Esters of Quinoxaline-7-Carboxylate 1,4-di-N-Oxide as Potential Inhibitors of Glycolytic Enzymes of Entamoeba histolytica: In silico Approach


Дәйексөз келтіру

Толық мәтін

Аннотация

Background:Esters of quinoxaline-7-carboxylate 1,4-di-N-oxide (7-carboxylate QdNOs) derivatives are compounds that inhibit the growth of Entamoeba histolytica, the causative agent of amebiasis. Although these compounds cause changes in the redistribution of glycogen deposits within the parasite, it is unknown whether these compounds interact with enzymes of the glycolytic pathway.

Objective:The aim of this study was to test the binding affinity of these compounds to pyrophosphate- dependent phosphofructokinase (PPi-PFK), triosephosphate isomerase (TIM), and pyruvate phosphate dikinase (PPDK) from E. histolytica as a possible mechanism of action.

Methods:The molecular docking study of the 7-carboxylate QdNOs derivatives and the proteins was performed using AutoDock/Vina software. Molecular dynamics simulation was performed for 100 ns.

Results:Among all the selected compounds, T-072 exhibited the best binding affinity to EhPPi- PFK and EhTIM proteins, while T-006 interacted best with EhPPDK. ADMET analysis revealed that T-072 was non-toxic, while T-006 could become harmful to the host. In addition, molecular dynamics showed that T-072 has stable interaction with EhPPi-PFK and EhTIM.

Conclusion:Including all aspects, these data indicated that these compounds might inhibit the activity of key enzymes in energy metabolism leading to parasite death. Furthermore, these compounds may be a good starting point for the future development of new potent antiamebic agents.

Авторлар туралы

Lizeth Zavala-Ocampo

Laboratorio de Productos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México

Email: info@benthamscience.net

Jacqueline Soto-Sánchez

Sección de Estudios de Posgrado e Investigación, Escuela Nacional de Medicina y Homeopatía, Instituto Politécnico Naciona

Хат алмасуға жауапты Автор.
Email: info@benthamscience.net

Salvador Pérez-Mora

Sección de Estudios de Posgrado e Investigación, Escuela Nacional de Medicina y Homeopatía, Instituto Politécnico Nacional

Email: info@benthamscience.net

Juan Ospina-Villa

Instituto Colombiano de Medicina Tropical, Universidad CES, Sabaneta

Email: info@benthamscience.net

Әдебиет тізімі

  1. Quintanilla-Licea, R.; Vargas-Villarreal, J.; Verde-Star, M.J.; Rivas-Galindo, V.M.; Torres-Hernández, Á.D. Antiprotozoal activity against Entamoeba histolytica of flavonoids isolated from Lippia graveolens Kunth. Molecules, 2020, 25(11), 2464. doi: 10.3390/molecules25112464 PMID: 32466359
  2. Amoebiasis. Institut Pasteur. 2015. Available from: www.pasteur.fr/en/medical-center/disease-sheets/amoebiasis-0
  3. Espinosa-Cantellano, M.; Martínez-Palomo, A. Pathogenesis of intestinal amebiasis: From molecules to disease. Clin. Microbiol. Rev., 2000, 13(2), 318-331. doi: 10.1128/CMR.13.2.318 PMID: 10756002
  4. Mi-ichi, F.; Ishikawa, T.; Tam, V.K.; Deloer, S.; Hamano, S.; Hamada, T.; Yoshida, H. Characterization of Entamoeba histolytica adenosine 5′-phosphosulfate (APS) kinase; validation as a target and provision of leads for the development of new drugs against amoebiasis. PLoS Negl. Trop. Dis., 2019, 13(8), e0007633. doi: 10.1371/journal.pntd.0007633 PMID: 31425516
  5. Weir, C.B.; Le, J.K. Metronidazole; StatPearls Publishing: Treasure Island, FL, 2022.
  6. Wassmann, C.; Hellberg, A.; Tannich, E.; Bruchhaus, I. Metronidazole resistance in the protozoan parasite Entamoeba histolytica is associated with increased expression of iron-containing superoxide dismutase and peroxiredoxin and decreased expression of ferredoxin 1 and flavin reductase. J. Biol. Chem., 1999, 274(37), 26051-26056. doi: 10.1074/jbc.274.37.26051 PMID: 10473552
  7. Nagaraja, S.; Ankri, S. Target identification and intervention strategies against amebiasis. Drug Resist. Updat., 2019, 44, 1-14. doi: 10.1016/j.drup.2019.04.003 PMID: 31112766
  8. Saavedra, E.; Encalada, R.; Vázquez, C.; Olivos-García, A.; Michels, P.A.M.; Moreno-Sánchez, R. Control and regulation of the pyrophosphate-dependent glucose metabolism in Entamoeba histolytica. Mol. Biochem. Parasitol., 2019, 229, 75-87. doi: 10.1016/j.molbiopara.2019.02.002 PMID: 30772421
  9. Cheng, G.; Sa, W.; Cao, C.; Guo, L.; Hao, H.; Liu, Z.; Wang, X.; Yuan, Z. Quinoxaline 1,4-di-N-oxides: Biological activities and mechanisms of actions. Front. Pharmacol., 2016, 7, 64. doi: 10.3389/fphar.2016.00064 PMID: 27047380
  10. Soto-Sánchez, J.; Ospina-Villa, J.D. Current status of quinoxaline and quinoxaline 1,4‐di‐ N ‐oxides derivatives as potential antiparasitic agents. Chem. Biol. Drug Des., 2021, 98(4), 683-699. doi: 10.1111/cbdd.13921 PMID: 34289242
  11. Khatoon, H.; Abdulmalek, E. Novel synthetic routes to prepare biologically active quinoxalines and their derivatives: A synthetic review for the last two decades. Molecules, 2021, 26(4), 1055. doi: 10.3390/molecules26041055 PMID: 33670436
  12. Palos, I.; Luna-Herrera, J.; Lara-Ramírez, E.; Loera-Piedra, A.; Fernández-Ramírez, E.; Aguilera-Arreola, M.; Paz-González, A.; Monge, A.; Wan, B.; Franzblau, S.; Rivera, G. Anti-Mycobacterium tuberculosis activity of esters of quinoxaline 1,4-Di-N-oxide. Molecules, 2018, 23(6), 1453. doi: 10.3390/molecules23061453 PMID: 29914062
  13. Rivera, G.; Ahmad Shah, S.S.; Arrieta-Baez, D.; Palos, I.; Mongue, A.; Sánchez-Torres, L.E. Esters of quinoxaline 1`4-Di-N-oxide with cytotoxic activity on tumor cell lines based on NCI-60 panel. Iran. J. Pharm. Res., 2017, 16(3), 953-965. PMID: 29201086
  14. Chacón-Vargas, K.; Nogueda-Torres, B.; Sánchez-Torres, L.; Suarez-Contreras, E.; Villalobos-Rocha, J.; Torres-Martinez, Y.; Lara-Ramirez, E.; Fiorani, G.; Krauth-Siegel, R.; Bolognesi, M.; Monge, A.; Rivera, G. Trypanocidal activity of quinoxaline 1,4 Di-N-oxide derivatives as trypanothione reductase inhibitors. Molecules, 2017, 22(2), 220. doi: 10.3390/molecules22020220 PMID: 28157150
  15. Villalobos-Rocha, J.C.; Sánchez-Torres, L.; Nogueda-Torres, B.; Segura-Cabrera, A.; García-Pérez, C.A.; Bocanegra-García, V.; Palos, I.; Monge, A.; Rivera, G. Anti-Trypanosoma cruzi and anti-leishmanial activity by quinoxaline-7-carboxylate 1,4-di-N-oxide derivatives. Parasitol. Res., 2014, 113(6), 2027-2035. doi: 10.1007/s00436-014-3850-8 PMID: 24691716
  16. Chacón-Vargas, K.F.; Andrade-Ochoa, S.; Nogueda-Torres, B.; Juárez-Ramírez, D.C.; Lara-Ramírez, E.E.; Mondragón-Flores, R.; Monge, A.; Rivera, G.; Sánchez-Torres, L.E. Isopropyl quinoxaline-7-carboxylate 1,4-di-N-oxide derivatives induce regulated necrosis-like cell death on Leishmania (Leishmania) mexicana. Parasitol. Res., 2018, 117(1), 45-58. doi: 10.1007/s00436-017-5635-3 PMID: 29159705
  17. Palos, I.; Moo-Puc, R.; Vique-Sánchez, J.L.; Benítez-Cardoza, C.G.; Monge, A.; Villalobos-Rocha, J.C.; Paz-Gonzalez, A.D.; Rivera, G. Esters of quinoxaline-7-carboxylate-1,4-di- N -oxide as Trichomonas vaginalis triosephosphate isomerase inhibitors. Acta Pharm., 2021, 71(3), 485-495. doi: 10.2478/acph-2021-0032 PMID: 36654088
  18. Duque-Montaño, B.E.; Gómez-Caro, L.C.; Sanchez-Sanchez, M.; Monge, A.; Hernández-Baltazar, E.; Rivera, G.; Torres-Angeles, O. Synthesis and in vitro evaluation of new ethyl and methyl quinoxaline-7-carboxylate 1,4-di-N-oxide against Entamoeba histolytica. Bioorg. Med. Chem., 2013, 21(15), 4550-4558. doi: 10.1016/j.bmc.2013.05.036 PMID: 23787289
  19. Soto-Sánchez, J.; Caro-Gómez, L.A.; Paz-González, A.D.; Marchat, L.A.; Rivera, G.; Moo-Puc, R.; Arias, D.G.; Ramírez-Moreno, E. Biological activity of esters of quinoxaline-7-carboxylate 1,4-di-N-oxide against E. histolytica and their analysis as potential thioredoxin reductase inhibitors. Parasitol. Res., 2020, 119(2), 695-711. doi: 10.1007/s00436-019-06580-8 PMID: 31907668
  20. Benitez, D.; Cabrera, M.; Hernández, P.; Boiani, L.; Lavaggi, M.L.; Di Maio, R.; Yaluff, G.; Serna, E.; Torres, S.; Ferreira, M.E.; Vera de Bilbao, N.; Torres, E.; Pérez-Silanes, S.; Solano, B.; Moreno, E.; Aldana, I.; López de Ceráin, A.; Cerecetto, H.; González, M.; Monge, A. 3-Trifluoromethylquinoxaline N,N′-dioxides as anti-trypanosomatid agents. Identification of optimal anti-T. cruzi agents and mechanism of action studies. J. Med. Chem., 2011, 54(10), 3624-3636. doi: 10.1021/jm2002469 PMID: 21506600
  21. Álvarez, G.; Aguirre-López, B.; Varela, J.; Cabrera, M.; Merlino, A.; López, G.V.; Lavaggi, M.L.; Porcal, W.; Di Maio, R.; González, M.; Cerecetto, H.; Cabrera, N.; Pérez-Montfort, R.; de Gómez-Puyou, M.T.; Gómez-Puyou, A. Massive screening yields novel and selective Trypanosoma cruzi triosephosphate isomerase dimer-interface-irreversible inhibitors with anti-trypanosomal activity. Eur. J. Med. Chem., 2010, 45(12), 5767-5772. doi: 10.1016/j.ejmech.2010.09.034 PMID: 20889239
  22. Wierenga, R.K.; Kapetaniou, E.G.; Venkatesan, R. Triosephosphate isomerase: A highly evolved biocatalyst. Cell. Mol. Life Sci., 2010, 67(23), 3961-3982. doi: 10.1007/s00018-010-0473-9 PMID: 20694739
  23. Zomosa-Signoret, V.; Hernández-Alcántara, G.; Reyes-Vivas, H.; Martínez-Martínez, E.; Garza-Ramos, G.; Pérez-Montfort, R.; de Gómez-Puyou, M.T.; Gómez-Puyou, A. Control of the reactivation kinetics of homodimeric triosephosphate isomerase from unfolded monomers. Biochemistry, 2003, 42(11), 3311-3318. doi: 10.1021/bi0206560 PMID: 12641463
  24. Rodríguez-Romero, A.; Hernández-Santoyo, A.; del Pozo Yauner, L.; Kornhauser, A.; Fernández-Velasco, D.A. Structure and inactivation of triosephosphate isomerase from Entamoeba histolytica. J. Mol. Biol., 2002, 322(4), 669-675. doi: 10.1016/S0022-2836(02)00809-4 PMID: 12270704
  25. Deng, Z.; Huang, M.; Singh, K.; Albach, A.R.; Latshaw, P.S.; Chang, K.P.; Kemp, G.R. Cloning and expression of the gene for the active PPi-dependent phosphofructokinase of Entamoeba histolytica. Biochem. J., 1998, 329(3), 659-664. doi: 10.1042/bj3290659 PMID: 9445396
  26. Li, Z.J.; Phillips, N.F.B. Pyrophosphate-dependent phosphofructokinase from Giardia lamblia: Purification and characterization. Protein Expr. Purif., 1995, 6(3), 319-328. doi: 10.1006/prep.1995.1042 PMID: 7663168
  27. Mertens, E. ATP versus pyrophosphate: Glycolysis revisited in parasitic protists. Parasitol. Today, 1993, 9(4), 122-126. doi: 10.1016/0169-4758(93)90169-G PMID: 15463728
  28. Mertens, E. Pyrophosphate-dependent phosphofructokinase, an anaerobic glycolytic enzyme? FEBS Lett., 1991, 285(1), 1-5. doi: 10.1016/0014-5793(91)80711-B PMID: 1648508
  29. Li, Z.; Phillips, N.F.B. Involvement and identification of a lysine in the PPi-site of pyrophosphate-dependent phosphofructokinase from Giardia lamblia. Biochimie, 1997, 79(4), 221-227. doi: 10.1016/S0300-9084(97)83509-2 PMID: 9242987
  30. Nevalainen, L.; Hrdý, I.; Müller, M. Sequence of a Giardia lamblia gene coding for the glycolytic enzyme, pyruvate,phosphate dikinase. Mol. Biochem. Parasitol., 1996, 77(2), 217-223. doi: 10.1016/0166-6851(96)02604-7 PMID: 8813667
  31. Feng, X.M.; Cao, L.J.; Adam, R.D.; Zhang, X.C.; Lu, S.Q. The catalyzing role of PPDK in Giardia lamblia. Biochem. Biophys. Res. Commun., 2008, 367(2), 394-398. doi: 10.1016/j.bbrc.2007.12.139 PMID: 18167307
  32. Mertens, E.; Ladror, U.S.; Lee, J.A.; Miretsky, A.; Morris, A.; Rozario, C.; Kemp, R.G.; Müller, M. The pyrophosphate-dependent phosphofructokinase of the protist, Trichomonas vaginalis, and the evolutionary relationships of protist phosphofructokinases. J. Mol. Evol., 1998, 47(6), 739-750. doi: 10.1007/PL00006433 PMID: 9847416
  33. Rodriguez-Contreras, D.; Hamilton, N. Gluconeogenesis in Leishmania mexicana. J. Biol. Chem., 2014, 289(47), 32989-33000. doi: 10.1074/jbc.M114.569434 PMID: 25288791
  34. González-Marcano, E.; Acosta, H.; Mijares, A.; Concepción, J.L. Kinetic and molecular characterization of the pyruvate phosphate dikinase from Trypanosoma cruzi. Exp. Parasitol., 2016, 165, 81-87. doi: 10.1016/j.exppara.2016.03.023 PMID: 27003459
  35. Cosenza, L.W.; Bringaud, F.; Baltz, T.; Vellieux, F.M.D. Crystallization and preliminary crystallographic investigation of glycosomal pyruvate phosphate dikinase from Trypanosoma brucei. Acta Crystallogr. D Biol. Crystallogr., 2000, 56(12), 1688-1690. doi: 10.1107/S0907444900015298 PMID: 11092947
  36. González-Marcano, E.; Acosta, H.; Quiñones, W.; Mijares, A.; Concepción, J.L. Hysteresis of pyruvate phosphate dikinase from Trypanosoma cruzi. Parasitol. Res., 2021, 120(4), 1421-1428. doi: 10.1007/s00436-020-06934-7 PMID: 33098461
  37. Eubank, W.B.; Reeves, R.E. Analog inhibitors for the pyrophosphate-dependent phosphofructokinase of Entamoeba histolytica and their effect on culture growth. J. Parasitol., 1982, 68(4), 599-602. doi: 10.2307/3280916 PMID: 6288907
  38. Bruchhaus, I.; Jacobs, T.; Denart, M.; Tannich, E. Pyrophosphate-dependent phosphofructokinase of Entamoeba histolytica: Molecular cloning, recombinant expression and inhibition by pyrophosphate analogues. Biochem. J., 1996, 316(1), 57-63. doi: 10.1042/bj3160057 PMID: 8645233
  39. Saavedra-Lira, E.; Ramirez-Silva, L.; Perez-Montfort, R. Expression and characterization of recombinant pyruvate phosphate dikinase from Entamoeba histolytica. Biochim. Biophys. Acta Protein Struct. Mol. Enzymol., 1998, 1382(1), 47-54. doi: 10.1016/S0167-4838(97)00139-8 PMID: 9507062
  40. Saavedra-Lira, E.; Pérez-Montfort, R. Energy production in Entamoeba histolytica: New perspectives in rational drug design. Arch. Med. Res., 1996, 27(3), 257-264. PMID: 8854380
  41. Stephen, P.; Vijayan, R.; Bhat, A.; Subbarao, N.; Bamezai, R.N.K. Molecular modeling on pyruvate phosphate dikinase of Entamoeba histolytica and in silico virtual screening for novel inhibitors. J. Comput. Aided Mol. Des., 2008, 22(9), 647-660. doi: 10.1007/s10822-007-9130-2 PMID: 17710553
  42. Juárez-Saldivar, A.; Barbosa-Cabrera, E.; Lara-Ramírez, E.E.; Paz-González, A.D.; Martínez-Vázquez, A.V.; Bocanegra-García, V.; Palos, I.; Campillo, N.E.; Rivera, G. Virtual screening of FDA-approved drugs against triose phosphate isomerase from Entamoeba histolytica and Giardia lamblia identifies inhibitors of their trophozoite growth phase. Int. J. Mol. Sci., 2021, 22(11), 5943. doi: 10.3390/ijms22115943 PMID: 34073021
  43. Saidin, S.; Othman, N.; Noordin, R. In vitro testing of potential Entamoeba histolytica pyruvate phosphate dikinase inhibitors. Am. J. Trop. Med. Hyg., 2017, 97(4), 1204-1213. doi: 10.4269/ajtmh.17-0132 PMID: 28820699
  44. Daina, A.; Michielin, O.; Zoete, V. SwissADME: A free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Sci. Rep., 2017, 7(1), 42717. doi: 10.1038/srep42717 PMID: 28256516
  45. Deng, Z.; Wang, X.; Kemp, R.G. Site-directed mutagenesis of the fructose 6-phosphate binding site of the pyrophosphate-dependent phosphofructokinase of Entamoeba histolytica. Arch. Biochem. Biophys., 2000, 380(1), 56-62. doi: 10.1006/abbi.2000.1881 PMID: 10900132
  46. Radchenko, E.V.; Dyabina, A.S.; Palyulin, V.A.; Zefirov, N.S. Prediction of human intestinal absorption of drug compounds. Russ. Chem. Bull., 2016, 65(2), 576-580. doi: 10.1007/s11172-016-1340-0
  47. Mi-ichi, F.; Yousuf, M.A.; Nakada-Tsukui, K.; Nozaki, T. Mitosomes in Entamoeba histolytica contain a sulfate activation pathway. Proc. Natl. Acad. Sci., 2009, 106(51), 21731-21736. doi: 10.1073/pnas.0907106106 PMID: 19995967
  48. Matt, J.; Duchêne, M. Molecular and biochemical characterization of Entamoeba histolytica fructokinase. Parasitol. Res., 2015, 114(5), 1939-1947. doi: 10.1007/s00436-015-4383-5 PMID: 25700717
  49. Kumari, P.; Idrees, D.; Rath, P.P.; Vijayan, R.; Gourinath, S. Biochemical and biophysical characterization of the smallest pyruvate kinase from Entamoeba histolytica. Biochim. Biophys. Acta. Proteins Proteomics, 2020, 1868(1), 140296. doi: 10.1016/j.bbapap.2019.140296 PMID: 31676451
  50. Pineda, E.; Encalada, R.; Vázquez, C.; Néquiz, M.; Olivos-García, A.; Moreno-Sánchez, R.; Saavedra, E. In vivo identification of the steps that control energy metabolism and survival of Entamoeba histolytica. FEBS J., 2015, 282(2), 318-331. doi: 10.1111/febs.13131 PMID: 25350227
  51. Brimacombe, K.R.; Walsh, M.J.; Liu, L.; Vásquez-Valdivieso, M.G.; Morgan, H.P.; McNae, I.; Fothergill-Gilmore, L.A.; Michels, P.A.M.; Auld, D.S.; Simeonov, A.; Walkinshaw, M.D.; Shen, M.; Boxer, M.B. Identification of ML251, a potent inhibitor of T. brucei and T. cruzi Phosphofructokinase. ACS Med. Chem. Lett., 2014, 5(1), 12-17. doi: 10.1021/ml400259d PMID: 24900769
  52. Zinsser, V.L.; Hoey, E.M.; Trudgett, A.; Timson, D.J. Biochemical characterisation of glyceraldehyde 3-phosphate dehydrogenase (GAPDH) from the liver fluke, Fasciola hepatica. Biochim. Biophys. Acta. Proteins Proteomics, 2014, 1844(4), 744-749. doi: 10.1016/j.bbapap.2014.02.008 PMID: 24566472
  53. Dax, C.; Duffieux, F.; Chabot, N.; Coincon, M.; Sygusch, J.; Michels, P.A.M.; Blonski, C. Selective irreversible inhibition of fructose 1,6-bisphosphate aldolase from Trypanosoma brucei. J. Med. Chem., 2006, 49(5), 1499-1502. doi: 10.1021/jm050237b PMID: 16509566
  54. Reeves, R.E.; South, D.J.; Blytt, H.J.; Warren, L.G. Pyrophosphate:D-fructose 6-phosphate 1-phosphotransferase. A new enzyme with the glycolytic function of 6-phosphofructokinase. J. Biol. Chem., 1974, 249(24), 7737-7741. doi: 10.1016/S0021-9258(19)42029-2 PMID: 4372217
  55. Moreno-Sánchez, R.; Marín-Hernández, A.; Gallardo-Pérez, J.C.; Quezada, H.; Encalada, R.; Rodríguez-Enríquez, S.; Saavedra, E. Phosphofructokinase type 1 kinetics, isoform expression and gene polymorphisms in cancer cells. J. Cell. Biochem., 2011, 113(5), 1692-1703. doi: 10.1002/jcb.24039 PMID: 22213537
  56. Fernandes, P.M.; Kinkead, J.; McNae, I.W.; Bringaud, F.; Michels, P.A.M.; Walkinshaw, M.D. The kinetic characteristics of human and trypanosomatid phosphofructokinases for the reverse reaction. Biochem. J., 2019, 476(2), 179-191. doi: 10.1042/BCJ20180635 PMID: 30404924
  57. Moreno-Viguri, E.; Pérez-Silanes, S. Quinoxaline 1,4-di- N -oxide derivatives: Interest in the treatment of chagas disease. Revista Virtual de Química, 2013, 5(6), 1101-1119. doi: 10.5935/1984-6835.20130080
  58. Yang, X.; Yin, X.; Liu, J.; Niu, Z.; Yang, J.; Shen, B. Essential role of pyrophosphate homeostasis mediated by the pyrophosphate-dependent phosphofructokinase in Toxoplasma gondii. PLoS Pathog., 2022, 18(2), e1010293. doi: 10.1371/journal.ppat.1010293 PMID: 35104280
  59. Téllez-Valencia, A.; Olivares-Illana, V.; Hernández-Santoyo, A.; Pérez-Montfort, R.; Costas, M.; Rodríguez-Romero, A.; López-Calahorra, F.; Tuena de Gómez-Puyou, M.; Gómez-Puyou, A. Inactivation of triosephosphate isomerase from Trypanosoma cruzi by an agent that perturbs its dimer interface. J. Mol. Biol., 2004, 341(5), 1355-1365. doi: 10.1016/j.jmb.2004.06.056 PMID: 15321726
  60. Schliebs, W.; Thanki, N.; Eritja, R.; Wierenga, R. Active site properties of monomeric triosephosphate isomerase (monoTIM) as deduced from mutational and structural studies. Protein Sci., 1996, 5(2), 229-239. doi: 10.1002/pro.5560050206 PMID: 8745400
  61. Tellez, L.A.; Blancas-Mejia, L.M.; Carrillo-Nava, E.; Mendoza-Hernández, G.; Cisneros, D.A.; Fernández-Velasco, D.A. Thermal unfolding of triosephosphate isomerase from Entamoeba histolytica: Dimer dissociation leads to extensive unfolding. Biochemistry, 2008, 47(44), 11665-11673. doi: 10.1021/bi801360k PMID: 18837510
  62. Téllez-Valencia, A.; Ávila-Ríos, S.; Pérez-Montfort, R.; Rodríguez-Romero, A.; de Gómez-Puyou, T.M.; López-Calahorra, F.; Gómez-Puyou, A. Highly specific inactivation of triosephosphate isomerase from Trypanosoma cruzi. Biochem. Biophys. Res. Commun., 2002, 295(4), 958-963. doi: 10.1016/S0006-291X(02)00796-9 PMID: 12127988
  63. 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
  64. Ferraro, F.; Corvo, I.; Bergalli, L.; Ilarraz, A.; Cabrera, M.; Gil, J.; Susuki, B.M.; Caffrey, C.R.; Timson, D.J.; Robert, X.; Guillon, C.; Freire, T.; Álvarez, G. Novel and selective inactivators of Triosephosphate isomerase with anti-trematode activity. Sci. Rep., 2020, 10(1), 2587. doi: 10.1038/s41598-020-59460-y PMID: 32054976
  65. Enriquez-Flores, S.; Rodriguez-Romero, A.; Hernandez-Alcantara, G.; De la Mora-De la Mora, I.; Gutierrez-Castrellon, P.; Carvajal, K.; Lopez-Velazquez, G.; Reyes-Vivas, H. Species-specific inhibition of Giardia lamblia triosephosphate isomerase by localized perturbation of the homodimer. Mol. Biochem. Parasitol., 2008, 157(2), 179-186. doi: 10.1016/j.molbiopara.2007.10.013 PMID: 18077010
  66. Vique-Sánchez, J.L.; Jiménez-Pineda, A.; Benítez-Cardoza, C.G. Amoebicidal effect of 5,5′‐(4‐nitrophenyl)methylenebis‐6‐hydroxy‐2‐mercapto‐3‐methyl‐4(3 H)‐pyrimidinone), a new drug against Entamoeba histolytica. Arch. Pharm., 2021, 354(2), 2000263. doi: 10.1002/ardp.202000263 PMID: 33017058
  67. Ye, D.; Wei, M.; McGuire, M.; Huang, K.; Kapadia, G.; Herzberg, O.; Martin, B.M.; Dunaway-Mariano, D. Investigation of the catalytic site within the ATP-grasp domain of Clostridium symbiosum pyruvate phosphate dikinase. J. Biol. Chem., 2001, 276(40), 37630-37639. doi: 10.1074/jbc.M105631200 PMID: 11468288
  68. Avila-Bonilla, R.G.; López-Sandoval, Á.; Soto-Sánchez, J.; Marchat, L.A.; Rivera, G.; Medina-Contreras, O.; Ramírez-Moreno, E. Proteomic and functional analysis of the effects of quinoxaline derivatives on Entamoeba histolytica. Front. Cell. Infect. Microbiol., 2022, 12, 887647. doi: 10.3389/fcimb.2022.887647 PMID: 35832378
  69. Malik, A.; Dalal, V.; Ankri, S.; Tomar, S. Structural insights into Entamoeba histolytica arginase and structure‐based identification of novel non‐amino acid based inhibitors as potential antiamoebic molecules. FEBS J., 2019, 286(20), 4135-4155. doi: 10.1111/febs.14960 PMID: 31199070
  70. Probst, A.; Nguyen, T.N.; El-Sakkary, N.; Skinner, D.; Suzuki, B.M.; Buckner, F.S.; Gelb, M.H.; Caffrey, C.R.; Debnath, A. Bioactivity of farnesyltransferase inhibitors against Entamoeba histolytica and Schistosoma mansoni. Front. Cell. Infect. Microbiol., 2019, 9, 180. doi: 10.3389/fcimb.2019.00180 PMID: 31192168
  71. Rodrigues, J.H.S.; Ueda-Nakamura, T.; Corrêa, A.G.; Sangi, D.P.; Nakamura, C.V. A quinoxaline derivative as a potent chemotherapeutic agent, alone or in combination with benznidazole, against Trypanosoma cruzi. PLoS One, 2014, 9(1), e85706. doi: 10.1371/journal.pone.0085706 PMID: 24465654
  72. Williams, C.F.; Vacca, A.R.; Dunham, L.; Lloyd, D.; Coogan, M.P.; Evans, G.; Graz, M.; Cable, J. The redox-active drug metronidazole and thiol-depleting garlic compounds act synergistically in the protist parasite Spironucleus vortens. Mol. Biochem. Parasitol., 2016, 206(1-2), 20-28. doi: 10.1016/j.molbiopara.2016.03.001 PMID: 26968264
  73. Planer, J.D.; Hulverson, M.A.; Arif, J.A.; Ranade, R.M.; Don, R.; Buckner, F.S. Synergy testing of FDA-approved drugs identifies potent drug combinations against Trypanosoma cruzi. PLoS Negl. Trop. Dis., 2014, 8(7), e2977. doi: 10.1371/journal.pntd.0002977 PMID: 25033456
  74. Zahid, M.S.H.; Johnson, M.M.; Tokarski, R.J., II; Satoskar, A.R.; Fuchs, J.R.; Bachelder, E.M.; Ainslie, K.M. Evaluation of synergy between host and pathogen-directed therapies against intracellular Leishmania donovani. Int. J. Parasitol. Drugs Drug Resist., 2019, 10, 125-132. doi: 10.1016/j.ijpddr.2019.08.004 PMID: 31493763
  75. Sun, Y.; Chen, D.; Pan, Y.; Qu, W.; Hao, H.; Wang, X.; Liu, Z.; Xie, S. Nanoparticles for antiparasitic drug delivery. Drug Deliv., 2019, 26(1), 1206-1221. doi: 10.1080/10717544.2019.1692968 PMID: 31746243
  76. de Oliveira, J.K.; Ueda-Nakamura, T.; Corrêa, A.G.; Petrilli, R.; Lopez, R.F.V.; Nakamura, C.V.; Auzely-Velty, R. Liposome-based nanocarrier loaded with a new quinoxaline derivative for the treatment of cutaneous leishmaniasis. Mater. Sci. Eng. C, 2020, 110(110720), 110720. doi: 10.1016/j.msec.2020.110720 PMID: 32204033

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