Investigations on the binding specificity of β-galactoside analogues with human galectin-1 using molecular dynamics simulations

References

• Arifuzzaman, M., Hamza, A., Zannat, S. S., Fahad, R., Rahman, A., Hosen, S. Z., Dash, R., & Hossain, M. K. (2020). Targeting galectin-3 by natural glycosides: A computational approach. Network Modeling Analysis in Health Informatics and Bioinformatics, 9(1), 1–15. https://doi.org/10.1007/s13721-020-0219-z
   Web of Science ®Google Scholar
• Bahar, I., Atilgan, A. R., Demirel, M. C., & Erman, B. (1998). Vibrational dynamics of folded proteins: Significance of slow and fast motions in relation to function and stability. Physical Review Letters, 80(12), 2733–2736. https://doi.org/10.1103/PhysRevLett.80.2733
   Web of Science ®Google Scholar
• Beigoli, S., Sharifi Rad, A., Askari, A., Assaran Darban, R., & Chamani, J. (2019). Isothermal titration calorimetry and stopped flow circular dichroism investigations of the interaction between lomefloxacin and human serum albumin in the presence of amino acids. Journal of Biomolecular Structure and Dynamics, 37(9), 2265–2282. https://doi.org/10.1080/07391102.2018.1491421
   PubMed Web of Science ®Google Scholar
• Blanchard, H., Bum-Erdene, K., Bohari, M. H., & Yu, X. (2016). Galectin-1 inhibitors and their potential therapeutic applications: A patent review. Expert Opinion on Therapeutic Patents, 26(5), 537–554. https://doi.org/10.1517/13543776.2016.1163338
   PubMed Web of Science ®Google Scholar
• Blaser, C., Kaufmann, M., Müller, C., Zimmermann, C., Wells, V., Mallucci, L., & Pircher, H. (1998). β-Galactoside-binding protein secreted by activated T cells inhibits antigen-induced proliferation of T cells. European Journal of Immunology, 28(8), 2311–2319. https://doi.org/10.1002/(SICI)1521-4141(199808)28:08<2311::AID-IMMU2311>3.0.CO;2-G
   PubMed Web of Science ®Google Scholar
• Blessy, J. J., & Sharmila, D. J. S. (2015). Molecular modeling of methyl-α-Neu5Ac analogues docked against cholera toxin-a molecular dynamics study. Glycoconjugate Journal, 32(1–2), 49–67. https://doi.org/10.1007/s10719-014-9570-6
   PubMed Web of Science ®Google Scholar
• Burley, S. K., Berman, H. M., Bhikadiya, C., Bi, C., Chen, L., Costanzo, L. D., Christie, C., Duarte, J. M., Dutta, S., Feng, Z., & Ghosh, S. (2018). Protein Data Bank: The single global archive for 3D macromolecular structure data. Nucleic Acids Research, 47, D520–D528.
   Web of Science ®Google Scholar
• Camby, I., Le Mercier, M., Lefranc, F., & Kiss, R. (2006). Galectin-1: A small protein with major functions. Glycobiology, 16(11), 137R–157R. https://doi.org/10.1093/glycob/cwl025
   PubMed Web of Science ®Google Scholar
• Case, D. A., Betz, R. M., Cerutti, D. S., Cheatham, T. E., III, Darden, T. A., Duke, R. E., Giese, T. J., Gohlke, H., Goetz, A. W., Homeyer, N., & Izadi, S. (2016). AMBER 2016 Reference Manual (pp. 1–923). University of California.
   Google Scholar
• Chen, I. J., & Foloppe, N. (2010). Drug-like bioactive structures and conformational coverage with the LigPrep/ConfGen suite: Comparison to programs MOE and catalyst. Journal of Chemical Information and Modeling, 50(5), 822–839. https://doi.org/10.1021/ci100026x
   PubMed Web of Science ®Google Scholar
• Cummings, R. D., Liu, F. T., & Vasta, G. R. (2017). Galectins. In A. Varki, R. D. Cummings, J. D. Esko, P. Stanley, G. W. Hart, M. Aebi, A. G. Darvill, T. Kinoshita, N. H. Packer, J. H. Prestegard, R. L. Schnaar, & P. H. Seeberger (Eds.), Essentials of glycobiology (3rd ed., pp. 2015–2017). Cold Spring Harbor Laboratory Press.
   Google Scholar
• Cumpstey, I., Carlsson, S., Leffler, H., & Nilsson, U. J. (2005). Synthesis of a phenyl thio-β-D-galactopyranoside library from 1, 5-difluoro-2, 4-dinitrobenzene: Discovery of efficient and selective monosaccharide inhibitors of galectin-7. Organic & Biomolecular Chemistry, 3(10), 1922–1932. https://doi.org/10.1039/b502354h
   PubMed Web of Science ®Google Scholar
• Danesh, N., Navaee Sedighi, Z., Beigoli, S., Sharifi-Rad, A., Saberi, M. R., & Chamani, J. (2018). Determining the binding site and binding affinity of estradiol to human serum albumin and holo-transferrin: Fluorescence spectroscopic, isothermal titration calorimetry and molecular modeling approaches. Journal of Biomolecular Structure and Dynamics, 36(7), 1747–1763. https://doi.org/10.1080/07391102.2017.1333460
   PubMed Web of Science ®Google Scholar
• Di Lella, S., Sundblad, V., Cerliani, J. P., Guardia, C. M., Estrin, D. A., Vasta, G. R., & Rabinovich, G. A. (2011). When galectins recognize glycans: From biochemistry to physiology and back again. Biochemistry, 50(37), 7842–7857. https://doi.org/10.1021/bi201121m
   PubMed Web of Science ®Google Scholar
• Dings, R. P., Miller, M. C., Griffin, R. J., & Mayo, K. H. (2018). Galectins as molecular targets for therapeutic intervention. International Journal of Molecular Sciences, 19(3), 905. https://doi.org/10.3390/ijms19030905
   PubMed Web of Science ®Google Scholar
• Duke, R. E., & Pedersen, L. G. (2003). PMEMD 3. University of North Carolina-Chapel Hill.
   Google Scholar
• Eisold, A., & Labudde, D. (2018). Detailed Analysis of 17β-Estradiol-Aptamer Interactions: A Molecular Dynamics Simulation Study. Molecules, 23(7), 1690. https://doi.org/10.3390/molecules23071690
   PubMed Web of Science ®Google Scholar
• Ford, M. G., Weimar, T., Köhli, T., & Woods, R. J. (2003). Molecular dynamics simulations of galectin‐1‐oligosaccharide complexes reveal the molecular basis for ligand diversity. Proteins: Structure, Function, and Bioinformatics, 53(2), 229–240. https://doi.org/10.1002/prot.10428
   PubMed Web of Science ®Google Scholar
• Friesner, R. A., Banks, J. L., Murphy, R. B., Halgren, T. A., Klicic, J. J., Mainz, D. T., Repasky, M. P., Knoll, E. H., Shelley, M., Perry, J. K., Shaw, D. E., Francis, P., & Shenkin, P. S. (2004). Glide: A new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. Journal of Medicinal Chemistry, 47(7), 1739–1749. https://doi.org/10.1021/jm0306430
   PubMed Web of Science ®Google Scholar
• Friesner, R. A., Murphy, R. B., Repasky, M. P., Frye, L. L., Greenwood, J. R., Halgren, T. A., Sanschagrin, P. C., & Mainz, D. T. (2006). Extra precision glide: Docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes. Journal of Medicinal Chemistry, 49(21), 6177–6196. https://doi.org/10.1021/jm051256o
   PubMed Web of Science ®Google Scholar
• Genheden, S., & Ryde, U. (2015). The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities. Expert Opinion on Drug Discovery, 10(5), 449–461. https://doi.org/10.1517/17460441.2015.1032936
   PubMed Web of Science ®Google Scholar
• He, L., André, S., Siebert, H. C., Helmholz, H., Niemeyer, B., & Gabius, H. J. (2003). Detection of ligand-and solvent-induced shape alterations of cell-growth-regulatory human lectin galectin-1 in solution by small angle neutron and x-ray scattering. Biophysical Journal, 85(1), 511–524. https://doi.org/10.1016/S0006-3495(03)74496-8
   PubMed Web of Science ®Google Scholar
• Hsieh, T. J., Lin, H. Y., Tu, Z., Lin, T. C., Wu, S. C., Tseng, Y. Y., Liu, F. T., Hsu, S. T. D., & Lin, C. H. (2016). Dual thio-digalactoside-binding modes of human galectins as the structural basis for the design of potent and selective inhibitors. Scientific Reports, 6(1), 29457. https://doi.org/10.1038/srep29457
   PubMedGoogle Scholar
• Jain, M., Muthukumaran, J., & Singh, A. K. (2020). Structural and functional characterization of chitin binding lectin from Datura stramonium: Insights from phylogenetic analysis, protein structure prediction, molecular docking and molecular dynamics simulation. Journal of Biomolecular Structure and Dynamics, 39(5), 1698–1619. https://doi.org/10.1080/07391102.2020.1737234
   PubMed Web of Science ®Google Scholar
• Kaminski, G. A., Friesner, R. A., Tirado-Rives, J., & Jorgensen, W. L. (2001). Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides. The Journal of Physical Chemistry B, 105(28), 6474–6487. https://doi.org/10.1021/jp003919d
   Web of Science ®Google Scholar
• Kamshad, M., Jahanshah Talab, M., Beigoli, S., Sharifirad, A., & Chamani, J. (2019). Use of spectroscopic and zeta potential techniques to study the interaction between lysozyme and curcumin in the presence of silver nanoparticles at different sizes. Journal of Biomolecular Structure and Dynamics, 37(8), 2030–2040. https://doi.org/10.1080/07391102.2018.1475258
   PubMed Web of Science ®Google Scholar
• Kim, S., Chen, J., Cheng, T., Gindulyte, A., He, J., He, S., Li, Q., Shoemaker, B. A., Thiessen, P. A., Yu, B., Zaslavsky, L., Zhang, J., & Bolton, E. E. (2019). PubChem 2019 update: Improved access to chemical data. Nucleic Acids Research, 47(D1), D1102–D1109. https://doi.org/10.1093/nar/gky1033
   PubMed Web of Science ®Google Scholar
• Lengauer, T., & Rarey, M. (1996). Computational methods for biomolecular docking. Current Opinion in Structural Biology, 6(3), 402–406. https://doi.org/10.1016/S0959-440X(96)80061-3
   PubMed Web of Science ®Google Scholar
• López-Lucendo, M. F., Solís, D., André, S., Hirabayashi, J., Kasai, K. I., Kaltner, H., Gabius, H. J., & Romero, A. (2004). Growth-regulatory human galectin-1: Crystallographic characterisation of the structural changes induced by single-site mutations and their impact on the thermodynamics of ligand binding. Journal of Molecular Biology, 343(4), 957–970. https://doi.org/10.1016/j.jmb.2004.08.078
   PubMed Web of Science ®Google Scholar
• Maier, J. A., Martinez, C., Kasavajhala, K., Wickstrom, L., Hauser, K. E., & Simmerling, C. (2015). ff14SB: Improving the accuracy of protein side chain and backbone parameters from ff99SB. Journal of Chemical Theory and Computation, 11(8), 3696–3713. https://doi.org/10.1021/acs.jctc.5b00255
   PubMed Web of Science ®Google Scholar
• McGibbon, R. T., Beauchamp, K. A., Harrigan, M. P., Klein, C., Swails, J. M., Hernández, C. X., Schwantes, C. R., Wang, L. P., Lane, T. J., & Pande, V. S. (2015). MDTraj: A modern open library for the analysis of molecular dynamics trajectories. Biophysical Journal, 109(8), 1528–1532. https://doi.org/10.1016/j.bpj.2015.08.015
   PubMed Web of Science ®Google Scholar
• Meynier, C., Feracci, M., Espeli, M., Chaspoul, F., Gallice, P., Schiff, C., Guerlesquin, F., & Roche, P. (2009). NMR and MD investigations of human galectin-1/oligosaccharide complexes. Biophysical Journal, 97(12), 3168–3177. https://doi.org/10.1016/j.bpj.2009.09.026
   PubMed Web of Science ®Google Scholar
• Miller, B. R., III, McGee, T. D., Jr., Swails, J. M., Homeyer, N., Gohlke, H., & Roitberg, A. E. (2012). MMPBSA.py: An efficient program for end-state free energy calculations. Journal of Chemical Theory and Computation, 8(9), 3314–3321. https://doi.org/10.1021/ct300418h
   PubMed Web of Science ®Google Scholar
• Miller, M. C., Nesmelova, I. V., Platt, D., Klyosov, A., & Mayo, K. H. (2009). The carbohydrate-binding domain on galectin-1 is more extensive for a complex glycan than for simple saccharides: Implications for galectin–glycan interactions at the cell surface. Biochemical Journal, 421(2), 211–221. https://doi.org/10.1042/BJ20090265
   PubMedGoogle Scholar
• Mokaberi, P., Reyhani, V., Amiri-Tehranizadeh, Z., Saberi, M. R., Beigoli, S., Samandar, F., & Chamani, J. (2019). New insights into the binding behavior of lomefloxacin and human hemoglobin using biophysical techniques: Binary and ternary approaches. New Journal of Chemistry, 43(21), 8132–8145. https://doi.org/10.1039/C9NJ01048C
   Web of Science ®Google Scholar
• Morris, G. M., Huey, R., & Olson, A. J. (2008). Using autodock for ligand‐receptor docking. Current Protocols in Bioinformatics, 24(1), 8–14. https://doi.org/10.1002/0471250953.bi0814s24
   Google Scholar
• Mukherjee, R., & Yun, J. W. (2015). Lactobionic acid reduces body weight gain in dietinduced obese rats by targeted inhibition of galectin-1. Biochemical and Biophysical Research Communications, 463(4), 1311–1316. https://doi.org/10.1016/j.bbrc.2015.06.114
   PubMed Web of Science ®Google Scholar
• Nesmelova, I. V., Ermakova, E., Daragan, V. A., Pang, M., Menéndez, M., Lagartera, L., Solís, D., Baum, L. G., & Mayo, K. H. (2010). Lactose binding to galectin-1 modulates structural dynamics, increases conformational entropy, and occurs with apparent negative cooperativity. Journal of Molecular Biology, 397(5), 1209–1230. https://doi.org/10.1016/j.jmb.2010.02.033
   PubMed Web of Science ®Google Scholar
• Parasuraman, P., Murugan, V., Selvin, J. F., Gromiha, M. M., Fukui, K., & Veluraja, K. (2015). Theoretical investigation on the glycan‐binding specificity of Agrocybe cylindracea galectin using molecular modeling and molecular dynamics simulation studies. Journal of Molecular Recognition, 28(9), 528–538. https://doi.org/10.1002/jmr.2468
   PubMed Web of Science ®Google Scholar
• Rubinstein, N., Alvarez, M., Zwirner, N. W., Toscano, M. A., Ilarregui, J. M., Bravo, A., Mordoh, J., Fainboim, L., Podhajcer, O. L., & Rabinovich, G. A. (2004). Targeted inhibition of galectin-1 gene expression in tumor cells results in heightened T cell-mediated rejection: A potential mechanism of tumor-immune privilege. Cancer Cell, 5(3), 241–251. https://doi.org/10.1016/S1535-6108(04)00024-8
   PubMed Web of Science ®Google Scholar
• Salameh, B. A., Leffler, H., & Nilsson, U. J. (2005). 3-(1, 2, 3-Triazol-1-yl)-1-thio-galactosides as small, efficient, and hydrolytically stable inhibitors of galectin-3. Bioorganic & Medicinal Chemistry Letters, 15(14), 3344–3346. https://doi.org/10.1016/j.bmcl.2005.05.084
   PubMed Web of Science ®Google Scholar
• Saraboji, K., Håkansson, M., Genheden, S., Diehl, C., Qvist, J., Weininger, U., Nilsson, U. J., Leffler, H., Ryde, U., Akke, M., & Logan, D. T. (2012). The carbohydrate-binding site in galectin-3 is preorganized to recognize a sugarlike framework of oxygens: Ultra-high-resolution structures and water dynamics. Biochemistry, 51(1), 296–306. https://doi.org/10.1021/bi201459p
   PubMed Web of Science ®Google Scholar
• Satelli, A., Rao, P. S., Gupta, P. K., Lockman, P. R., Srivenugopal, K. S., & Rao, U. S. (2008). Varied expression and localization of multiple galectins in different cancer cell lines. Oncology Reports, 19, 587–594.
   PubMed Web of Science ®Google Scholar
• Schwarz, F. P., Ahmed, H., Bianchet, M. A., Amzel, L. M., & Vasta, G. R. (1998). Thermodynamics of bovine spleen galectin-1 binding to disaccharides: Correlation with structure and its effect on oligomerization at the denaturation temperature. Biochemistry, 37(17), 5867–5877. https://doi.org/10.1021/bi9716478
   PubMed Web of Science ®Google Scholar
• Shakibapour, N., Dehghani Sani, F., Beigoli, S., Sadeghian, H., & Chamani, J. (2019). Multi-spectroscopic and molecular modeling studies to reveal the interaction between propyl acridone and calf thymus DNA in the presence of histone H1: Binary and ternary approaches. Journal of Biomolecular Structure and Dynamics, 37(2), 359–371. https://doi.org/10.1080/07391102.2018.1427629
   PubMed Web of Science ®Google Scholar
• Shanmugam, N. R. S., Blessy, J. J., Veluraja, K., & Gromiha, M. M. (2020). ProCaff: Protein-carbohydrate complex binding affinity database. Bioinformatics, 36(11), 3615–3617. https://doi.org/10.1093/bioinformatics/btaa141
   PubMed Web of Science ®Google Scholar
• Sharifi-Rad, A., Mehrzad, J., Darroudi, M., Saberi, M. R., & Chamani, J. (2021). Oil-in-water nanoemulsions comprising Berberine in olive oil: Biological activities, binding mechanisms to human serum albumin or holo-transferrin and QMMD simulations. Journal of Biomolecular Structure and Dynamics, 39(3), 1029–1043. https://doi.org/10.1080/07391102.2020.1724568
   PubMed Web of Science ®Google Scholar
• Sharmila, D. J. S., & Blessy, J. J. (2017). Molecular dynamics of sialic acid analogues complex with cholera toxin and DFT optimization of ethylene glycol-mediated zinc nanocluster conjugation. Journal of Biomolecular Structure and Dynamics, 35(1), 182–206. https://doi.org/10.1080/07391102.2015.1136689
   PubMed Web of Science ®Google Scholar
• Stannard, K. A., Collins, P. M., Ito, K., Sullivan, E. M., Scott, S. A., Gabutero, E., Darren Grice, I., Low, P., Nilsson, U. J., Leffler, H., Blanchard, H., & Ralph, S. J. (2010). Galectin inhibitory disaccharides promote tumour immunity in a breast cancer model. Cancer Letters, 299(2), 95–110. https://doi.org/10.1016/j.canlet.2010.08.005
   PubMed Web of Science ®Google Scholar
• Stillman, B. N., Hsu, D. K., Pang, M., Brewer, C. F., Johnson, P., Liu, F. T., & Baum, L. G. (2006). Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death. The Journal of Immunology, 176(2), 778–789. https://doi.org/10.4049/jimmunol.176.2.778
   PubMed Web of Science ®Google Scholar
• Tasumi, S., & Vasta, G. R. (2007). A galectin of unique domain organization from hemocytes of the Eastern oyster (Crassostrea virginica) is a receptor for the protistan parasite Perkinsus marinus. The Journal of Immunology, 179(5), 3086–3098. https://doi.org/10.4049/jimmunol.179.5.3086
   PubMed Web of Science ®Google Scholar
• Tejler, J., Leffler, H., & Nilsson, U. J. (2005). Synthesis of O-galactosyl aldoximes as potent LacNAc-mimetic galectin-3 inhibitors. Bioorganic & Medicinal Chemistry Letters, 15(9), 2343–2345. https://doi.org/10.1016/j.bmcl.2005.02.079
   PubMed Web of Science ®Google Scholar
• Than, N. G., Romero, R., Goodman, M., Weckle, A., Xing, J., Dong, Z., Xu, Y., Tarquini, F., Szilagyi, A., Gal, P., Hou, Z. (2009). A primate subfamily of galectins expressed at the maternal–fetal interface that promote immune cell death. Proceedings of the National Academy of Sciences, 106, 9731–9736.
   PubMed Web of Science ®Google Scholar
• Vangone, A., Schaarschmidt, J., Koukos, P., Geng, C., Citro, N., Trellet, M. E., Xue, L. C., & Bonvin, A. M. (2019). Large-scale prediction of binding affinity in protein–small ligand complexes: The PRODIGY-LIG web server. Bioinformatics, 35(9), 1585–1587. https://doi.org/10.1093/bioinformatics/bty816
   PubMed Web of Science ®Google Scholar
• Vasta, G. R., Ahmed, H., Nita-Lazar, M., Banerjee, A., Pasek, M., Shridhar, S., Guha, P., & Fernández-Robledo, J. A. (2012). Galectins as self/non-self recognition receptors in innate and adaptive immunity: An unresolved paradox. Frontiers in Immunology, 3, 199. https://doi.org/10.3389/fimmu.2012.00199
   PubMed Web of Science ®Google Scholar
• Vilar, S., Cozza, G., & Moro, S. (2008). Medicinal chemistry and the molecular operating environment (MOE): application of QSAR and molecular docking to drug discovery. Current Topics in Medicinal Chemistry, 8(18), 1555–1572. https://doi.org/10.2174/156802608786786624
   PubMed Web of Science ®Google Scholar
• Wang, E., Sun, H., Wang, J., Wang, Z., Liu, H., Zhang, J. Z., & Hou, T. (2019). End-point binding free energy calculation with MM/PBSA and MM/GBSA: Strategies and applications in drug design. Chemical Reviews, 119(16), 9478–9508. https://doi.org/10.1021/acs.chemrev.9b00055
   PubMed Web of Science ®Google Scholar
• Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., & Case, D. A. (2004). Development and testing of a general amber force field. Journal of Computational Chemistry, 25(9), 1157–1174. https://doi.org/10.1002/jcc.20035
   PubMed Web of Science ®Google Scholar
• Wang, Z., Sun, H., Yao, X., Li, D., Xu, L., Li, Y., Tian, S., & Hou, T. (2016). Comprehensive evaluation of ten docking programs on a diverse set of protein–ligand complexes: The prediction accuracy of sampling power and scoring power. Physical Chemistry Chemical Physics, 18(18), 12964–12975. https://doi.org/10.1039/C6CP01555G
   PubMed Web of Science ®Google Scholar
• Weng, G., Wang, E., Chen, F., Sun, H., Wang, Z., & Hou, T. (2019). Assessing the performance of MM/PBSA and MM/GBSA methods. 9. Prediction reliability of binding affinities and binding poses for protein–peptide complexes. Physical Chemistry Chemical Physics, 21(19), 10135–10145. https://doi.org/10.1039/C9CP01674K
   PubMed Web of Science ®Google Scholar
• Wong, S. E., & Lightstone, F. C. (2011). Accounting for water molecules in drug design. Expert Opinion on Drug Discovery, 6(1), 65–74. https://doi.org/10.1517/17460441.2011.534452
   PubMed Web of Science ®Google Scholar
• Yadav, P., Shahane, G., & Gaikwad, S. (2018). Amaranthus caudatus lectin with polyproline II fold: Conformational and functional transitions and molecular dynamics. Journal of Biomolecular Structure and Dynamics, 36(9), 2203–2215. https://doi.org/10.1080/07391102.2017.1345328
   PubMed Web of Science ®Google Scholar
• Yongye, A. B., Calle, L., Ardá, A., Jiménez-Barbero, J., André, S., Gabius, H.-J., Martínez-Mayorga, K., & Cudic, M. (2012). Molecular recognition of the Thomsen-Friedenreich antigen–threonine conjugate by adhesion/growth regulatory galectin-3: Nuclear magnetic resonance studies and molecular dynamics simulations. Biochemistry, 51(37), 7278–7289. https://doi.org/10.1021/bi300761s
   PubMed Web of Science ®Google Scholar