Advances in the Development of Carbonic Anhydrase Inhibitors as New Antiprotozoal Agents


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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

  1. 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
  2. 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
  3. 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
  4. 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
  5. 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
  6. 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.
  7. Organization, W.H. Vector-borne Diseases; WHO Regional Office for South-east Asia, 2014.
  8. 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
  9. 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
  10. 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
  11. 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
  12. 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
  13. 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
  14. 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
  15. 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
  16. 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.
  17. Protein Data Bank Available from: https://www.rcsb.org/
  18. 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
  19. 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
  20. 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
  21. 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
  22. 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
  23. 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
  24. 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
  25. 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
  26. 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
  27. World Health Organization. Available from: https://www. who.int/es/news-room/fact-sheets/detail/chagas-disease-(american-trypanosomiasis) (Accessed on: 2022-02-03).
  28. NTD. World Health Organization. Available from: https://www.who.int/ (Accessed on: 2022-02-23).
  29. DrugBank. Available from: https://go.drugbank.com/ (Accessed on: 2021-02-03).
  30. 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
  31. Frampton, J.E. Tafenoquine: First global approval. Drugs, 2018, 78(14), 1517-1523. doi: 10.1007/s40265-018-0979-2 PMID: 30229442
  32. 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
  33. Duffy, P.E.; Patrick Gorres, J. Malaria Vaccines since 2000: Progress, priorities, products. NPJ. Vaccines (Basel), 2020, 5(1), 48. PMID: 32012760
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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
  39. 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
  40. 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
  41. 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
  42. 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
  43. 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
  44. 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
  45. 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
  46. 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
  47. 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
  48. 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
  49. 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
  50. 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
  51. 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
  52. 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
  53. 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
  54. 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
  55. 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
  56. 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
  57. 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
  58. 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
  59. 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
  60. 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
  61. 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
  62. 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
  63. 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
  64. 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
  65. 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
  66. 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
  67. 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
  68. 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
  69. 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
  70. 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
  71. 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
  72. 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
  73. 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
  74. 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
  75. 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
  76. 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
  77. 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
  78. 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
  79. 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
  80. 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

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