Advances in the Development of Carbonic Anhydrase Inhibitors as New Antiprotozoal Agents
- Authors: Ortiz-Perez E.1, Vazquez-Jimenez L.1, Paz-Gonzalez A.1, Delgado-Maldonado T.1, González-González A.1, Gaona-Lopez C.1, Moreno-Herrera A.1, Vazquez K.2, Rivera G.1
-
Affiliations:
- Laboratorio de Biotecnología Farmacéutica, Centro de Biotecnología Genómica, Instituto Politécnico Nacional
- Departamento de Biotecnología Farmacéutica, Facultad de Medicina Veterinaria y Zootecnia,, Universidad Autónoma de Nuevo León,
- Issue: Vol 31, No 41 (2024)
- Pages: 6735-6759
- Section: Anti-Infectives and Infectious Diseases
- URL: https://hum-ecol.ru/0929-8673/article/view/645138
- DOI: https://doi.org/10.2174/0109298673249553231018070920
- ID: 645138
Cite item
Full Text
Abstract
Background:Parasitic diseases are a public health problem despite the existence of drugs for their treatment. These treatments have variable efficacy and, in some cases, serious adverse effects. There has been interest in the enzyme carbonic anhydrase (CA) in the last two decades since it is essential in the life cycle of various parasites due to its important participation in processes such as pyrimidine synthesis, HCO3 - transport across cell membranes, and the maintenance of intracellular pH and ion transport (Na+, K+, and H+), among others.
Objective:In this review, CA was analyzed as a pharmacological target in etiological agents of malaria, American trypanosomiasis, leishmaniasis, amoebiasis, and trichomoniasis. The CA inhibitors´ design, binding mode, and structure-activity relationship are also discussed.
Conclusion:According to this review, advances in discovering compounds with potent inhibitory activity suggest that CA is a candidate for developing new antiprotozoal agents.
About the authors
Eyra Ortiz-Perez
Laboratorio de Biotecnología Farmacéutica, Centro de Biotecnología Genómica, Instituto Politécnico Nacional
Email: info@benthamscience.net
Lenci Vazquez-Jimenez
Laboratorio de Biotecnología Farmacéutica, Centro de Biotecnología Genómica, Instituto Politécnico Nacional
Email: info@benthamscience.net
Alma Paz-Gonzalez
Laboratorio de Biotecnología Farmacéutica, Centro de Biotecnología Genómica, Instituto Politécnico Nacional
Email: info@benthamscience.net
Timoteo Delgado-Maldonado
Laboratorio de Biotecnología Farmacéutica, Centro de Biotecnología Genómica, Instituto Politécnico Nacional
Email: info@benthamscience.net
Alonzo González-González
Laboratorio de Biotecnología Farmacéutica, Centro de Biotecnología Genómica, Instituto Politécnico Nacional
Email: info@benthamscience.net
Carlos Gaona-Lopez
Laboratorio de Biotecnología Farmacéutica, Centro de Biotecnología Genómica, Instituto Politécnico Nacional
Email: info@benthamscience.net
Antonio Moreno-Herrera
Laboratorio de Biotecnología Farmacéutica, Centro de Biotecnología Genómica, Instituto Politécnico Nacional
Email: info@benthamscience.net
Karina Vazquez
Departamento de Biotecnología Farmacéutica, Facultad de Medicina Veterinaria y Zootecnia,, Universidad Autónoma de Nuevo León,
Email: info@benthamscience.net
Gildardo Rivera
Laboratorio de Biotecnología Farmacéutica, Centro de Biotecnología Genómica, Instituto Politécnico Nacional
Author for correspondence.
Email: info@benthamscience.net
References
- Singh, B.; Varikuti, S.; Halsey, G.; Volpedo, G.; Hamza, O.M.; Satoskar, A.R. Host-directed therapies for parasitic diseases. Future Med. Chem., 2019, 11(15), 1999-2018. doi: 10.4155/fmc-2018-0439 PMID: 31390889
- Andargie, G.; Kassu, A.; Moges, F.; Tiruneh, M.; Huruy, K. Prevalence of bacteria and intestinal parasites among food-handlers in Gondar town, Northwest Ethiopia. J. Health Popul. Nutr., 2008, 26(4), 451-455. PMID: 19069624
- Robertson, L.J.; Sprong, H.; Ortega, Y.R.; van der Giessen, J.W.B.; Fayer, R. Impacts of globalisation on foodborne parasites. Trends Parasitol., 2014, 30(1), 37-52. doi: 10.1016/j.pt.2013.09.005 PMID: 24140284
- Dorny, P.; Praet, N.; Deckers, N.; Gabriël, S. Emerging food-borne parasites. Vet. Parasitol., 2009, 163(3), 196-206. doi: 10.1016/j.vetpar.2009.05.026 PMID: 19559535
- Pickles, R.S.A.; Thornton, D.; Feldman, R.; Marques, A.; Murray, D.L. Predicting shifts in parasite distribution with climate change: A multitrophic level approach. Glob. Change Biol., 2013, 19(9), 2645-2654. doi: 10.1111/gcb.12255 PMID: 23666800
- Altizer, S.; Ostfeld, R. S.; Johnson, P. T. J.; Kutz, S.; Harvell, C. D. Climate change and infectious diseases: From evidence to a predictive framework. Science (80-.), 2013, 341(6145), 514-519.
- Organization, W.H. Vector-borne Diseases; WHO Regional Office for South-east Asia, 2014.
- Torgerson, P.R. One world health: Socioeconomic burden and parasitic disease control priorities. Vet. Parasitol., 2013, 195(3-4), 223-232. doi: 10.1016/j.vetpar.2013.04.004 PMID: 23628712
- Beatriz Vermelho, A.; Rodrigues, G.C.; Nocentini, A.; Mansoldo, F.R.P.; Supuran, C.T. Discovery of novel drugs for Chagas disease: is carbonic anhydrase a target for antiprotozoal drugs? Expert Opin. Drug Discov., 2022, 17(10), 1147-1158. doi: 10.1080/17460441.2022.2117295 PMID: 36039500
- Pan, P.; Vermelho, A.B.; Scozzafava, A.; Parkkila, S.; Capasso, C.; Supuran, C.T. 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. doi: 10.1016/j.bmc.2013.05.058 PMID: 23790722
- Reungprapavut, S.; Krungkrai, S.R.; Krungkrai, J. Plasmodium falciparum carbonic anhydrase is a possible target for malaria chemotherapy. J. Enzyme Inhib. Med. Chem., 2004, 19(3), 249-256. doi: 10.1080/14756360410001689577 PMID: 15499996
- Ozensoy Guler, O.; Capasso, C.; Supuran, C.T. A magnificent enzyme superfamily: carbonic anhydrases, their purification and characterization. J. Enzyme Inhib. Med. Chem., 2016, 31(5), 689-694. doi: 10.3109/14756366.2015.1059333 PMID: 26118417
- Aspatwar, A.; Barker, H.; Tolvanen, M.; Emameh, R.Z.; Parkkila, S. Carbonic anhydrases from pathogens: protozoan cas and related inhibitors as potential antiprotozoal agents. In: Carbonic Anhydrases; Elsevier, 2019; pp. 449-475. doi: 10.1016/B978-0-12-816476-1.00020-4
- Capasso, C.; Supuran, C.T. Bacterial, fungal and protozoan carbonic anhydrases as drug targets. Expert Opin. Ther. Targets, 2015, 19(12), 1689-1704. doi: 10.1517/14728222.2015.1067685 PMID: 26235676
- Lomelino, C.L.; Andring, J.T.; McKenna, R. Crystallography and its impact on carbonic anhydrase research. Int. J. Med. Chem., 2018, 2018, 1-21. doi: 10.1155/2018/9419521 PMID: 30302289
- Capasso, C.; Supuran, C.T. Protozoan, fungal and bacterial carbonic anhydrases targeting for obtaining antiinfectives; Target. Carbon. anhydrases; London Futur. Sci. Ltd, 2014, pp. 133-141.
- Protein Data Bank Available from: https://www.rcsb.org/
- Supuran, C.T. Carbonic anhydrase inhibitors. Bioorg. Med. Chem. Lett., 2010, 20(12), 3467-3474. doi: 10.1016/j.bmcl.2010.05.009 PMID: 20529676
- Supuran, C.T.; Capasso, C. The η-class carbonic anhydrases as drug targets for antimalarial agents. Expert Opin. Ther. Targets, 2015, 19(4), 551-563. doi: 10.1517/14728222.2014.991312 PMID: 25495426
- Akocak, S.; Supuran, C.T. Activation of α-, β-, γ- δ-, ζ- and η- class of carbonic anhydrases with amines and amino acids: a review. J. Enzyme Inhib. Med. Chem., 2019, 34(1), 1652-1659. doi: 10.1080/14756366.2019.1664501 PMID: 31530034
- da Silva Cardoso, V.; Vermelho, A.B.; Ricci Junior, E.; Almeida Rodrigues, I.; Mazotto, A.M.; Supuran, C.T. Antileishmanial activity of sulphonamide nanoemulsions targeting the β -carbonic anhydrase from Leishmania species. J. Enzyme Inhib. Med. Chem., 2018, 33(1), 850-857. doi: 10.1080/14756366.2018.1463221 PMID: 29708476
- Llanos, M.A.; Sbaraglini, M.L.; Villalba, M.L.; Ruiz, M.D.; Carrillo, C.; Alba Soto, C.; Talevi, A.; Angeli, A.; Parkkila, S.; Supuran, C.T.; Gavernet, L. 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. doi: 10.1080/14756366.2019.1677638 PMID: 31619095
- Krungkrai, J.; Supuran, C. The alpha-carbonic anhydrase from the malaria parasite and its inhibition. Curr. Pharm. Des., 2008, 14(7), 631-640. doi: 10.2174/138161208783877901 PMID: 18336308
- Krungkrai, S.R.; Suraveratum, N.; Rochanakij, S.; Krungkrai, J. Characterisation of carbonic anhydrase in Plasmodium falciparum. Int. J. Parasitol., 2001, 31(7), 661-668. doi: 10.1016/S0020-7519(01)00172-2 PMID: 11336746
- Basu, S.; Sahi, P.K. Malaria: An update. Indian J. Pediatr., 2017, 84(7), 521-528. doi: 10.1007/s12098-017-2332-2 PMID: 28357581
- Krungkrai, S.R.; Krungkrai, J. Malaria parasite carbonic anhydrase: inhibition of aromatic/heterocyclic sulfonamides and its therapeutic potential. Asian Pac. J. Trop. Biomed., 2011, 1(3), 233-242. doi: 10.1016/S2221-1691(11)60034-8 PMID: 23569766
- World Health Organization. Available from: https://www. who.int/es/news-room/fact-sheets/detail/chagas-disease-(american-trypanosomiasis) (Accessed on: 2022-02-03).
- NTD. World Health Organization. Available from: https://www.who.int/ (Accessed on: 2022-02-23).
- DrugBank. Available from: https://go.drugbank.com/ (Accessed on: 2021-02-03).
- Vullo, D.; Del Prete, S.; Fisher, G.M.; Andrews, K.T.; Poulsen, S.A.; Capasso, C.; Supuran, C.T. Sulfonamide inhibition studies of the η-class carbonic anhydrase from the malaria pathogen Plasmodium falciparum. Bioorg. Med. Chem., 2015, 23(3), 526-531. doi: 10.1016/j.bmc.2014.12.009 PMID: 25533402
- Frampton, J.E. Tafenoquine: First global approval. Drugs, 2018, 78(14), 1517-1523. doi: 10.1007/s40265-018-0979-2 PMID: 30229442
- Adebayo, J.O.; Tijjani, H.; Adegunloye, A.P.; Ishola, A.A.; Balogun, E.A.; Malomo, S.O. Enhancing the antimalarial activity of artesunate. Parasitol. Res., 2020, 119(9), 2749-2764. doi: 10.1007/s00436-020-06786-1 PMID: 32638101
- Duffy, P.E.; Patrick Gorres, J. Malaria Vaccines since 2000: Progress, priorities, products. NPJ. Vaccines (Basel), 2020, 5(1), 48. PMID: 32012760
- Del Prete, S.; Vullo, D.; Fisher, G.M.; Andrews, K.T.; Poulsen, S.A.; Capasso, C.; Supuran, C.T. 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. doi: 10.1016/j.bmcl.2014.08.015 PMID: 25168745
- Krungkrai, J.; Krungkrai, S.; Supuran, C. Malarial parasite carbonic anhydrase and its inhibitors. Curr. Top. Med. Chem., 2007, 7(9), 909-917. doi: 10.2174/156802607780636744 PMID: 17504136
- Del Prete, S.; Vullo, D.; De Luca, V.; Carginale, V.; di Fonzo, P.; Osman, S.M.; AlOthman, Z.; Supuran, C.T.; Capasso, C. Anion inhibition profiles of the complete domain of the η-carbonic anhydrase from Plasmodium falciparum. Bioorg. Med. Chem., 2016, 24(18), 4410-4414. doi: 10.1016/j.bmc.2016.07.034 PMID: 27480028
- Del Prete, S.; Vullo, D.; De Luca, V.; Carginale, V.; Osman, S.M.; Alothman, Z.; Supuran, C.T.; Capasso, C. Cloning, expression, purification and sulfonamide inhibition profile of the complete domain of the η-carbonic anhydrase from Plasmodium falciparum. Bioorg. Med. Chem. Lett., 2016, 26(17), 4184-4190. doi: 10.1016/j.bmcl.2016.07.060 PMID: 27485387
- Giovannuzzi, S.; De Luca, V.; Nocentini, A.; Capasso, C.; Supuran, C.T. Coumarins inhibit η-class carbonic anhydrase from Plasmodium falciparum. J. Enzyme Inhib. Med. Chem., 2022, 37(1), 680-685. doi: 10.1080/14756366.2022.2036986 PMID: 35139744
- Rodrigues, G.C.; Feijó, D.F.; Bozza, M.T.; Pan, P.; Vullo, D.; Parkkila, S.; Supuran, C.T.; Capasso, C.; Aguiar, A.P.; Vermelho, A.B. 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. doi: 10.1021/jm400902y PMID: 24299463
- Pan, P.; Vermelho, A.B.; Capaci Rodrigues, G.; Scozzafava, A.; Tolvanen, M.E.E.; Parkkila, S.; Capasso, C.; Supuran, C.T. 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. doi: 10.1021/jm4000616 PMID: 23391336
- Robertson, L.J.; Devleesschauwer, B.; Alarcón de Noya, B.; Noya González, O.; Torgerson, P.R. Trypanosoma cruzi: Time for international recognition as a foodborne parasite. PLoS Negl. Trop. Dis., 2016, 10(6), e0004656. doi: 10.1371/journal.pntd.0004656 PMID: 27253136
- Echavarría, N.G.; Echeverría, L.E.; Stewart, M.; Gallego, C.; Saldarriaga, C. Chagas disease: Chronic chagas cardiomyopathy. Curr. Probl. Cardiol., 2021, 46(3), 100507. doi: 10.1016/j.cpcardiol.2019.100507 PMID: 31983471
- Güzel-Akdemir, Ö.; Akdemir, A.; Pan, P.; Vermelho, A.B.; Parkkila, S.; Scozzafava, A.; Capasso, C.; Supuran, C.T. A class of sulfonamides with strong inhibitory action against the α-carbonic anhydrase from Trypanosoma cruzi. J. Med. Chem., 2013, 56(14), 5773-5781. doi: 10.1021/jm400418p PMID: 23815159
- Ribeiro, V.; Dias, N.; Paiva, T.; Hagström-Bex, L.; Nitz, N.; Pratesi, R.; Hecht, M. Current trends in the pharmacological management of Chagas disease. Int. J. Parasitol. Drugs Drug Resist., 2020, 12, 7-17. doi: 10.1016/j.ijpddr.2019.11.004 PMID: 31862616
- Campos, M.C.O.; Leon, L.L.; Taylor, M.C.; Kelly, J.M. Benznidazole-resistance in Trypanosoma cruzi: Evidence that distinct mechanisms can act in concert. Mol. Biochem. Parasitol., 2014, 193(1), 17-19. doi: 10.1016/j.molbiopara.2014.01.002 PMID: 24462750
- Mejia, A.M.; Hall, B.S.; Taylor, M.C.; Gómez-Palacio, A.; Wilkinson, S.R.; Triana-Chávez, O.; Kelly, J.M. Benznidazole-resistance in Trypanosoma cruzi is a readily acquired trait that can arise independently in a single population. J. Infect. Dis., 2012, 206(2), 220-228. doi: 10.1093/infdis/jis331 PMID: 22551809
- Adasme, M.F.; Bolz, S.N.; Adelmann, L.; Salentin, S.; Haupt, V.J.; Moreno-Rodríguez, A.; Nogueda-Torres, B.; Castillo-Campos, V.; Yepez-Mulia, L.; De Fuentes-Vicente, J.A.; Rivera, G.; Schroeder, M. Repositioned drugs for chagas disease unveiled via structure-based drug repositioning. Int. J. Mol. Sci., 2020, 21(22), 8809. doi: 10.3390/ijms21228809 PMID: 33233837
- Vázquez-Jiménez, L.K.; Moreno-Herrera, A.; Juárez-Saldivar, A.; González-González, A.; Ortiz-Pérez, E.; Paz-González, A.D.; Palos, I.; Ramírez-Moreno, E.; Rivera, G. Recent advances in the development of triose phosphate isomerase inhibitors as antiprotozoal agents. Curr. Med. Chem., 2022, 29(14), 2504-2529. doi: 10.2174/0929867328666210913090928 PMID: 34517794
- Lara-Ramirez, E.E.; López-Cedillo, J.C.; Nogueda-Torres, B.; Kashif, M.; Garcia-Perez, C.; Bocanegra-Garcia, V.; Agusti, R.; Uhrig, M.L.; Rivera, G. An in vitro and in vivo evaluation of new potential trans -sialidase inhibitors of Trypanosoma cruzi predicted by a computational drug repositioning method. Eur. J. Med. Chem., 2017, 132, 249-261. doi: 10.1016/j.ejmech.2017.03.063 PMID: 28364659
- Vázquez-Jiménez, L.K.; Paz-González, A.D.; Juárez-Saldivar, A.; Uhrig, M.L.; Agusti, R.; Reyes-Arellano, A.; Nogueda-Torres, B.; Rivera, G. Structure-based virtual screening of new benzoic acid derivatives as Trypanosoma cruzi trans-sialidase inhibitors. Med. Chem., 2021, 17(7), 724-731. doi: 10.2174/1573406416666200506084611 PMID: 32370720
- Palos, I.; Lara-Ramirez, E.E.; Lopez-Cedillo, J.C.; Garcia-Perez, C.; Kashif, M.; Bocanegra-Garcia, V.; Nogueda-Torres, B.; Rivera, G. Repositioning FDA drugs as potential cruzain inhibitors from Trypanosoma cruzi: virtual screening, in vitro and in vivo studies. Molecules, 2017, 22(6), 1015. doi: 10.3390/molecules22061015 PMID: 28629155
- Herrera-Mayorga, V.; Lara-Ramírez, E.; Chacón-Vargas, K.; Aguirre-Alvarado, C.; Rodríguez-Páez, L.; Alcántara-Farfán, V.; Cordero-Martínez, J.; Nogueda-Torres, B.; Reyes-Espinosa, F.; Bocanegra-García, V.; Rivera, G. Structure-based virtual screening and in vitro evaluation of new Trypanosoma cruzi cruzain inhibitors. Int. J. Mol. Sci., 2019, 20(7), 1742. doi: 10.3390/ijms20071742 PMID: 30970549
- Juárez-Saldivar, A.; Schroeder, M.; Salentin, S.; Haupt, V.J.; Saavedra, E.; Vázquez, C.; Reyes-Espinosa, F.; Herrera-Mayorga, V.; Villalobos-Rocha, J.C.; García-Pérez, C.A.; Campillo, N.E.; Rivera, G. Computational drug repositioning for chagas disease using protein-ligand interaction profiling. Int. J. Mol. Sci., 2020, 21(12), 4270. doi: 10.3390/ijms21124270 PMID: 32560043
- Yepes, A.F.; Quintero-Saumeth, J.; Cardona-Galeano, W. Biologically active quinoline-hydrazone conjugates as potential Trypanosoma cruzi DHFR-TS inhibitors: Docking, molecular dynamics, MM/PBSA and drug-likeness studies. Chem. Select, 2021, 6(12), 2928-2938. doi: 10.1002/slct.202100238
- Espinosa-Bustos, C.; Ortiz Pérez, M.; Gonzalez-Gonzalez, A.; Zarate, A.M.; Rivera, G.; Belmont-Díaz, J.A.; Saavedra, E.; Cuellar, M.A.; Vázquez, K.; Salas, C.O. New amino naphthoquinone derivatives as anti-trypanosoma cruzi agents targeting trypanothione reductase. Pharmaceutics, 2022, 14(6), 1121. doi: 10.3390/pharmaceutics14061121 PMID: 35745694
- Battista, T.; Colotti, G.; Ilari, A.; Fiorillo, A. Targeting trypanothione reductase, a key enzyme in the redox trypanosomatid metabolism, to develop new drugs against leishmaniasis and trypanosomiases. Molecules, 2020, 25(8), 1924. doi: 10.3390/molecules25081924 PMID: 32326257
- Mansoldo, F.R.P.; Carta, F.; Angeli, A.; Cardoso, V.S.; Supuran, C.T.; Vermelho, A.B. Chagas disease: Perspectives on the past and present and challenges in drug discovery. Molecules, 2020, 25(22), 5483. doi: 10.3390/molecules25225483 PMID: 33238613
- Nocentini, A.; Cadoni, R.; Dumy, P.; Supuran, C.T.; Winum, J.Y. Carbonic anhydrases from Trypanosoma cruzi and Leishmania donovani chagasi are inhibited by benzoxaboroles. J. Enzyme Inhib. Med. Chem., 2018, 33(1), 286-289. doi: 10.1080/14756366.2017.1414808 PMID: 29278948
- Supuran, C.T. 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. doi: 10.4155/fmc.15.185 PMID: 26898220
- Winum, J.Y.; Supuran, C.T. Recent advances in the discovery of zinc-binding motifs for the development of carbonic anhydrase inhibitors. J. Enzyme Inhib. Med. Chem., 2015, 30(2), 321-324. doi: 10.3109/14756366.2014.913587 PMID: 24939097
- Vermelho, A.B.; da Silva Cardoso, V.; Ricci Junior, E.; dos Santos, E.P.; Supuran, C.T. Nanoemulsions of sulfonamide carbonic anhydrase inhibitors strongly inhibit the growth of Trypanosoma cruzi. J. Enzyme Inhib. Med. Chem., 2018, 33(1), 139-146. doi: 10.1080/14756366.2017.1405264 PMID: 29192555
- Alafeefy, A.M.; Ceruso, M.; Al-Jaber, N.A.; Parkkila, S.; Vermelho, A.B.; Supuran, C.T. 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. doi: 10.3109/14756366.2014.956309 PMID: 25373503
- Alterio, V.; Cadoni, R.; Esposito, D.; Vullo, D.; Fiore, A.D.; Monti, S.M.; Caporale, A.; Ruvo, M.; Sechi, M.; Dumy, P.; Supuran, C.T.; Simone, G.D.; Winum, J.Y. Benzoxaborole as a new chemotype for carbonic anhydrase inhibition. Chem. Commun. (Camb.), 2016, 52(80), 11983-11986. doi: 10.1039/C6CC06399C PMID: 27722534
- Nocentini, A.; Osman, S.M.; Rodrigues, I.A.; Cardoso, V.S.; Alasmary, F.A.S.; AlOthman, Z.; Vermelho, A.B.; Gratteri, P.; Supuran, C.T. 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. doi: 10.1080/14756366.2019.1626375 PMID: 31219348
- Bonardi, A.; Parkkila, S.; Supuran, C.T. Inhibition studies of the protozoan α-carbonic anhydrase from Trypanosoma cruzi with phenols. J. Enzyme Inhib. Med. Chem., 2022, 37(1), 2417-2422. doi: 10.1080/14756366.2022.2119965 PMID: 36065959
- Pal, D.S.; Mondal, D.K.; Datta, R. Identification of metal dithiocarbamates as a novel class of antileishmanial agents. Antimicrob. Agents Chemother., 2015, 59(4), 2144-2152. doi: 10.1128/AAC.05146-14 PMID: 25624329
- Syrjänen, L.; Vermelho, A.B.; de Almeida Rodrigues, I.; Corte-Real, S.; Salonen, T.; Pan, P.; Vullo, D.; Parkkila, S.; Capasso, C.; Supuran, C.T. 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. doi: 10.1021/jm400939k PMID: 23977960
- Ceruso, M.; Carta, F.; Osman, S.M.; Alothman, Z.; Monti, S.M.; Supuran, C.T. 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. doi: 10.1016/j.bmc.2015.06.050 PMID: 26145821
- Nocentini, A.; Cadoni, R.; del Prete, S.; Capasso, C.; Dumy, P.; Gratteri, P.; Supuran, C.T.; Winum, J.Y. Benzoxaboroles as efficient inhibitors of the β-carbonic anhydrases from pathogenic fungi: activity and modeling study. ACS Med. Chem. Lett., 2017, 8(11), 1194-1198. doi: 10.1021/acsmedchemlett.7b00369 PMID: 29152053
- Al-Tamimi, A.M.S.; Etxebeste-Mitxeltorena, M.; Sanmartín, C.; Jiménez-Ruiz, A.; Syrjänen, L.; Parkkila, S.; Selleri, S.; Carta, F.; Angeli, A.; Supuran, C.T. Discovery of new organoselenium compounds as antileishmanial agents. Bioorg. Chem., 2019, 86, 339-345. doi: 10.1016/j.bioorg.2019.01.069 PMID: 30743174
- Angeli, A.; Etxebeste-Mitxeltorena, M.; Sanmartín, C.; Espuelas, S.; Moreno, E.; Azqueta, A.; Parkkila, S.; Carta, F.; Supuran, C.T. Tellurides bearing sulfonamides as novel inhibitors of leishmanial carbonic anhydrase with potent antileishmanial activity. J. Med. Chem., 2020, 63(8), 4306-4314. doi: 10.1021/acs.jmedchem.0c00211 PMID: 32223141
- Bua, S.; Haapanen, S.; Kuuslahti, M.; Parkkila, S.; Supuran, C. Sulfonamide inhibition studies of a new β-carbonic anhydrase from the pathogenic protozoan Entamoeba histolytica. Int. J. Mol. Sci., 2018, 19(12), 3946. doi: 10.3390/ijms19123946 PMID: 30544802
- Haapanen, S.; Bua, S.; Kuuslahti, M.; Parkkila, S.; Supuran, C. Cloning, characterization and anion inhibition studies of a β-carbonic anhydrase from the pathogenic protozoan Entamoeba histolytica. Molecules, 2018, 23(12), 3112. doi: 10.3390/molecules23123112 PMID: 30486513
- Zolfaghari Emameh, R.; Barker, H.; Tolvanen, M.E.E.; Ortutay, C.; Parkkila, S. Bioinformatic analysis of beta carbonic anhydrase sequences from protozoans and metazoans. Parasit. Vectors, 2014, 7(1), 38. doi: 10.1186/1756-3305-7-38 PMID: 24447594
- Zolfaghari Emameh, R.; Barker, H.; Hytönen, V.P.; Tolvanen, M.E.E.; Parkkila, S. Beta carbonic anhydrases: novel targets for pesticides and anti-parasitic agents in agriculture and livestock husbandry. Parasit. Vectors, 2014, 7(1), 403. doi: 10.1186/1756-3305-7-403 PMID: 25174433
- Urbański, L.J.; Di Fiore, A.; Azizi, L.; Hytönen, V.P.; Kuuslahti, M.; Buonanno, M.; Monti, S.M.; Angeli, A.; Zolfaghari Emameh, R.; Supuran, C.T.; De Simone, G.; Parkkila, S. Biochemical and structural characterisation of a protozoan beta-carbonic anhydrase from Trichomonas vaginalis. J. Enzyme Inhib. Med. Chem., 2020, 35(1), 1292-1299. doi: 10.1080/14756366.2020.1774572 PMID: 32515610
- Van Gerwen, O.T.; Muzny, C.A. Recent advances in the epidemiology, diagnosis, and management of Trichomonas vaginalis infection. F1000 Res., 2019, 8, 1666. doi: 10.12688/f1000research.19972.1 PMID: 31583080
- Urbański, L.J.; Angeli, A.; Hytönen, V.P.; Di Fiore, A.; Parkkila, S.; De Simone, G.; Supuran, C.T. 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. doi: 10.1016/j.jinorgbio.2020.111274 PMID: 33068968
- Urbański, L.J.; Angeli, A.; Mykuliak, V.V.; Azizi, L.; Kuuslahti, M.; Hytönen, V.P.; Supuran, C.T.; Parkkila, S. Biochemical and structural characterization of beta-carbonic anhydrase from the parasite Trichomonas vaginalis. J. Mol. Med. (Berl.), 2022, 100(1), 115-124. doi: 10.1007/s00109-021-02148-1 PMID: 34652457
- Urbański, L.J.; Angeli, A.; Hytönen, V.P.; Di Fiore, A.; De Simone, G.; Parkkila, S.; Supuran, C.T. Inhibition of the β-carbonic anhydrase from the protozoan pathogen Trichomonas vaginalis with sulphonamides. J. Enzyme Inhib. Med. Chem., 2021, 36(1), 330-335. doi: 10.1080/14756366.2020.1863958 PMID: 33356653
Supplementary files
