Elucidating structure and dynamics of glutathione S-transferase from Rhipicephalus (Boophilus) microplus

References

• Aguilar, G., Olvera, A. M., Carvajal, B. I., & Mosqueda, J. (2018). SNPs and other polymorhisms associated with acaricide resistance in Rhipicephalus microplus. Frontiers in Bioscience (Landmark Edition), 23(1), 65–82. https://doi.org/10.2741/4582
   PubMedGoogle Scholar
• Alves, C. S., Kuhnert, D. C., Sayed, Y., & Dirr, H. W. (2006). The intersubunit lock-and-key motif in human glutathione transferase A1-1: Role of the key residues Met51 and Phe52 in function and dimer stability. The Biochemical Journal, 393(Pt 2), 523–528. https://doi.org/10.1042/BJ20051066
   PubMedGoogle Scholar
• Angelucci, F., Baiocco, P., Brunori, M., Gourlay, L., Morea, V., & Bellelli, A. (2005). Insights into the catalytic mechanism of glutathione S-transferase: The lesson from Schistosoma haematobium. Structure (London, England : 1993), 13(9), 1241–1246. https://doi.org/10.1016/j.str.2005.06.007
   PubMed Web of Science ®Google Scholar
• Armstrong, R. N. (1991). Glutathione S-transferases: reaction mechanism, structure, and function. Chemical Research in Toxicology, 4(2), 131–140. https://doi.org/10.1021/tx00020a001
   PubMed Web of Science ®Google Scholar
• Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. Journal of Chemical Physics, 81(8), 3684–3690. https://doi.org/10.1063/1.448118
   Web of Science ®Google Scholar
• Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Cassarino, T. G., Bertoni, M., Bordoli, L., & Schwede, T. (2014). SWISS-MODEL: Modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Research, 42(Web Server issue), W252–8W258. https://doi.org/10.1093/nar/gku340
   PubMed Web of Science ®Google Scholar
• Chen, T. H., Lo, Y. P., Yang, C. F., & Chen, W. J. (2012). Additive protection by antioxidant and apoptosis-inhibiting effects on mosquito cells with dengue 2 virus infection. PLoS Neglected Tropical Diseases, 6(4), e1613. https://doi.org/10.1371/journal.pntd.0001613
   PubMed Web of Science ®Google Scholar
• Chevillon, C., Ducornez, S., de Meeus, T., Koffi, B. B., Gaia, H., Delathiere, J. M., & Barre, N. (2007). Accumulation of acaricide resistance mechanisms in Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) populations from New Caledonia Island. Vet Parasitol, 147(3-4), 276–288. https://doi.org/10.1016/j.vetpar.2007.05.003
   PubMed Web of Science ®Google Scholar
• Codreanu, S. G., Thompson, L. C., Hachey, D. L., Dirr, H. W., & Armstrong, R. N. (2005). Influence of the dimer interface on glutathione transferase structure and dynamics revealed by amide H/D exchange mass spectrometry. Biochemistry, 44(31), 10605–10612. https://doi.org/10.1021/bi050836k
   PubMed Web of Science ®Google Scholar
• Daborn, P. J., Yen, J. L., Bogwitz, M. R., Le Goff, G., Feil, E., Jeffers, S., Tijet, N., Perry, T., Heckel, D., Batterham, P., Feyereisen, R., Wilson, T. G., & ffrench-Constant, R. H. (2002). ffrench-Constant RH. A single p450 allele associated with insecticide resistance in Drosophila. Science (New York, N.Y.), 297(5590), 2253–2256. https://doi.org/10.1126/science.1074170
   PubMed Web of Science ®Google Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N·log(N) method for Ewald sums in large systems. Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
   Web of Science ®Google Scholar
• Deponte, M. (2013). Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochimica et Biophysica Acta, 1830(5), 3217–3266. https://doi.org/10.1016/j.bbagen.2012.09.018
   PubMed Web of Science ®Google Scholar
• Dourado, D. F., Fernandes, P. A., & Ramos, M. J. (2010). Glutathione transferase classes alpha, pi, and mu: GSH activation mechanism. The Journal of Physical Chemistry B, 114(40), 12972–12980. https://doi.org/10.1021/jp1053875
   PubMed Web of Science ®Google Scholar
• Dzemo, W. D., Thekisoe, O., & Vudriko, P. (2022). Development of acaricide resistance in tick populations of cattle: A systematic review and meta-analysis. Heliyon, 8(1), e08718. https://doi.org/10.1016/j.heliyon.2022.e08718
   PubMed Web of Science ®Google Scholar
• Eswar, N., Webb, B., Marti-Renom, M. A., Madhusudhan, M. S., Eramian, D., Shen, M. Y., Pieper, U., & Sali, A. (2006). Comparative protein structure modeling using modeller. Current Protocols in Bioinformatics, 5, Unit–UnU5.6. Chapter 5:Unit 5 6. https://doi.org/10.1002/0471250953.bi0506s15
   Google Scholar
• Graf, J. F., Gogolewski, R., Leach-Bing, N., Sabatini, G. A., Molento, M. B., Bordin, E. L., & Arantes, G. J. (2004). Tick control: an industry point of view. Parasitology, 129(Suppl), S427–S42. https://doi.org/10.1017/s0031182004006079
   PubMedGoogle Scholar
• Guerrero, F. D., Lovis, L., & Martins, J. R. (2012). Acaricide resistance mechanisms in Rhipicephalus (Boophilus) microplus. Revista brasileira de parasitologia veterinaria = Brazilian journal of veterinary parasitology : Orgao Oficial do Colegio Brasileiro de Parasitologia Veterinaria, 21(1), 1–6. https://doi.org/10.1590/s1984-29612012000100002
   PubMed Web of Science ®Google Scholar
• Gülçin, İ., Scozzafava, A., Supuran, C. T., Akıncıoğlu, H., Koksal, Z., Turkan, F., & Alwasel, S. (2016). The effect of caffeic acid phenethyl ester (CAPE) on metabolic enzymes including acetylcholinesterase, butyrylcholinesterase, glutathione S-transferase, lactoperoxidase, and carbonic anhydrase isoenzymes I, II, IX, and XII. Journal of Enzyme Inhibition and Medicinal Chemistry, 31(6), 1095–1101. https://doi.org/10.3109/14756366.2015.1094470
   PubMed Web of Science ®Google Scholar
• Gülçin, İ., Scozzafava, A., Supuran, C. T., Koksal, Z., Turkan, F., Çetinkaya, S., Bingöl, Z., Huyut, Z., & Alwasel, S. H. (2016). Rosmarinic acid inhibits some metabolic enzymes including glutathione S-transferase, lactoperoxidase, acetylcholinesterase, butyrylcholinesterase and carbonic anhydrase isoenzymes. Journal of Enzyme Inhibition and Medicinal Chemistry, 31(6), 1698–1702. https://doi.org/10.3109/14756366.2015.1135914
   PubMed Web of Science ®Google Scholar
• Gulçin, İ., Taslimi, P., Aygün, A., Sadeghian, N., Bastem, E., Kufrevioglu, O. I., Turkan, F., & Şen, F. (2018). Antidiabetic and antiparasitic potentials: Inhibition effects of some natural antioxidant compounds on α-glycosidase, α-amylase and human glutathione S-transferase enzymes. International Journal of Biological Macromolecules, 119, 741–746. https://doi.org/10.1016/j.ijbiomac.2018.08.001
   PubMed Web of Science ®Google Scholar
• He, H., Chen, A. C., Davey, R. B., Ivie, G. W., & George, J. E. (1999). Characterization and molecular cloning of a glutathione S-transferase gene from the tick, Boophilus microplus (Acari: Ixodidae). Insect Biochemistry and Molecular Biology, 29(8), 737–743. https://doi.org/10.1016/S0965-1748(99)00056-9
   PubMed Web of Science ®Google Scholar
• Hearne, J. L., & Colman, R. F. (2006). Contribution of the mu loop to the structure and function of rat glutathione transferase M1-1. Protein Science : A Publication of the Protein Society, 15(6), 1277–1289. https://doi.org/10.1110/ps.062129506
   PubMed Web of Science ®Google Scholar
• Hegazy, U. M., Mannervik, B., & Stenberg, G. (2004). Functional role of the lock and key motif at the subunit interface of glutathione transferase p1-1. The Journal of Biological Chemistry, 279(10), 9586–9596. https://doi.org/10.1074/jbc.M312320200
   PubMed Web of Science ®Google Scholar
• Hernandez, E. P., Kusakisako, K., Talactac, M. R., Galay, R. L., Hatta, T., Fujisaki, K., Tsuji, N., & Tanaka, T. (2018). Glutathione S-transferases play a role in the detoxification of flumethrin and chlorpyrifos in Haemaphysalis longicornis. Parasites & Vectors, 11(1), 460.
   PubMedGoogle Scholar
• Hernandez, E. P., Shimazaki, K., Niihara, H., Umemiya-Shirafuji, R., Fujisaki, K., & Tanaka, T. (2020). Expression analysis of glutathione S-transferases and ferritins during the embryogenesis of the tick Haemaphysalis longicornis. Heliyon, 6(3), e03644. https://doi.org/10.1016/j.heliyon.2020.e03644
   PubMed Web of Science ®Google Scholar
• Hernandez, E. P., Talactac, M. R., Vitor, R. J. S., Yoshii, K., & Tanaka, T. (2021). An Ixodes scapularis glutathione S-transferase plays a role in cell survival and viability during Langat virus infection of a tick cell line. Acta Tropica, 214, 105763. https://doi.org/10.1016/j.actatropica.2020.105763
   PubMed Web of Science ®Google Scholar
• Hornby, J. A., Codreanu, S. G., Armstrong, R. N., & Dirr, H. W. (2002). Molecular recognition at the dimer interface of a class mu glutathione transferase: Role of a hydrophobic interaction motif in dimer stability and protein function. Biochemistry, 41(48), 14238–14247. https://doi.org/10.1021/bi020548d
   PubMed Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD—Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. https://doi.org/10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Johnson, K. A., Angelucci, F., Bellelli, A., Herve, M., Fontaine, J., Tsernoglou, D., Capron, A., Trottein, F., & Brunori, M. (2003). Crystal structure of the 28 kDa glutathione S-transferase from Schistosoma haematobium. Biochemistry, 42(34), 10084–10094. https://doi.org/10.1021/bi034449r
   PubMed Web of Science ®Google Scholar
• Klafke, G., Webster, A., Agnol, B. D., Pradel, E., Silva, J., de La Canal, L. H., Becker, M., Osorio, M. F., Mansson, M., Barreto, R., Scheffer, R., Souza, U. A., Corassini, V. B., dos Santos, J., Reck, J., & Martins, J. R. (2017). Multiple resistance to acaricides in field populations of Rhipicephalus microplus from Rio Grande do Sul state, Southern Brazil. Ticks and Tick-Borne Diseases, 8(1), 73–80. https://doi.org/10.1016/j.ttbdis.2016.09.019
   PubMed Web of Science ®Google Scholar
• Ku, C.-C., Chiang, F.-M., Hsin, C.-Y., Yao, Y.-E., & Sun, C.-N. (1994). Glutathione transferase isozymes involved in insecticide resistance of diamondback moth larvae. Pesticide Biochemistry and Physiology, 50(3), 191–197. https://doi.org/10.1006/pest.1994.1071
   Web of Science ®Google Scholar
• Kumar, R. (2019). Molecular markers and their application in the monitoring of acaricide resistance in Rhipicephalus microplus. Experimental & Applied Acarology, 78(2), 149–172. https://doi.org/10.1007/s10493-019-00394-0
   PubMed Web of Science ®Google Scholar
• Laborde, E. (2010). Glutathione transferases as mediators of signaling pathways involved in cell proliferation and cell death. Cell Death and Differentiation, 17(9), 1373–1380. https://doi.org/10.1038/cdd.2010.80
   PubMed Web of Science ®Google Scholar
• Le Gall, V. L., Klafke, G. M., & Torres, T. T. (2018). Detoxification mechanisms involved in ivermectin resistance in the cattle tick, Rhipicephalus (Boophilus) microplus. Scientific Reports, 8(1), 12401. https://doi.org/10.1038/s41598-018-30907-7
   PubMedGoogle Scholar
• Li, A. Y., Davey, R. B., Miller, R. J., & George, J. E. (2004). Detection and characterization of amitraz resistance in the southern cattle tick, Boophilus microplus (Acari: Ixodidae). Journal of Medical Entomology, 41(2), 193–200. https://doi.org/10.1603/0022-2585-41.2.193
   PubMed Web of Science ®Google Scholar
• Lindahl, E., Hess, B., & van der Spoel, D. (2001). GROMACS 3.0: A package for molecular simulation and trajectory analysis. Journal of Molecular Modeling, 7(8), 306–317. https://doi.org/10.1007/s008940100045
   Web of Science ®Google Scholar
• Miller, R. J., Davey, R. B., & George, J. E. (1999). Characterization of pyrethroid resistance and susceptibility to coumaphos in Mexican Boophilus microplus (Acari: Ixodidae). Journal of Medical Entomology, 36(5), 533–538. https://doi.org/10.1093/jmedent/36.5.533
   PubMed Web of Science ®Google Scholar
• Miller, R. J., George, J. E., Guerrero, F., Carpenter, L., & Welch, J. B. (2001). Characterization of acaricide resistance in Rhipicephalus sanguineus (latreille) (Acari: Ixodidae) collected from the Corozal Army Veterinary Quarantine Center, Panama. Journal of Medical Entomology, 38(2), 298–302. https://doi.org/10.1603/0022-2585-38.2.298
   PubMed Web of Science ®Google Scholar
• Muller, P., Warr, E., Stevenson, B. J., Pignatelli, P. M., Morgan, J. C., Steven, A., Yawson, A. E., Mitchell, S. N., Ranson, H., Hemingway, J., Paine, M. J., & Donnelly, M. J. (2008). Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLoS Genetics, 4(11), e1000286. https://doi.org/10.1371/journal.pgen.1000286
   PubMed Web of Science ®Google Scholar
• Narasimhan, S., Kurokawa, C., DeBlasio, M., Matias, J., Sajid, A., Pal, U., Lynn, G., & Fikrig, E. (2021). Acquired tick resistance: The trail is hot. Parasite Immunology, 43(5), e12808. https://doi.org/10.1111/pim.12808
   PubMed Web of Science ®Google Scholar
• Parizi, L. F., Utiumi, K. U., Imamura, S., Onuma, M., Ohashi, K., Masuda, A., & da Silva Vaz, I. (2011). Cross immunity with Haemaphysalis longicornis glutathione S-transferase reduces an experimental Rhipicephalus (Boophilus) microplus infestation. Experimental Parasitology, 127(1), 113–118. https://doi.org/10.1016/j.exppara.2010.07.001
   PubMed Web of Science ®Google Scholar
• Parsons, J. F., & Armstrong, R. N. (1996). Proton configuration in the ground state and transition state of a glutathione transferase-catalyzed reaction inferred from the properties of tetradeca (3-fluorotyrosyl) glutathione transferase. Journal of the American Chemical Society, 118(9), 2295–2296. https://doi.org/10.1021/ja960022e
   Web of Science ®Google Scholar
• Pasay, C., Arlian, L., Morgan, M., Gunning, R., Rossiter, L., Holt, D., Walton, S., Beckham, S., & McCarthy, J. (2009). The effect of insecticide synergists on the response of scabies mites to pyrethroid acaricides. PLoS Neglected Tropical Diseases, 3(1), e354. https://doi.org/10.1371/journal.pntd.0000354
   PubMed Web of Science ®Google Scholar
• Patskovsky, Y. V., Patskovska, L. N., & Listowsky, I. (1999). An asparagine-phenylalanine substitution accounts for catalytic differences between hGSTM3-3 and other human class mu glutathione S-transferases. Biochemistry, 38(49), 16187–16194. https://doi.org/10.1021/bi991714t
   PubMed Web of Science ®Google Scholar
• Perbandt, M., Burmeister, C., Walter, R. D., Betzel, C., & Liebau, E. (2004). Native and inhibited structure of a Mu class-related glutathione S-transferase from Plasmodium falciparum. The Journal of Biological Chemistry, 279(2), 1336–1342. https://doi.org/10.1074/jbc.M309663200
   PubMed Web of Science ®Google Scholar
• Pohl, P. C., Klafke, G. M., Júnior, J. R., Martins, J. R., da Silva Vaz, I., & Masuda, A. (2012). ABC transporters as a multidrug detoxification mechanism in Rhipicephalus (Boophilus) microplus. Parasitology Research, 111(6), 2345–2351. https://doi.org/10.1007/s00436-012-3089-1
   PubMed Web of Science ®Google Scholar
• Pongprayoon, P., Kaewhom, P., Kaewmongkol, S., Suwan, E., Stich, R. W., Wiriya, B., & Jittapalapong, S. (2021). Structural dynamics of Rhipicephalus microplus serpin-3. Molecular Simulation, 47(15), 1209–1216. https://doi.org/10.1080/08927022.2021.1962011
   Web of Science ®Google Scholar
• Pongprayoon, P., Niramitranon, J., Kaewhom, P., Kaewmongkol, S., Suwan, E., Stich, R. W., & Jittapalapong, S. (2020). Dynamic and structural insights into tick serpin from Ixodes ricinus. Journal of Biomolecular Structure & Dynamics, 38(8), 2296–2303. https://doi.org/10.1080/07391102.2019.1630003
   PubMed Web of Science ®Google Scholar
• Reddy, B. N., Prasad, G., & Raghavendra, K. (2011). In silico analysis of glutathione S-transferase supergene family revealed hitherto unreported insect specific δ-and ɛ-GSTs and mammalian specific μ-GSTs in Ixodes scapularis (Acari: Ixodidae). Computational Biology and Chemistry, 35(2), 114–120. https://doi.org/10.1016/j.compbiolchem.2011.03.004
   PubMed Web of Science ®Google Scholar
• Ricci, G., Caccuri, A. M., Lo Bello, M., Rosato, N., Mei, G., Nicotra, M., Chiessi, E., Mazzetti, A. P., & Federici, G. (1996). Structural flexibility modulates the activity of human glutathione transferase P1-1. Role of helix 2 flexibility in the catalytic mechanism. The Journal of Biological Chemistry, 271(27), 16187–16192. https://doi.org/10.1074/jbc.271.27.16187
   PubMed Web of Science ®Google Scholar
• Rodriguez-Hidalgo, R., Perez-Otanez, X., Garces-Carrera, S., Vanwambeke, S. O., Madder, M., & Benitez-Ortiz, W. (2017). The current status of resistance to alpha-cypermethrin, ivermectin, and amitraz of the cattle tick (Rhipicephalus microplus) in Ecuador. PloS One, 12(4), e0174652. https://doi.org/10.1371/journal.pone.0174652
   PubMed Web of Science ®Google Scholar
• Sayed, Y., Wallace, L. A., & Dirr, H. W. (2000). The hydrophobic lock-and-key intersubunit motif of glutathione transferase A1-1: Implications for catalysis, ligandin function and stability. FEBS Letters, 465(2-3), 169–172. https://doi.org/10.1016/s0014-5793(99)01747-0
   PubMed Web of Science ®Google Scholar
• Schetters, T., Bishop, R., Crampton, M., Kopacek, P., Lew-Tabor, A., Maritz-Olivier, C., Miller, R., Mosqueda, J., Patarroyo, J., Rodriguez-Valle, M., Scoles, G. A., & de la Fuente, J. (2016). Cattle tick vaccine researchers join forces in CATVAC. Parasites & Vectors, 9(105), 105.
   PubMedGoogle Scholar
• Shahein, Y., Abouelella, A., & Hamed, R. (2013). Glutathione S-Transferase Genes from Ticks. An Integrated View of the Molecular Recognition and Toxinology—From Analytical Procedures to Biomedical Applications. IntechOpen.
   Google Scholar
• Sinning, I., Kleywegt, G. J., Cowan, S. W., Reinemer, P., Dirr, H. W., Huber, R., Gilliland, G. L., Armstrong, R. N., Ji, X., & Board, P. G. (1993). Structure determination and refinement of human alpha class glutathione transferase A1-1, and a comparison with the Mu and Pi class enzymes. Journal of Molecular Biology, 232(1), 192–212. https://doi.org/10.1006/jmbi.1993.1376
   PubMed Web of Science ®Google Scholar
• Stella, L., Caccuri, A. M., Rosato, N., Nicotra, M., Lo Bello, M., De Matteis, F., Mazzetti, A. P., Federici, G., & Ricci, G. (1998). Flexibility of helix 2 in the human glutathione transferase P1-1. time-resolved fluorescence spectroscopy. The Journal of Biological Chemistry, 273(36), 23267–23273. https://doi.org/10.1074/jbc.273.36.23267
   PubMed Web of Science ®Google Scholar
• Stella, L., Nicotra, M., Ricci, G., Rosato, N., & Di Iorio, E. E. (1999). Molecular dynamics simulations of human glutathione transferase P1‐1: Analysis of the induced‐fit mechanism by GSH binding. Proteins: Structure, Function, and Genetics, 37(1), 1–9. https://doi.org/10.1002/(SICI)1097-0134(19991001)37:1<1::AID-PROT1>3.0.CO;2-B
   PubMed Web of Science ®Google Scholar
• Sun, Y. J., Kuan, I. C., Tam, M. F., & Hsiao, C. D. (1998). The three-dimensional structure of an avian class-mu glutathione S-transferase, cGSTM1-1 at 1.94 A resolution. Journal of Molecular Biology, 278(1), 239–252. https://doi.org/10.1006/jmbi.1998.1716
   PubMed Web of Science ®Google Scholar
• Temel, Y., Kocyigit, U. M., Taysi, M. S., Gokalp, F., Gurdere, M. B., Budak, Y., Ceylan, M., Gulcin, I., & Ciftci, M. (2018). Purification of glutathione S-transferase enzyme from quail liver tissue and inhibition effects of (3aR,4S,7R,7aS)-2-(4-((E)-3-(aryl)acryloyl)phenyl)-3a,4,7,7a-tetrahydro-1H-4,7-me thanoisoindole-1,3(2H)-dione derivatives on the enzyme activity. Journal of Biochemical and Molecular Toxicology, 32(3), e22034. https://doi.org/10.1002/jbt.22034
   PubMed Web of Science ®Google Scholar
• Veerapathran, A., Dakshinamoorthy, G., Gnanasekar, M., Reddy, M. V. R., & Kalyanasundaram, R. (2009). Evaluation of Wuchereria bancrofti GST as a vaccine candidate for lymphatic filariasis. PLoS Neglected Tropical Diseases, 3(6), e457. https://doi.org/10.1371/journal.pntd.0000457
   PubMed Web of Science ®Google Scholar
• Walker, A. R. (2014). Ticks and associated diseases: a retrospective review. Medical and Veterinary Entomology, 28(Suppl 1), 1–5. https://doi.org/10.1111/mve.12031
   PubMed Web of Science ®Google Scholar
• Wei, S., Clark, A., & Syvanen, M. (2001). Identification and cloning of a key insecticide-metabolizing glutathione S-transferase (MdGST-6A) from a hyper insecticide-resistant strain of the housefly Musca domestica. Insect Biochemistry and Molecular Biology, 31(12), 1145–1153. https://doi.org/10.1016/S0965-1748(01)00059-5
   PubMed Web of Science ®Google Scholar
• Yang, L., Mei, Y. T., Fang, Q., Wang, J. L., Yan, Z. C., Song, Q. S., Lin, Z., & Ye, G. Y. (2017). Identification and characterization of serine protease inhibitors in a parasitic wasp, Pteromalus puparum. Scientific Reports, 7(1), 1-13. https://doi.org/10.1038/s41598-017-16000-5
   Google Scholar