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Research Articles

Sialic acid analog as inhibitor for human coronavirus OC43-a study by molecular dynamics simulations

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Pages 197-215 | Received 02 Nov 2023, Accepted 26 Feb 2024, Published online: 09 Mar 2024

References

  • Lu, H.; Stratton, C. W.; Tang, Y. W. Outbreak of Pneumonia of Unknown Etiology in Wuhan, China: The Mystery and the Miracle. J. Med. Virol. 2020, 92(4), 401–402. DOI: 10.1002/jmv.25678.
  • Sohrabi, C.; Alsafi, Z.; O'Neill, N.; Khan, M.; Kerwan, A.; Al-Jabir, A.; Iosifidis, C.; Agha, R. World Health Organization Declares Global Emergency: A Review of the 2019 Novel Coronavirus (COVID-19). Int. J. Surg. 2020, 76, 71–76. DOI: 10.1016/j.ijsu.2020.02.034.
  • Rosenthal, P. B.; Zhang, X.; Formanowski, F.; Fitz, W.; Wong, C. H.; Meier-Ewert, H.; Skehel, J. J.; Wiley, D. C. Structure of the Haemagglutinin-Esterase-Fusion Glycoprotein of Influenza C Virus. Nature 1998, 396(6706), 92–96. DOI: 10.1038/23974.
  • Tortorici, M. A.; Veesler, D. Structural Insights into Coronavirus Entry. Adv. Virus Res. 2019, 105, 93–116. DOI: 10.1016/bs.aivir.2019.08.002.
  • Zeng, Q.; Langereis, M. A.; Van Vliet, A. L.; Huizinga, E. G.; De Groot, R. J. Structure of Coronavirus Hemagglutinin-Esterase Offers Insight into Corona and Influenza Virus Evolution. Proc. Natl. Acad. Sci. U.S.A. 2008, 105(26), 9065–9069. DOI: 10.1073/pnas.0800502105.
  • Belouzard, S.; Chu, V. C.; Whittaker, G. R. Activation of the SARS Coronavirus Spike Protein via Sequential Proteolytic Cleavage at Two Distinct Sites. Proc. Natl. Acad. Sci. U.S.A. 2009, 106(14), 5871–5876. DOI: 10.1073/pnas.0809524106.
  • Millet, J. K.; Whittaker, G. R. Host Cell Proteases: Critical Determinants of Coronavirus Tropism and Pathogenesis. Virus Res. 2015, 202, 120–134. DOI: 10.1016/j.virusres.2014.11.021.
  • Park, Y. J.; Walls, A. C.; Wang, Z.; Sauer, M. M.; Li, W.; Tortorici, M. A.; Bosch, B. J.; DiMaio, F.; Veesler, D. Structures of MERS-CoV Spike Glycoprotein in Complex with Sialoside Attachment Receptors. Nat. Struct. Mol. Biol. 2019, 26(12), 1151–1157. DOI: 10.1038/s41594-019-0334-7.
  • Raj, V. S.; Mou, H.; Smits, S. L.; Dekkers, D. H. W.; Müller, M. A.; Dijkman, R.; Muth, D.; Demmers, J. A. A.; Zaki, A.; Fouchier, R. A. M.; et al. Dipeptidyl Peptidase 4 Is a Functional Receptor for the Emerging Human Coronavirus-EMC. Nature 2013, 495(7440), 251–254. DOI: 10.1038/nature12005.
  • Hulswit, R. J. G.; Lang, Y.; Bakkers, M. J. G.; Li, W.; Li, Z.; Schouten, A.; Ophorst, B.; van Kuppeveld, F. J. M.; Boons, G.-J.; Bosch, B.-J.; et al. Human Coronaviruses OC43 and HKU1 Bind to 9-O-Ac-Sia via a Conserved Receptor-Binding Site in Spike Protein Domain A. Proc. Natl. Acad. Sci. U.S.A. 2019, 116(7), 2681–2690. DOI: 10.1073/pnas.1809667116.
  • Tortorici, M. A.; Walls, A. C.; Lang, Y.; Wang, C.; Li, Z.; Koerhuis, D.; Boons, G. J.; Bosch, B. J.; Rey, F. A.; de Groot, R. J.; Veesler, D. Structural Basis for Human Coronavirus Attachment to Sialic Acid Receptors. Nat. Struct. Mol. Biol. 2019, 26(6), 481–489. DOI: 10.1038/s41594-019-0233-y.
  • De Groot, R. J. Structure, Function and Evolution of the Hemagglutinin-Esterase Proteins of Corona- and Toroviruses. Glycoconj. J. 2006, 23(1–2), 59–72. DOI: 10.1007/s10719-006-5438-8.
  • Bakkers, M. J. G.; Lang, Y.; Feitsma, L. J.; Hulswit, R. J. G.; de Poot, S. A. H.; van Vliet, A. L. W.; Margine, I.; de Groot-Mijnes, J. D. F.; van Kuppeveld, F. J. M.; Langereis, M. A.; et al. Betacoronavirus Adaptation to Humans Involved Progressive Loss of Hemagglutinin-Esterase Lectin Activity. Cell Host Microbe 2017, 21(3), 356–366. DOI: 10.1016/j.chom.2017.02.008.
  • Song, H.; Qi, J.; Khedri, Z.; Diaz, S.; Yu, H.; Chen, X.; Varki, A.; Shi, Y.; Gao, G. F. Correction: An Open Receptor-Binding Cavity of Hemagglutinin-Esterase-Fusion Glycoprotein from Newly-Identified Influenza D Virus: Basis for Its Broad Cell Tropism. PLOS Pathog. 2016, 12(3), e1005505. DOI: 10.1371/journal.ppat.1005505.
  • Schauer, R.; Kelm, S.; Reuter, G.; Roggentin, P.; Shaw, L. Biochemistry and Role of Sialic Acids. In Biology of the Sialic Acids; Springer: Boston, MA, 1995; pp 7–67.
  • Varki, A.; Schnaar, R. L.; Schauer, R. 2017 Sialic Acids and Other Nonulosonic Acids. In Essentials of Glycobiology, 3rd ed. Cold Spring Harbor Laboratory Press: New York, USA.
  • Veluraja, K.; Shanmugam, N. R. S.; Blessy, J. J.; Jeyaram, R. A.; Lalithamaheswari, B.; Gromiha, M. M. Protein-Carbohydrate Complexes: Binding Site Analysis, Prediction, Binding Affinity and Molecular Dynamics Simulations. In Protein Interactions: Computational Methods, Analysis and Applications; Gromiha, M. M., Ed.; World Scientific Press: Singapore, 2020; pp 299–332.
  • Blessy, J. J.; Jawahar, D.; Sharmila, D. J.; S. Multivalent Interactions of Nano-spaced Dimers of N-Acetylneuraminic Acid Analogues Complex with H5N1 Influenza Viral Neuraminidase and Haemagglutinin-A Molecular Dynamics Investigation. Int. J. Curr. Microbiol. Appl. Sci. 2019, 8(01), 1517–1546. DOI: 10.20546/ijcmas.2019.801.161.
  • Sharmila, D. J. S.; Blessy, J. J. Molecular Dynamics of Sialic Acid Analogues Complex with Cholera Toxin and DFT Optimization of Ethylene Glycol-Mediated Zinc Nanocluster Conjugation. J. Biomol. Struct. Dyn. 2017, 35(1), 182–206. DOI: 10.1080/07391102.2015.1136689.
  • Sun, X. L. The Role of Cell Surface Sialic Acids for SARS-CoV-2 Infection. Glycobiology 2021, 31(10), 1245–1253. DOI: 10.1093/glycob/cwab032.
  • Petitjean, S. J.; Chen, W.; Koehler, M.; Jimmidi, R.; Yang, J.; Mohammed, D.; Juniku, B.; Stanifer, M.L.; Boulant, S.; Vincent, S.P.; Alsteens, D. Multivalent 9-O-Acetylated-Sialic Acid Glycoclusters as Potent Inhibitors for SARS-CoV-2 Infection. Nat. Commun. 2022, 13(1), 2564. DOI: 10.1038/s41467-022-30313-8.
  • Peng, G.; Sun, D.; Rajashankar, K. R.; Qian, Z.; Holmes, K. V.; Li, F. Crystal Structure of Mouse Coronavirus Receptor-Binding Domain Complexed with Its Murine Receptor. Proc. Natl. Acad. Sci. U.S.A. 2011, 108(26), 10696–10701. DOI: 10.1073/pnas.1104306108.
  • Peng, G.; Xu, L.; Lin, Y. L.; Chen, L.; Pasquarella, J. R.; Holmes, K. V.; Li, F. Crystal Structure of Bovine Coronavirus Spike Protein Lectin Domain. J. Biol. Chem. 2012, 287(50), 41931–41938. DOI: 10.1074/jbc.M112.418210.
  • Huang, X.; Dong, W.; Milewska, A.; Golda, A.; Qi, Y.; Zhu, Q. K.; Marasco, W. A.; Baric, R. S.; Sims, A. C.; Pyrc, K.; et al. Human Coronavirus HKU1 Spike Protein Uses O-Acetylated Sialic Acid as an Attachment Receptor Determinant and Employs Hemagglutinin-Esterase Protein as a Receptor-Destroying Enzyme. J. Virol. 2015, 89(14), 7202–7213. DOI: 10.1128/JVI.00854-15.
  • Weimar, T.; Woods, R. J. Combining NMR and Simulation Methods in Oligosaccharide Conformational Analysis. In NMR Spectroscopy of Glycoconjugates; Jiménez-Barbero, J., Peters, T., Eds.; Wiley-VCH Verlag GmbH & Co. KgaA: Weinheim, Germany, 2002; pp 109–144.
  • Bickelhaupt, F. M.; Baerends, E. J.; Lipkowitz, K. B.; Boyd, D. B. Reviews in Computational Chemistry. Wiley-VCH 2000, 15, 1–86.
  • Wallace, A. C.; Laskowski, R. A.; Thornton, J. M. LIGPLOT: A Program to Generate Schematic Diagrams of Protein-Ligand Interactions. Protein Eng. 1996, 8(2), 127–134. DOI: 10.1093/protein/8.2.127.
  • Engin, A. B.; Engin, E. D.; Engin, A. Dual Function of Sialic Acid in Gastrointestinal SARS-CoV-2 Infection. Environ. Toxicol. Pharmacol. 2020, 79, 103436. DOI: 10.1016/j.etap.2020.103436.
  • Blessy, J. J.; Sharmila, D. J.; S. Molecular Simulation of N-Acetylneuraminic Acid Analogs and Molecular Dynamics Studies of Cholera Toxin-Neu5Gc Complex. J. Biomol. Struct. Dyn. 2015, 33(5), 1126–1139. DOI: 10.1080/07391102.2014.931825.
  • Haselhorst, T.; Wilson, J. C.; Thomson, R. J.; McAtamney, S.; Menting, J. G.; Coppel, R. L.; von Itzstein, M. Saturation Transfer Difference (STD) 1H‐NMR Experiments and In Silico Docking Experiments to Probe the Binding of N‐Acetylneuraminic Acid and Derivatives to Vibrio cholerae Sialidase. Proteins 2004, 56(2), 346–353. DOI: 10.1002/prot.20143.
  • Shi, Y.; Si, L.; Han, X.; Fan, Z.; Wang, S.; Li, M.; Sun, J.; Zhang, Y.; Zhou, D.; Xiao, S. Synthesis of Novel Pentacyclic Triterpene–Neu5Ac2en Derivatives and Investigation of Their In Vitro Anti-Influenza Entry Activity. MedChemComm. 2017, 8(7), 1531–1541. DOI: 10.1039/c7md00245a.
  • Tomris, I.; Unione, L.; Nguyen, L.; Zaree, P.; Bouwman, K. M.; Liu, L.; Li, Z.; Fok, J. A.; Ríos Carrasco, M.; van der Woude, R.; et al. SARS-CoV-2 Spike N-Terminal Domain Engages 9-O-Acetylated α2–8-Linked Sialic Acids. ACS Chem. Biol. 2023, 18(5), 1180–1191. DOI: 10.1021/acschembio.3c00066.
  • Sargsyan, K.; Grauffel, C.; Lim, C. How Molecular Size Impacts RMSD Applications in Molecular Dynamics Simulations. J. Chem. Theory Comput. 2017, 13(4), 1518–1524. DOI: 10.1021/acs.jctc.7b00028.
  • Eisold, A.; Labudde, D. Detailed Analysis of 17β-Estradiol-Aptamer Interactions: A Molecular Dynamics Simulation Study. Molecules 2018, 23(7), 23–1690. DOI: 10.3390/molecules23071690.
  • Li, Z.; Lang, Y.; Liu, L.; Bunyatov, M. I.; Sarmiento, A. I.; de Groot, R. J.; Boons, G. J. Synthetic O-Acetylated Sialosides Facilitate Functional Receptor Identification for Human Respiratory Viruses. Nat. Chem. 2021, 13(5), 496–503. DOI: 10.1038/s41557-021-00655-9.
  • Burley, S. K.; Bhikadiya, C.; Bi, C.; Bittrich, S.; Chen, L.; Crichlow, G. V.; Christie, C. H.; Dalenberg, K.; Costanzo, L. D.; Duarte, J. M.; et al. RCSB Protein Data Bank: Powerful New Tools for Exploring 3D Structures of Biological Macromolecules for Basic and Applied Research and Education in Fundamental Biology, Biomedicine, Biotechnology, Bioengineering and Energy Sciences. Nucleic Acids Res. 2021, 49(D1), D437–D451. DOI: 10.1093/nar/gkaa1038.
  • 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.; et al. Reference Manual; University of California: San Francisco, CA, 2016; pp 1–923.
  • Veluraja, K.; Selvin, J. F. A.; Venkateshwari, S.; Priyadarzini, T. R.; K. 3DSDSCAR – A Three Dimensional Structural Database for Sialic Acid – Containing Carbohydrate through Molecular Dynamic Simulation. Carbohydr. Res. 2010, 345(14), 2030–2037. DOI: 10.1016/j.carres.2010.06.021.
  • Kim, S.; Chen, J.; Cheng, T.; Gindulyte, A.; He, J.; He, S.; Li, Q.; Shoemaker, B. A.; Thiessen, P. A.; Yu, B.; et al. PubChem 2019 Update: Improved Access to Chemical Data. Nucleic Acids Res. 2019, 47(D1), D1102–D1109. DOI: 10.1093/nar/gky1033.
  • Hunter, A. D. ACD/ChemSketch 1.0 (Freeware); ACD/ChemSketch 2.0 and Its Tautomers, Dictionary, and 3D Plug-Ins; ACD/HNMR 2.0; ACD/CNMR 2.0, 1997.
  • Morris, G. M.; Huey, R.; Lindstrom, W.; Sanner, M. F.; Belew, R. K.; Goodsell, D. S.; Olson, A. J. AutoDock4 and AutoDockTools4: Automated Docking with Selective Receptor Flexibility. J. Comput. Chem. 2009, 30(16), 2785–2791. DOI: 10.1002/jcc.21256.
  • Salomon-Ferrer, R.; Götz, A. W.; Poole, D.; Le Grand, S.; Walker, R. C. Routine Microsecond Molecular Dynamics Simulations with AMBER Part II: Particle Mesh Ewald. J. Chem. Theory Comput. 2013, 9(9), 3878–3888. DOI: 10.1021/ct400314y.
  • Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kalé, L.; Schulten, K. Scalable Molecular Dynamics with NAMD. J. Comput. Chem. 2005, 26(16), 1781–1802. DOI: 10.1002/jcc.20289.

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