In silico and in vitro investigations on the protein–protein interactions of glutathione S-transferases with mitogen-activated protein kinase 8 and apoptosis signal-regulating kinase 1

References

• Adler, V., Yin, Z., Fuchs, S. Y., Benezra, M., Rosario, L., Tew, K. D., Pincus, M. R., Sardana, M., Henderson, C. J., Wolf, C. R., Davis, R. J., & Ronai, Z. (1999). Regulation of JNK signaling by GSTp. The EMBO Journal, 18(5), 1321–1334. https://doi.org/https://doi.org/10.1093/emboj/18.5.1321
   PubMed Web of Science ®Google Scholar
• Bateman, A., Martin, M. J., O’Donovan, C., et.al. (2017). UniProt: the universal protein knowledgebase. Nucleic Acids Research, 45, D158–D169.
   PubMed Web of Science ®Google Scholar
• Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., & Bourne, P. E. (2000). The Protein Data Bank. Nucleic Acids Research, 28(1), 235–242. https://doi.org/https://doi.org/10.1093/nar/28.1.235
   PubMed Web of Science ®Google Scholar
• Cho, S. G., Lee, Y. H., Park, H. S., Ryoo, K., Kang, K. W., Park, J., Eom, S. J., Kim, M. J., Chang, T. S., Choi, S. Y., Shim, J., Kim, Y., Dong, M. S., Lee, M. J., Kim, S. G., Ichijo, H., & Choi, E. J. (2001). Glutathione S-transferase mu modulates the stress-activated signals by suppressing apoptosis signal-regulating kinase 1. The Journal of Biological Chemistry, 276(16), 12749–12755. https://doi.org/https://doi.org/10.1074/jbc.M005561200
   PubMed Web of Science ®Google Scholar
• De Beer, T. A. P., Berka, K., Thornton, J. M., & Laskowski, R. A. (2014). PDBsum additions. Nucleic Acids Research, 42, D292–D296. https://doi.org/https://doi.org/10.1093/nar/gkt940
   PubMed Web of Science ®Google Scholar
• De Vries, S. J., Van Dijk, M., & Bonvin, A. M. J. J. (2010). The HADDOCK web server for data-driven biomolecular docking. Nature Protocols, 5(5), 883–897. [Database] https://doi.org/https://doi.org/10.1038/nprot.2010.32
   PubMed Web of Science ®Google Scholar
• Fabrini, R., De Luca, A., Stella, L., Mei, G., Orioni, B., Ciccone, S., Federici, G., Lo Bello, M., & Ricci, G. (2009). Monomer − dimer equilibrium in glutathione transferases: A critical re-examination. Biochemistry, 48(43), 10473–10482. https://doi.org/https://doi.org/10.1021/bi901238t
   PubMed Web of Science ®Google Scholar
• Gilot, D., Loyer, P., Corlu, A., Glaise, D., Lagadic-Gossmann, D., Atfi, A., Morel, F., Ichijo, H., & Guguen-Guillouzo, C. (2002). Liver protection from apoptosis requires both blockage of initiator caspase activities and inhibition of ASK1/JNK pathway via glutathione S-transferase regulation. The Journal of Biological Chemistry, 277(51), 49220–49229. https://doi.org/https://doi.org/10.1074/jbc.M207325200
   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/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/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/https://doi.org/10.1016/j.ijbiomac.2018.08.001
   PubMed Web of Science ®Google Scholar
• Hall, B. G. (2013). Building phylogenetic trees from molecular data with MEGA. Molecular Biology and Evolution, 30(5), 1229–1235. https://doi.org/https://doi.org/10.1093/molbev/mst012
   PubMed Web of Science ®Google Scholar
• Hayes, J. D., Flanagan, J. U., & Jowsey, I. R. (2005). Glutathione transferases. Annual Review of Pharmacology and Toxicology, 45(1), 51–88. https://doi.org/https://doi.org/10.1146/annurev.pharmtox.45.120403.095857
   PubMed Web of Science ®Google Scholar
• Hayes, J. D., & Pulford, D. J. (1995). The glutathione S-transferase supergene family: Regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Critical Reviews in Biochemistry and Molecular Biology, 30(6), 445–600. https://doi.org/https://doi.org/10.3109/10409239509083491
   PubMed Web of Science ®Google Scholar
• Krüger, D. M., & Gohlke, H. (2010). DrugScorePPI webserver: Fast and accurate in silico alanine scanning for scoring protein-protein interactions. Nucleic Acids Research, 38, W480–W486. https://doi.org/https://doi.org/10.1093/nar/gkq471
   PubMed Web of Science ®Google Scholar
• Lian, L. Y. (1998). NMR structural studies of glutathione S-transferase. Cellular and Molecular Life Sciences, 54(4), 359–362. https://doi.org/https://doi.org/10.1007/s000180050164
   PubMed Web of Science ®Google Scholar
• Lo Bello, M., Oakley, A. J., Battistoni, A., Mazzetti, A. P., Nuccetelli, M., Mazzarese, G., Rossjohn, J., Parker, M. W., & Ricci, G. (1997). Multifunctional role of Tyr 108 in the catalytic mechanism of human glutathione transferase P1-1. Crystallographic and kinetic studies on the Y108F mutant enzyme. Biochemistry, 36(20), 6207–6217. https://doi.org/https://doi.org/10.1021/bi962813z
   PubMed Web of Science ®Google Scholar
• Lu, W. D., & Atkins, W. M. (2004). A novel antioxidant role for ligandin behavior of glutathione S-transferases: Attenuation of the photodynamic effects of hypericin. Biochemistry, 43(40), 12761–12769. https://doi.org/https://doi.org/10.1021/bi049217m
   PubMed Web of Science ®Google Scholar
• Ma, F. Y., Tesch, G. H., Flavell, R. A., Davis, R. J., & Nikolic-Paterson, D. J. (2007). MKK3-p38 signaling promotes apoptosis and the early inflammatory response in the obstructed mouse kidney. American Journal of Physiology. Renal Physiology, 293(5), F1556–F1563. https://doi.org/https://doi.org/10.1152/ajprenal.00010.2007
   PubMed Web of Science ®Google Scholar
• Ma, F. Y., Tesch, G. H., & Nikolic-Paterson, D. J. (2014). ASK1/p38 signaling in renal tubular epithelial cells promotes renal fibrosis in the mouse obstructed kidney. American Journal of Physiology. Renal Physiology, 307(11), F1263–F1273. https://doi.org/https://doi.org/10.1152/ajprenal.00211.2014
   PubMed Web of Science ®Google Scholar
• Mollica, L., Theret, I., Antoine, M., Perron-Sierra, F., Charton, Y., Fourquez, J. M., Wierzbicki, M., Boutin, J. A., Ferry, G., Decherchi, S., Bottegoni, G., Ducrot, P., & Cavalli, A. (2016). Molecular dynamics simulations and kinetic measurements to estimate and predict protein-ligand residence times. Journal of Medicinal Chemistry, 59(15), 7167–7176. https://doi.org/https://doi.org/10.1021/acs.jmedchem.6b00632
   PubMed Web of Science ®Google Scholar
• Nebert, D. W., & Vasiliou, V. (2004). Analysis of the glutathione S-transferase (GST) gene family. Human Genomics, 1(6), 460–464. https://doi.org/https://doi.org/10.1186/1479-7364-1-6-460
   PubMedGoogle Scholar
• Oakley, A. J., Bello, M., Lo, Battistoni, A., Ricci, G., Rossjohn, J., Villar, H. O., & Parker, M. W. (1997). The structures of human glutathione transferase P1-1 in complex with glutathione and various inhibitors at high resolution. Journal of Molecular Biology, 274(1), 84–100. https://doi.org/https://doi.org/10.1006/jmbi.1997.1364
   PubMed Web of Science ®Google Scholar
• Patskovsky, Y., Patskovska, L., Almo, S. C., & Listowsky, I. (2006). Transition state model and mechanism of nucleophilic aromatic substitution reactions catalyzed by human glutathione S-transferase M1a-1a. Biochemistry, 45(12), 3852–3862. https://doi.org/https://doi.org/10.1021/bi051823+
   PubMed Web of Science ®Google Scholar
• Patskovsky, Y. V., Patskovska, L. N., & Listowsky, I. (2000). The enhanced affinity for thiolate anion and activation of enzyme-bound glutathione is governed by an arginine residue of human Mu class glutathione S-transferases. The Journal of Biological Chemistry, 275(5), 3296–3304. https://doi.org/https://doi.org/10.1074/jbc.275.5.3296
   PubMed Web of Science ®Google Scholar
• Robertson, M. J.,Tirado-Rives, J., &Jorgensen, W. L. (2015). Improved Peptide and Protein Torsional Energetics with the OPLSAA Force Field. Journal of Chemical Theory and Computation, 11(7), 3499–3509. https://doi.org/10.1021/acs.jctc.5b00356 26190950
   PubMed Web of Science ®Google Scholar
• Robin, S. K. D., Ansari, M., & Uppugunduri, C. R. S. (2020). Spectrophotometric Screening for Potential Inhibitors of Cytosolic Glutathione S-Transferases. Journal of Visualized Experiments, e61347.
   Google Scholar
• Rother, K. (2005). Methods in Molecular Biology (Clifton, N.J.), 635, 32.
   Google Scholar
• Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Soding, J., Thompson, J. D., & Higgins, D. G. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology, 7(1), 539–539. https://doi.org/https://doi.org/10.1038/msb.2011.75
   PubMed Web of Science ®Google Scholar
• Tars, K., Larsson, A.-K., Shokeer, A., Olin, B., Mannervik, B., & Kleywegt, G. J. (2006). Structural basis of the suppressed catalytic activity of wild-type human glutathione transferase T1-1 compared to its W234R mutant. Journal of Molecular Biology, 355(1), 96–105. https://doi.org/https://doi.org/10.1016/j.jmb.2005.10.049
   PubMed Web of Science ®Google Scholar
• Taslimi, P., Işık, M., Türkan, F., Durgun, M., Türkeş, C., Gülçin, İ., & Beydemir, Ş. (2020). Journal of Biomolecular Structure and Dynamics, 1–12.
   Web of Science ®Google Scholar
• Temel, Y., Koçyigit, U. M., Taysı, M. Ş., Gökalp, F., Gürdere, M. B., Budak, Y., Ceylan, M., Gülçin, İ., & Çiftci, 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-methanoisoindole-1,3(2H)-dione derivatives on the enzyme activity. Journal of Biochemical and Molecular Toxicology, 32(3), e22034. https://doi.org/https://doi.org/10.1002/jbt.22034
   PubMed Web of Science ®Google Scholar
• Tobiume, K., Matsuzawa, A., Takahashi, T., Nishitoh, H., Morita, K., Takeda, K., Minowa, O., Miyazono, K., Noda, T., & Ichijo, H. (2001). ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Reports, 2(3), 222–228. https://doi.org/https://doi.org/10.1093/embo-reports/kve046
   PubMed Web of Science ®Google Scholar
• Türkan, F., Huyut, Z., Taslimi, P., Huyut, M. T., & Gülçin, İ. (2020). Investigation of the effects of cephalosporin antibiotics on glutathione S-transferase activity in different tissues of rats in vivo conditions in order to drug development research. Drug and Chemical Toxicology, 43(4), 423–428. https://doi.org/https://doi.org/10.1080/01480545.2018.1497644
   PubMed Web of Science ®Google Scholar
• Uhlén, M., Fagerberg, L., Hallström, B. M., Lindskog, C., Oksvold, P., Mardinoglu, A., Sivertsson, Å., Kampf, C., Sjöstedt, E., Asplund, A., Olsson, I., Edlund, K., Lundberg, E., Navani, S., Szigyarto, C. A.-K., Odeberg, J., Djureinovic, D., Takanen, J. O., Hober, S., … Pontén, F. (2015). Proteomics. Tissue-based map of the human proteome. Science (New York, N.Y.), 347(6220), 1260419. https://doi.org/https://doi.org/10.1126/science.1260419
   PubMed Web of Science ®Google Scholar
• Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. C. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718. [Database] https://doi.org/https://doi.org/10.1002/jcc.20291
   PubMed Web of Science ®Google Scholar
• Wang, L., Groves, M. J., Hepburn, M. D., & Bowen, D. T. (2000). Glutathione S-transferase enzyme expression in hematopoietic cell lines implies a differential protective role for T1 and A1 isoenzymes in erythroid and for M1 in lymphoid lineages. Haematologica, 85(6), 573–579.
   PubMed Web of Science ®Google Scholar
• Wu, Y., Fan, Y., Xue, B., Luo, L., Shen, J., Zhang, S., Jiang, Y., & Yin, Z. (2006). Human glutathione S-transferase P1-1 interacts with TRAF2 and regulates TRAF2-ASK1 signals. Oncogene, 25(42), 5787–5800. https://doi.org/https://doi.org/10.1038/sj.onc.1209576
   PubMed Web of Science ®Google Scholar