google Scholar
• Annunziato G, Giovati L, Angeli A, et al. Discovering a new class of antifungal agents that selectively inhibits microbial carbonic anhydrases. J Enzyme Inhib Med Chem. 2018;33(1):1537–1544.
   PubMed Web of Science ®Google Scholar
• Pander B, Harris G, Scott DJ, et al. The carbonic anhydrase of Clostridium autoethanogenum represents a new subclass of β-carbonic anhydrases. Appl Microbiol Biotechnol. 2019;103(17):7275–7286.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Nocentini A, Supuran CT, et al. Bacterial ι-carbonic anhydrase: a new active class of carbonic anhydrase identified in the genome of the Gram-negative bacterium Burkholderia territorii. J Enzyme Inhib Med Chem. 2020;35(1):1060–1068.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Capasso C. Antibacterial carbonic anhydrase inhibitors: an update on the recent literature. Expert Opin Ther Pat. 2020;30(12):963–982.
   PubMed Web of Science ®Google Scholar
• Reungprapavut S, Krungkrai SR, Krungkrai J. Plasmodium falciparum carbonic anhydrase is a possible target for malaria chemotherapy. J Enzyme Inhib Med Chem. 2004;19(3):249–256.
   PubMed Web of Science ®Google Scholar
• Giovannuzzi S, De Luca V, Nocentini A, et al. Coumarins inhibit η-class carbonic anhydrase from Plasmodium falciparum. J Enzyme Inhib Med Chem. 2022;37(1):680–685.
   PubMed Web of Science ®Google Scholar
• Bua S, Haapanen S, Kuuslahti M, et al. Sulfonamide inhibition studies of a new β-carbonic anhydrase from the pathogenic protozoan Entamoeba histolytica. IJMS. 2018;19(12):3946.
   Google Scholar
• Alterio V, Kellner M, Esposito D, et al. Biochemical and structural insights into carbonic anhydrase XII/Fab6A10 complex. J Mol Biol. 2019;431(24):4910–4921.
   PubMed Web of Science ®Google Scholar
• McDonald PC, Chia S, Bedard PL, et al. A phase 1 study of SLC-0111, a novel inhibitor of carbonic anhydrase IX, in patients with advanced solid tumors. Am J Clin Oncol. 2020;43(7):484–490.
   PubMed Web of Science ®Google Scholar
• Testa C, Papini AM, Zeidler R, et al. First studies on tumor associated carbonic anhydrases IX and XII monoclonal antibodies conjugated to small molecule inhibitors. J Enzyme Inhib Med Chem. 2022;37(1):592–596.
   PubMed Web of Science ®Google Scholar
• Buabeng ER, Henary M. Developments of small molecules as inhibitors for carbonic anhydrase isoforms. Bioorg Med Chem. 2021;39:116140.
   PubMed Web of Science ®Google Scholar
• Abdelrahman MA, Ibrahim HS, Nocentini A, et al. Novel 3-substituted coumarins as selective human carbonic anhydrase IX and XII inhibitors: synthesis, biological and molecular dynamics analysis. Eur J Med Chem. 2021;209:112897.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Angeli A, Carta F, et al. Reconsidering anion inhibitors in the general context of drug design studies of modulators of activity of the classical enzyme carbonic anhydrase. J Enzyme Inhib Med Chem. 2021;36(1):561–580.
   PubMed Web of Science ®Google Scholar
• Supuran C, Vullo D, Manole G, et al. Designing of novel carbonic anhydrase inhibitors and activators. CMCCHA. 2004;2(1):49–68.
   Google Scholar
• Mishra CB, Kumari S, Angeli A, et al. Discovery of potent carbonic anhydrase inhibitors as effective anticonvulsant agents: drug design, synthesis, and in vitro and in vivo investigations. J Med Chem. 2021;64(6):3100–3114.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov. 2008;7(2):168–181.
   PubMed Web of Science ®Google Scholar
• McKenna R, Supuran CT. Carbonic anhydrase inhibitors drug design. In: Frost SC, McKenna R, editors. Carbonic anhydrase: mechanism, regulation, links to disease, and industrial applications [Internet]. Dordrecht: Springer Netherlands; 2014. p. 291–323. cited 2022 Jan 5. Available from: http://link.springer.com/10.1007/978-94-007-7359-2_15
   Google Scholar
• Supuran C, Scozzafava A. Carbonic anhydrase inhibitors. CMCIEMA. 2001;1(1):61–97.
   Google Scholar
• Berrino E, Supuran CT. Novel approaches for designing drugs that interfere with pH regulation. Expert Opin Drug Discov. 2019;14(3):231–248.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov. 2017;12(1):61–88.
   PubMed Web of Science ®Google Scholar
• Tugrak M, Gul HI, Demir Y, et al. Synthesis of benzamide derivatives with thiourea‐substituted benzenesulfonamides as carbonic anhydrase inhibitors. Arch Pharm. 2021;354(2):2000230.
   Web of Science ®Google Scholar
• Tanpure RP, Ren B, Peat TS, et al. Carbonic anhydrase inhibitors with dual-tail moieties to match the hydrophobic and hydrophilic halves of the carbonic anhydrase active site. J Med Chem. 2015;58(3):1494–1501.
   PubMed Web of Science ®Google Scholar
• Manzoor S, Petreni A, Raza MK, et al. Novel triazole-sulfonamide bearing pyrimidine moieties with carbonic anhydrase inhibitory action: design, synthesis, computational and enzyme inhibition studies. Bioorg Med Chem Lett. 2021;48:128249.
   PubMed Web of Science ®Google Scholar
• Pala N, Micheletto L, Sechi M, et al. Carbonic anhydrase inhibition with benzenesulfonamides and tetrafluorobenzenesulfonamides obtained via click chemistry. ACS Med Chem Lett. 2014;5(8):927–930.
   PubMed Web of Science ®Google Scholar
• Pereira D, Pinto M, Correia-da-Silva M, et al. Recent advances in bioactive flavonoid hybrids linked by 1,2,3-triazole ring obtained by click chemistry. Molecules. 2021;27(1):230.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Vermelho AB, Supuran CT. Targeting carbonic anhydrases from Trypanosoma cruzi and Leishmania spp. as a therapeutic strategy to obtain new antiprotozoal drugs. Berlin (Heidelberg): Springer Berlin Heidelberg; 2021. [cited 2022 Jan 31]. Available from. https://link.springer.com/10.1007/7355_2021_140
   Google Scholar
• Supuran CT. Multitargeting approaches involving carbonic anhydrase inhibitors: hybrid drugs against a variety of disorders. J Enzyme Inhib Med Chem. 2021;36(1):1702–1714.
   PubMed Web of Science ®Google Scholar
• Güzel-Akdemir Ö, Akdemir A, Pan P, et al. A class of sulfonamides with strong inhibitory action against the α-carbonic anhydrase from Trypanosoma cruzi. J Med Chem. 2013;56(14):5773–5781.
   PubMed Web of Science ®Google Scholar
• Vermelho AB, da Silva Cardoso V, Ricci Junior E, et al. Nanoemulsions of sulfonamide carbonic anhydrase inhibitors strongly inhibit the growth of Trypanosoma cruzi. J Enzyme Inhib Med Chem. 2018;33(1):139–146.
   PubMed Web of Science ®Google Scholar
• da Silva Cardoso V, Vermelho AB, Ricci Junior E, et al. Antileishmanial activity of sulphonamide nanoemulsions targeting the β-carbonic anhydrase from Leishmania species. J Enzyme Inhib Med Chem. 2018;33(1):850–857.
   PubMed Web of Science ®Google Scholar
• Benediktsdottir A, Lu L, Cao S, et al. Antibacterial sulfonimidamide-based oligopeptides as type I signal peptidase inhibitors: synthesis and biological evaluation. Eur J Med Chem. 2021;224:113699.
   PubMed Web of Science ®Google Scholar
• Bredael K, Geurs S, Clarisse D, et al. Carboxylic acid bioisosteres in medicinal chemistry: synthesis and properties. Trabocchi A, editor. J Chem. 2022;2022:1–21.
   Web of Science ®Google Scholar
• Lima LM, Barreiro EJ. Bioisosterism: a useful strategy for molecular modification and drug design. Curr Med Chem. 2005;12(1):23–49.
   PubMed Web of Science ®Google Scholar
• Patani GA, LaVoie EJ. Bioisosterism: a rational approach in drug design. Chem Rev. 1996;96(8):3147–3176.
   PubMed Web of Science ®Google Scholar
• Almalki AJ, Ibrahim TS, Taher ES, et al. Synthesis, antimicrobial, anti-virulence and anticancer evaluation of new 5(4H)-oxazolone-based sulfonamides. Molecules. 2022;27(3):671.
   PubMed Web of Science ®Google Scholar
• Shoaib Ahmad Shah S, Rivera G, Ashfaq M. Recent advances in medicinal chemistry of sulfonamides. rational design as anti-tumoral, anti-bacterial and anti-inflammatory agents. Mrmc. 2012;13(1):70–86.
   Google Scholar
• Maldonado E, Rojas DA, Urbina F, et al. The oxidative stress and chronic inflammatory process in Chagas disease: role of exosomes and contributing genetic factors. Ribeiro D, editor. Oxid Med Cell Longev. 2021;2021:1–21.
   Web of Science ®Google Scholar
• Providello MV, Carneiro ZA, Portapilla GB, et al. Benefits of ascorbic acid in association with low-dose benznidazole in treatment of Chagas disease. Antimicrob Agents Chemother. 2018;62(9):e00514–18.
   PubMed Web of Science ®Google Scholar
• de Santos ES, de Aragão-França LS, Meira CS, et al. Tolerogenic dendritic cells reduce cardiac inflammation and fibrosis in chronic Chagas disease. Front Immunol. 2020;11:488.
   PubMed Web of Science ®Google Scholar
• Imperador CHL, Scarim CB, Bosquesi PL, et al. Resveratrol and curcumin for Chagas disease treatment—a systematic review. Pharmaceuticals. 2022;15(5):609.
   Web of Science ®Google Scholar
• Angeli A, Pinteala M, Maier SS, et al. Inhibition of α-, β-, γ-, δ-, ζ- and η-class carbonic anhydrases from bacteria, fungi, algae, diatoms and protozoans with famotidine. J Enzyme Inhib Med Chem. 2019;34(1):644–650.
   PubMed Web of Science ®Google Scholar
• Alafeefy AM, Ceruso M, Al-Jaber NA, et al. A new class of quinazoline-sulfonamides acting as efficient inhibitors against the α-carbonic anhydrase from Trypanosoma cruzi. J Enzyme Inhib Med Chem. 2015;30(4):581–585.
   PubMed Web of Science ®Google Scholar
• Bonardi A, Vermelho AB, da Silva Cardoso V, et al. N -nitrosulfonamides as carbonic anhydrase inhibitors: a promising chemotype for targeting Chagas disease and leishmaniasis. ACS Med Chem Lett. 2019;10(4):413–418.
   PubMed Web of Science ®Google Scholar
• Carta F, Osman SM, Vullo D, et al. Poly(amidoamine) dendrimers show carbonic anhydrase inhibitory activity against α-, β-, γ- and η-class enzymes. Bioorg Med Chem. 2015;23(21):6794–6798.
   PubMed Web of Science ®Google Scholar
• Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem. 2016;31(3):345–360.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Supuran CT. Carbonic anhydrase inhibitors as antitumor/antimetastatic agents: a patent review (2008–2018). Expert Opin Ther Pat. 2018;28(10):729–740.
   PubMed Web of Science ®Google Scholar
• Rodrigues GC, Feijó DF, Bozza MT, et al. Design, synthesis, and evaluation of hydroxamic acid derivatives as promising agents for the management of Chagas disease. J Med Chem. 2014;57(2):298–308.
   PubMed Web of Science ®Google Scholar
• de Menezes DDR, Calvet CM, Rodrigues GC, et al. Hydroxamic acid derivatives: a promising scaffold for rational compound optimization in Chagas disease. J Enzyme Inhib Med Chem. 2016;31(6):964–973.
   PubMed Web of Science ®Google Scholar
• Pan P, Vermelho AB, Scozzafava A, et al. Anion inhibition studies of the α-carbonic anhydrase from the protozoan pathogen Trypanosoma cruzi, the causative agent of Chagas disease. Bioorg Med Chem. 2013;21(15):4472–4476.
   PubMed Web of Science ®Google Scholar
• Ratto F, Witort E, Tatini F, et al. Plasmonic particles that hit hypoxic cells. Adv Funct Mater. 2015;25(2):316–323.
   Web of Science ®Google Scholar
• Giovannuzzi S, Hewitt CS, Nocentini A, et al. Coumarins effectively inhibit bacterial α-carbonic anhydrases. J Enzyme Inhib Med Chem. 2022;37(1):333–338.
   PubMed Web of Science ®Google Scholar
• Pinheiro LCS, de Lourdes G, Ferreira M, et al. Synthetic compounds with sulfonamide moiety against Leishmaniasis: an overview. Med Chem Res. 2019;28(11):1807–1817.
   Web of Science ®Google Scholar
• Ovung A, Bhattacharyya J. Sulfonamide drugs: structure, antibacterial property, toxicity, and biophysical interactions. Biophys Rev. 2021;13(2):259–272.
   PubMedGoogle Scholar
• Angeli A, Donald WA, Parkkila S, et al. Activation studies with amines and amino acids of the β-carbonic anhydrase from the pathogenic protozoan Leishmania donovani chagasi. Bioorg Chem. 2018;78:406–410.
   PubMed Web of Science ®Google Scholar
• Das P, Dikhit MR, Purkait B, et al. Activity of a novel sulfonamide compound 2-nitro-N-(pyridin-2-ylmethyl)benzenesulfonamide against Leishmania donovani. DDDT. 2016;10:1753–17612.
   PubMed Web of Science ®Google Scholar
• Urbański LJ, Angeli A, Hytönen VP, et al. Inhibition of the newly discovered β‑carbonic anhydrase from the protozoan pathogen Trichomonas vaginalis with inorganic anions and small molecules. J Inorg Biochem. 2020;213:111274.
   PubMed Web of Science ®Google Scholar
• Alissa SA, Alghulikah HA, Alothman ZA, et al. Phosphonamidates are the first phosphorus-based zinc binding motif to show inhibition of β-class carbonic anhydrases from bacteria, fungi, and protozoa. J Enzyme Inhib Med Chem. 2020;35(1):59–64.
   PubMed Web of Science ®Google Scholar
• Fisher GM, Bua S, Del Prete S, et al. Investigating the antiplasmodial activity of primary sulfonamide compounds identified in open source malaria data. Int J Parasitol. 2017;7(1):61–70.
   Web of Science ®Google Scholar
• Krungkrai J, Krungkrai SR, Supuran CT. Carbonic anhydrase inhibitors: inhibition of Plasmodium falciparum carbonic anhydrase with aromatic/heterocyclic sulfonamides—in vitro and in vivo studies. Bioorg Med Chem Lett. 2008;18(20):5466–5471.
   PubMed Web of Science ®Google Scholar
• Kratz JM, Gonçalves KR, Romera LM, et al. The translational challenge in Chagas disease drug development. Mem Inst Oswaldo Cruz. 2022;117:e200501.
   PubMed Web of Science ®Google Scholar
• Ribeiro V, Dias N, Paiva T, et al. Current trends in the pharmacological management of Chagas disease. Int J Parasitol. 2020;12:7–17.
   Web of Science ®Google Scholar
• Vermelho AB, Mori M, Donald WA, et al. Challenges and promises for obtaining new antiprotozoal drugs: what’s going wrong? Berlin (Heidelberg): Springer Berlin Heidelberg; 2021 [cited 2022 Jun 12]. Available from: https://link.springer.com/10.1007/7355_2021_136
   Google Scholar
• DNDi. Research & development portfolio. 2022 [cited 2022 May 5]. Available from: https://dndi.org/research-development/portfolio
   Google Scholar