Esters of quinoxaline-7-carboxylate-1,4-di-N-oxide as Trichomonas vaginalis triosephosphate isomerase inhibitors

1. D. Leitsch, Drug resistance in the microaerophilic parasite Giardia lamblia, Curr. Trop. Med. Rep.2 (2015) 128–135; https://doi.org/10.1007/s40475-015-0051-110.1007/s40475-015-0051-1452369426258002Search in Google Scholar

2. B. R. Ansell, M. J. McConville, S. Y. Ma’ayeh, M. J. Dagley, R. B. Gasser, S. G. Svärd and A. R. Jex, Drug resistance in Giardia duodenalis, Biotechnol. Adv.33 (2015) 888–901; https://doi.org/10.1016/j.biotechadv.2015.04.00910.1016/j.biotechadv.2015.04.00925922317Search in Google Scholar

3. C. B. Menezes, A. P. Frasson and T. Tasca, Trichomoniasis – are we giving the deserved attention to the most common non-viral sexually transmitted disease worldwide?, Microb. Cell3 (2016) 404–419; https://doi.org/10.15698/mic2016.09.52610.15698/mic2016.09.526535456828357378Search in Google Scholar

4. D. Leitsch, Recent advances in the Trichomonas vaginalis field, F1000Res.5 (2016) Article ID 162 (7 pages); https://doi.org/10.12688/f1000research.7594.110.12688/f1000research.7594.1475539626918168Search in Google Scholar

5. P. Kissinger, Trichomonas vaginalis: a review of epidemiologic, clinical and treatment issues, BMC Infect. Dis.15 (2015) Article ID 307 (8 pages); https://doi.org/10.1186/s12879-015-1055-010.1186/s12879-015-1055-0452574926242185Search in Google Scholar

6. P. Upcroft and J. A. Upcroft, Drug targets and mechanisms of resistance in the anaerobic protozoa, Clin. Microbiol. Rev.14 (2001) 150–164; https://doi.org/10.1128/CMR.14.1.150-164.200110.1128/CMR.14.1.150-164.20018896711148007Search in Google Scholar

7. P. A. Cano, A. Islas-Jácome, J. González-Marrero, L. Yépez-Mulia, F. Calzada and R. Gámez-Montaño, Synthesis of 3-tetrazolylmethyl-4H-chromen-4-ones via Ugi-azide and biological evaluation against Entamoeba histolytica, Giardia lamblia and Trichomona vaginalis, Bioorg. Med. Chem.22 (2014) 1370–1376; https://doi.org/10.1016/j.bmc.2013.12.06910.1016/j.bmc.2013.12.06924468633Search in Google Scholar

8. S. Chaturvedi, M. Y. Malik, M. Rashid, S. Singh, V. Tiwari, P. Gupta, S. Shukla, S. Singh and M. Wahajuddin, Mechanistic exploration of quercetin against metronidazole induced neurotoxicity in rats: possible role of nitric oxide isoforms and inflammatory cytokines, Neurotoxicology79 (2020) 1–10; https://doi.org/10.1016/j.neuro.2020.03.00210.1016/j.neuro.2020.03.00232151614Search in Google Scholar

9. J. Jampilek, Recent advances in design of potential quinoxaline anti-infectives, Curr. Med. Chem.21 (2014) 4347–4373; https://doi.org/10.2174/092986732166614101119482510.2174/092986732166614101119482525312209Search in Google Scholar

10. I. Balderas-Renteria, P. Gonzalez-Barranco, A. Garcia, B. K. Banik and G. Rivera, Anticancer drug design using scaffolds of β-lactams, sulfonamides, quinoline, quinoxaline and natural products. Drugs advances in clinical trials, Curr. Med. Chem.19 (2012) 4377–4398; https://doi.org/10.2174/09298671280325159310.2174/09298671280325159322709002Search in Google Scholar

11. N. B. Patel, J. N. Patel, A. C. Purohit, V. M. Patel, D. P. Rajani, R. Moo-Puc, J. C. Lopez-Cedillo, B. Nogueda-Torres and G. Rivera, In vitro and in vivo assessment of newer quinoxaline-oxadiazole hybrids as antimicrobial and antiprotozoal agents, Int. J. Antimicrob. Agents50 (2017) 413–418; https://doi.org/10.1016/j.ijantimicag.2017.04.01610.1016/j.ijantimicag.2017.04.01628687457Search in Google Scholar

12. G. Cheng, W. Sa, C. Cao, L. Guo, H. Hao, Z. Liu, X. Wang and Z. Yuan, Quinoxaline 1,4-di-N-oxides: Biological activities and mechanisms of actions, Front. Pharmacol.7 (2016) Article ID 64 (21 pages); https://doi.org/10.3389/fphar.2016.0006410.3389/fphar.2016.00064480018627047380Search in Google Scholar

13. R. El Aissi, J. Liu, S. Besse, D. Canitrot, O. Chavignon, J. M. Chezal, E. Miot-Noirault and E. Moreau, Synthesis and biological evaluation of new quinoxaline derivatives of ICF01012 as melanoma-targeting probes, ACS Med. Chem. Lett.5 (2014) 468–473; https://doi.org/10.1021/ml400468x10.1021/ml400468x402760924900863Search in Google Scholar

14. J. C. Villalobos-Rocha, L. Sánchez-Torres, B. Nogueda-Torres, A. Segura-Cabrera, C. A. García-Pérez, V. Bocanegra-García, I. Palos, A. Monge and G. Rivera, Anti-Trypanosoma cruzi and anti-leishmanial activity by quinoxaline-7-carboxylate 1,4-di-N-oxide derivatives, Parasitol. Res.113 (2014) 2027–2035; https://doi.org/10.1007/s00436-014-3850-810.1007/s00436-014-3850-824691716Search in Google Scholar

15. K. F. Chacón-Vargas, S. Andrade-Ochoa, B. Nogueda-Torres, D. C. Juárez-Ramírez, E. E. Lara-Ramírez, R. Mondragón-Flores, A. Monge and G. Rivera, L. E. Sánchez-Torres, Isopropyl quinoxaline-7-carboxylate 1,4-di-N-oxide derivatives induce regulated necrosis-like cell death on Leish-mania (Leishmania) mexicana, Parasitol. Res.117 (2018) 45–58; https://doi.org/10.1007/s00436-017-5635-310.1007/s00436-017-5635-329159705Search in Google Scholar

16. M. Quiliano, A. Pabón, G. Ramirez-Calderon, C. Barea, E. Deharo, S. Galiano and I. Aldana, New hydrazine and hydrazide quinoxaline 1,4-di-N-oxide derivatives: In silico ADMET, antiplasmo-dial and antileishmanial activity. Bioorg. Med. Chem. Lett.27 (2017) 1820–1825; https://doi.org/10.1016/j.bmcl.2017.02.04910.1016/j.bmcl.2017.02.04928291694Search in Google Scholar

17. B. E. Duque-Montaño, L. C. Gómez-Caro, M. Sanchez-Sanchez, A. Monge, E. Hernández-Baltazar, G. Rivera and O. Torres-Angeles, Synthesis and in vitro evaluation of new ethyl and methyl quinoxaline-7-carboxylate 1,4-di-N-oxide against Entamoeba histolytica, Bioorg. Med. Chem.21 (2013) 4550–4558; https://doi.org/10.1016/j.bmc.2013.05.03610.1016/j.bmc.2013.05.03623787289Search in Google Scholar

18. L. C. Gómez-Caro, M. Sánchez-Sánchez, V. Bocanegra-García, A. Monge and G. Rivera, Synthesis of quinoxaline 1,4-di-N-oxide derivatives on solid support using room temperature and microwave-assisted solvent-free procedures, Quim. Nova34 (2011) 1147–1151; https://doi.org/10.1590/S0100-4042201100070000810.1590/S0100-40422011000700008Search in Google Scholar

19. E. Hernández-Núñez, H. Tlahuext, R. Moo-Puc, H. Torres-Gómez, R. Reyes-Martínez, R Cedillo-Rivera, C. Nava-Zuazo and G. Navarrete-Vazquez, Synthesis and in vitro trichomonicidal, giardicidal and amebicidal activity of N-acetamide(sulfonamide)-2-methyl-4-nitro-1H-imidazoles, Eur. J. Med. Chem.44 (2009) 2975–2984; https://doi.org/10.1016/j.ejmech.2009.01.00510.1016/j.ejmech.2009.01.00519208443Search in Google Scholar

20. B. R. Brooks, C. L. Brooks, A. D. Mackerell, L. Nilsson, R. J. Petrella, B. Roux, Y. Won, G. Archontis, C. Bartels, S. Boresch, A. Caflisch, L. Caves, Q. Cui, A. R. Dinner, M. Feig, S. Fischer, J. Gao, M. Hodoscek, W. Im, K. Kuczera, T. Lazaridis, J. Ma, V. Ovchinnikov, E. Paci, R. W. Pastor, C. B. Post, J. Z. Pu, M. Schaefer, B. Tidor, R. M. Venable, H. L. Woodcock, X. Wu, W. Yang, D. M. York and M. Karplus, CHARMM: The biomolecular simulation program, J. Comput. Chem.30 (2009) 1545–1614; https://doi.org/10.1002/jcc.2128710.1002/jcc.21287281066119444816Search in Google Scholar

21. P. R. Gerber and K. Müller, MAB, a generally applicable molecular force field for structure modelling in medicinal chemistry, J. Comput. Aided Mol. Des.9 (1995) 251–268; https://doi.org/10.1007/bf0012445610.1007/BF00124456Search in Google Scholar

22. C. A. Del Carpio, Y. Takahashi and S.-i. Sasaki, A new approach to the automatic identification of candidates for ligand receptor sites in proteins: (I) Search for pocket regions, J. Mol. Graph.11 (1993) 23–29; https://doi.org/10.1016/0263-7855(93)85003-9Search in Google Scholar

23. A. Miranker and M. Karplus, Functionality maps of binding sites: A multiple copy simultaneous search method, Proteins: Struct. Funct. Genet.11 (1991) 29–34; https://doi.org/10.1002/prot.3401101010.1002/prot.340110104Search in Google Scholar

24. S. Thangapandian, S. John, Y. Lee, S. Kim and K. W. Lee, Dynamic structure-based pharmacophore model development: A new and effective addition in the histone deacetylase 8 (HDAC8) inhibitor discovery, Int. J. Mol. Sci.12 (2011) 9440–9462; https://doi.org/10.3390/ijms1212944010.3390/ijms12129440Search in Google Scholar

25. A. Wadood, M. Ghufran, S. F. Hassan, H. Khan, S. S. Azam and U. Rashid, In silico identification of promiscuous scaffolds as potential inhibitors of 1-deoxy-D-xylulose 5-phosphate reductoisom-erase for treatment of Falciparum malaria, Pharm. Biol.55 (2017) 19–32; https://doi.org/10.1080/13880209.2016.122577810.1080/13880209.2016.1225778Search in Google Scholar

26. A. M. Clark and P. Labute, 2D depiction of protein–ligand complexes, J. Chem. Inf. Model. 47 (2007) 1933–1944; https://doi.org/10.1021/ci700147310.1021/ci7001473Search in Google Scholar

27. S. Lara-González, P. Estrella, C. Portillo, M. E. Cruces, P. Jiménez-Sandoval, J. Fattori, A. C. Migliorini-Figueira, M. López-Hidalgo, C. Díaz-Quezada, M. López-Castillo, C. H. Trasviña-Arenas, E. Sánchez-Sandoval, A. Gómez-Puyou, J. Ortega-López, R. Arroyo, C. G. Benítez-Cardoza and L. G. Brieba, Substrate-induced dimerization of engineered monomeric variants of triosephosphate isomerase from Trichomonas vaginalis, PLoS ONE10 (2015) e0141747; https://doi.org/10.1371/journal.pone.014174710.1371/journal.pone.0141747Search in Google Scholar

28. P. Jiménez-Sandoval, J. L. Vique-Sanchez, M. L. Hidalgo, G. Velazquez-Juarez, C. Díaz-Quezada, L. F. Arroyo-Navarro, G. M. Morán, J. Fattori, A. J. Diaz-Salazar, E. Rudiño-Pinera, R. Sotelo-Mundo, A. C. Migliorini-Figueira, S. Lara-Gonzalez, C. G. Benítez-Cardoza and L. G. Brieba, A competent catalytic active site is necessary for substrate induced dimer assembly in triosephosphate isomerase, Biochim. Biophys. Acta – Prot. Proteom.1865 (2017) 1423–1432; https://doi.org/10.1016/j.bbapap.2017.07.01410.1016/j.bbapap.2017.07.014Search in Google Scholar

29. G. Álvarez, J. Martínez, B. Aguirre-López, N. Cabrera, L. Pérez-Díaz, M. T. de Gómez-Puyou, A. Gómez-Puyou, R. Pérez-Montfort, B. Garat, A. Merlino, M. González and H. Cerecetto, New chemotypes as Trypanosoma cruzi triosephosphate isomerase inhibitors: a deeper insight into the mechanism of inhibition, J. Enzyme Inhib. Med. Chem.29 (2014) 198–204; https://doi.org/10.3109/14756366.2013.76541510.3109/14756366.2013.765415Search in Google Scholar

30. A. Gómez-Puyou, E. Saavedra-Lira, I. Becker, R. A. Zubillaga, A. Rojo-Dominguez and R. Perez-Montfort, Using evolutionary changes to achieve species-specific inhibition of enzyme action — studies with triosephosphate isomerase, Chem. Biol.2 (1995) 847–855; https://doi.org/10.1016/1074-5521(95)90091-810.1016/1074-5521(95)90091-8Search in Google Scholar

31. M. de N. C. Soeiro and S. L. Castro, Screening of potential anti-Trypanosoma cruzi candidates: In vitro and in vivo studies, Open Med. Chem. J.5 (2011) 21–30; https://doi.org/10.2174/187410450110501002110.2174/1874104501105010021310389721629508Search in Google Scholar

32. G. Álvarez, B. Aguirre-López, J. Varela, M. Cabrera, A. Merlino, G. V. López, M. L. Lavaggi, W. Porcal, R. Di Maio, M. González, H. Cerecetto, N. Cabrera, R. Pérez-Montfort, M. Tuena de Gómez-Puyou and A. Gómez-Puyou, Massive screening yields novel and selective Trypanosoma cruzi triosephosphate isomerase dimer-interface-irreversible inhibitors with anti-trypanosomal activity, Eur. J. Med. Chem.45 (2010) 5767–5772; https://doi.org/10.1016/j.ejmech.2010.09.03410.1016/j.ejmech.2010.09.03420889239Search in Google Scholar

33. C. G. Benítez-Cardoza, D. A. Fernández-Velasco and J. L. Vique-Sánchez, Triosephosphate isom-erase inhibitors as potential drugs against Clostridium perfringens, Chem. Sel.5 (2020) 2365–2370; https://doi.org/10.1002/slct.20190463210.1002/slct.201904632Search in Google Scholar

34. J. L. Vique-Sánchez, L. A. Caro-Gómez, L. G. Brieba and C. G. Benítez-Cardoza, Developing a new drug against trichomoniasis, new inhibitory compounds of the protein triosephosphate isomerase, Parasitol. Int.76 (2020) Article ID 102086; https://doi.org/10.1016/j.parint.2020.10208610.1016/j.parint.2020.102086Search in Google Scholar

35. A. Téllez-Valencia, S. Avila-Ríos, R. Pérez-Montfort, A. Rodríguez-Romero, M. Tuena de Gómez-Puyou, F. López-Calahorra and A. Gómez-Puyou, Highly specific inactivation of triosephosphate isomerase from Trypanosoma cruzi, Biochem. Biophys. Res. Commun.295 (2002) 958–963; https://doi.org/10.1016/s0006-291x(02)00796-910.1016/S0006-291X(02)00796-9Search in Google Scholar

36. B. Hernández-Ochoa, G. Navarrete-Vázquez, C. Nava-Zuazo, A. Castillo-Villanueva, S. T. Méndez, A. Torres-Arroyo, S. Gómez-Manzo, J. Marcial-Quino, M. Ponce-Macotela, Y. Rufino-González, M. Martínez-Gordillo, G. Palencia-Hernández, N. Esturau-Escofet, E. Calderon-Jaimes, J. Oria-Hernández and H. Reyes-Vivas, Novel giardicidal compounds bearing proton pump inhibitor scaffold proceeding through triosephosphate isomerase inactivation, Sci. Rep.7 (2017) Article ID 7810; https://doi.org/10.1038/s41598-017-07612-y10.1038/s41598-017-07612-y555269128798383Search in Google Scholar