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Research Articles

One microsecond MD simulations of the SARS-CoV-2 main protease and hydroxychloroquine complex reveal the intricate nature of binding

ORCID Icon, ORCID Icon, , ORCID Icon & ORCID Icon
Pages 10763-10770 | Received 10 Sep 2020, Accepted 22 Jun 2021, Published online: 29 Jul 2021

References

  • Baildya, N., Ghosh, N. N., & Chattopadhyay, A. P. (2020). Inhibitory activity of hydroxychloroquine on COVID-19 main protease: An insight from MD-simulation studies. Journal of Molecular Structure, 1219, 128595. https://doi.org/10.1016/j.molstruc.2020.128595
  • Ben-Zvi, I., Kivity, S., Langevitz, P., & Shoenfeld, Y. (2012). Hydroxychloroquine: From malaria to autoimmunity. Clinical Reviews in Allergy and Immunology, 42(2), 145–153. https://doi.org/10.1007/s12016-010-8243-x
  • Berendsen, H. J. C., van der Spoel, D., & van Drunen, R. (1995). GROMACS: A message-passing parallel molecular dynamics implementation. Computer Physics Communications, 91(1–3), 43–56. https://doi.org/10.1016/0010-4655(95)00042-E
  • Bhardwaj, V. K., Singh, R., Sharma, J., Rajendran, V., Purohit, R., & Kumar, S. (2021). Identification of bioactive molecules from tea plant as SARS-CoV-2 main protease inhibitors. Journal of Biomolecular Structure & Dynamics, 39(10), 3449–3458. https://doi.org/10.1080/07391102.2020.1766572
  • Brown, S. M., Peltan, I. D., Webb, B., Kumar, N., Starr, N., Grissom, C., Buckel, W. R., Srivastava, R., Harris, E. S., Leither, L. M., Johnson, S. A., Paine, R., & Greene, T. (2020). Hydroxychloroquine versus azithromycin for hospitalized patients with suspected or confirmed COVID-19 (HAHPS). Protocol for a pragmatic, open-label, active comparator trial. Annals of the American Thoracic Society, 17(8), 1008–1015. https://doi.org/10.1513/AnnalsATS.202004-309SD
  • Chandran, A. V., Jayanthi, S., & Vijayan, M. (2018). Structure and interactions of RecA: Plasticity revealed by molecular dynamics simulations. Journal of Biomolecular Structure & Dynamics, 36(1), 98–111. https://doi.org/10.1080/07391102.2016.1268975
  • Duverger, E., Herlem, G., & Picaud, F. (2021). A potential solution to avoid overdose of mixed drugs in the event of Covid-19: Nanomedicine at the heart of the Covid-19 pandemic. Journal of Molecular Graphics & Modelling, 104, 107834. https://doi.org/10.1016/j.jmgm.2021.107834
  • 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
  • Giri, R., Bhardwaj, T., Shegane, M., Gehi, B. R., Kumar, P., Gadhave, K., Oldfield, C. J., & Uversky, V. N. (2021). Understanding COVID-19 via comparative analysis of dark proteomes of SARS-CoV-2, human SARS and bat SARS-like coronaviruses. Cellular and Molecular Life Sciences, 78(4), 1655–1688. https://doi.org/10.1007/s00018-020-03603-x
  • Grau-Pujol, B., Camprubí, D., Marti-Soler, H., Fernández-Pardos, M., Guinovart, C., & Muñoz, J. (2020, December 29). Pre-exposure prophylaxis with hydroxychloroquine for high-risk healthcare workers during the COVID-19 pandemic: A structured summary of a study protocol for a multicentre, double-blind randomized controlled trial. Trials. 21(1), 688. https://doi.org/10.1186/s13063-020-04621-7
  • Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. G. E. M. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. https://doi.org/10.1002/(SICI)1096-987X(199709)18:12 < 1463::AID-JCC4 > 3.0.CO;2-H
  • Hospital, A., Goñi, J. R., Orozco, M., & Gelpí, J. L. (2015). Molecular dynamics simulations: Advances and applications. Advances and Applications in Bioinformatics and Chemistry, 8, 37–47. https://doi.org/10.2147/AABC.S70333
  • Huynh, T., Wang, H., & Luan, B. (2020). In silico exploration of the molecular mechanism of clinically oriented drugs for possibly inhibiting SARS-CoV-2's main protease . The Journal of Physical Chemistry Letters, 11(11), 4413–4420. https://doi.org/10.1021/acs.jpclett.0c00994
  • Jacobson, M. P., Pincus, D. L., Rapp, C. S., Day, T. J. F., Honig, B., Shaw, D. E., & Friesner, R. A. (2004). A hierarchical approach to all-atom protein loop prediction. Proteins, 55(2), 351–367. https://doi.org/10.1002/prot.10613
  • Keyaerts, E., Vijgen, L., Maes, P., Neyts, J., & Ranst, M. & Van, (2004). In vitro inhibition of severe acute respiratory syndrome coronavirus by chloroquine. Biochemical and Biophysical Research Communications, 323(1), 264–268. https://doi.org/10.1016/j.bbrc.2004.08.085
  • Kingsmore, K. M., Grammer, A. C., & Lipsky, P. E. (2020, January 1). Drug repurposing to improve treatment of rheumatic autoimmune inflammatory diseases. Nature Reviews. Rheumatology, 16(1), 32–52. https://doi.org/10.1038/s41584-019-0337-0
  • Klepeis, J. L., Lindorff-Larsen, K., Dror, R. O., & Shaw, D. E. (2009, April 1). Long-timescale molecular dynamics simulations of protein structure and function. Current Opinion in Structural Biology, 19(2), 120–127. https://doi.org/10.1016/j.sbi.2009.03.004
  • Kumar, P., Bhardwaj, T., Kumar, A., Gehi, B. R., Kapuganti, S. K., Garg, N., Nath, G., & Giri, R. (2020). Reprofiling of approved drugs against SARS-CoV-2 main protease: An in-silico study. Journal of Biomolecular Structure and Dynamics, 1–15. https://doi.org/10.1080/07391102.2020.1845976
  • Kumar, A., Liang, B., Aarthy, M., Singh, S. K., Garg, N., Mysorekar, I. U., & Giri, R. (2018). Hydroxychloroquine inhibits zika virus NS2B-NS3 protease. ACS Omega, 3(12), 18132–18141. https://doi.org/10.1021/acsomega.8b01002
  • Larsson, D. S. D. D., Liljas, L., & van der Spoel, D. (2012). Virus capsid dissolution studied by microsecond molecular dynamics simulations. PLoS Computational Biology, 8(5), e1002502 https://doi.org/10.1371/journal.pcbi.1002502
  • Li, X., Wang, Y., Agostinis, P., Rabson, A., Melino, G., Carafoli, E., Shi, Y., & Sun, E. (2020). Is hydroxychloroquine beneficial for COVID-19 patients? Cell Death and Disease, 11(7), 1–6. https://doi.org/10.1038/s41419-020-2721-8
  • Liu, J., Cao, R., Xu, M., Wang, X., Zhang, H., Hu, H., Li, Y., Hu, Z., Zhong, W., & Wang, M. (2020). Hydroxychloroquine, a less toxic derivative of chloroquine, is effective in inhibiting SARS-CoV-2 infection in vitro. Cell Discovery, 6(1), 16. https://doi.org/10.1038/s41421-020-0156-0
  • Malik, J., Soni, H., Sharma, S., & Sarankar, S. (2020). Hydroxychloroquine as potent inhibitor of COVID-19 main protease: Grid based docking approach. Eurasian Journal of Medicine and Oncology, 4(3), 219–226. https://doi.org/10.14744/ejmo.2020.91607
  • McChesney, E. W. (1983). Animal toxicity and pharmacokinetics of hydroxychloroquine sulfate. The American Journal of Medicine, 75(1A), 11–18. https://doi.org/10.1016/0002-9343(83)91265-2
  • Morand, E. F., McCloud, P. I., & Littlejohn, G. O. (1992). Continuation of long term treatment with hydroxychloroquine in systemic lupus erythematosus and rheumatoid arthritis. Annals of the Rheumatic Diseases, 51(12), 1318–1321. https://doi.org/10.1136/ard.51.12.1318
  • Perilla, J. R., Goh, B. C., Cassidy, C. K., Liu, B., Bernardi, R. C., Rudack, T., Yu, H., Wu, Z., & Schulten, K. (2015, April 1). Molecular dynamics simulations of large macromolecular complexes. Current Opinion in Structural Biology, 31, 64–74. https://doi.org/10.1016/j.sbi.2015.03.007
  • Perilla, J. R., & Schulten, K. (2017, May). Physical properties of the HIV-1 capsid from all-atom molecular dynamics simulations. Nature Communications, 8, 15959–15910. https://doi.org/10.1038/ncomms15959
  • Picaud, F., & Herlem, G. (2021). Hydroxychloroquine and azithromycin molecular action against SARS-CoV-2 viral protein: A molecular dynamic study. Austin Journal of Nanomedicine Nanotechnology, 9(1), 1–8.
  • Pushpakom, S., Iorio, F., Eyers, P. A., Escott, K. J., Hopper, S., Wells, A., Doig, A., Guilliams, T., Latimer, J., McNamee, C., Norris, A., Sanseau, P., Cavalla, D., & Pirmohamed, M. (2019, December 28). Drug repurposing: Progress, challenges and recommendations. Nature Reviews. Drug Discovery, 18(1), 41–58. https://doi.org/10.1038/nrd.2018.168
  • Rainsford, K. D., Parke, A. L., Clifford-Rashotte, M., & Kean, W. F. (2015). Therapy and pharmacological properties of hydroxychloroquine and chloroquine in treatment of systemic lupus erythematosus, rheumatoid arthritis and related diseases. Inflammopharmacology, 23(5), 231–269. October 22). Birkhauser Verlag AG. https://doi.org/10.1007/s10787-015-0239-y
  • Rayne, F., Vendeville, A., Bonhoure, A., & Beaumelle, B. (2004). The ability of chloroquine to prevent tat-induced cytokine secretion by monocytes is implicated in its in vivo anti-human immunodeficiency virus type 1 activity. Journal of Virology, 78(21), 12054–12057.https://doi.org/10.1128/jvi.78.21.12054-12057.2004
  • Romanelli, F., Smith, K., & Hoven, A. (2004). Chloroquine and hydroxychloroquine as inhibitors of human immunodeficiency virus (HIV-1) activity. Current Pharmaceutical Design, 10(21), 2643–2648. https://doi.org/10.2174/1381612043383791
  • Savarino, A., Di Trani, L., Donatelli, I., Cauda, R., & Cassone, A. (2006). New insights into the antiviral effects of chloroquine. The Lancet Infectious Diseases, 6(2), 67–69. https://doi.org/10.1016/S1473-3099(06)70361-9
  • Sperber, K., Louie, M., Kraus, T., Proner, J., Sapira, E., Lin, S., Stecher, V., & Mayer, L. (1995). Hydroxychloroquine treatment of patients with human immunodeficiency virus type 1. Clinical Therapeutics, 17(4), 622–636. https://doi.org/10.1016/0149-2918(95)80039-5
  • van Aalten, D. M., Bywater, R., Findlay, J. B., Hendlich, M., Hooft, R. W., & Vriend, G. (1996). PRODRG, a program for generating molecular topologies and unique molecular descriptors from coordinates of small molecules. Journal of Computer-Aided Molecular Design, 10(3), 255–262. https://doi.org/10.1007/BF00355047
  • Vincent, M. J., Bergeron, E., Benjannet, S., Erickson, B. R., Rollin, P. E., Ksiazek, T. G., Seidah, N. G., & Nichol, S. T. (2005). Chloroquine is a potent inhibitor of SARS coronavirus infection and spread. Virology Journal, 2(1), 69 https://doi.org/10.1186/1743-422X-2-69
  • Wang, M., Cao, R., Zhang, L., Yang, X., Liu, J., Xu, M., Shi, Z., Hu, Z., Zhong, W., & Xiao, G. (2020). Remdesivir and chloroquine effectively inhibit the recently emerged novel coronavirus (2019-nCoV) in vitro. Cell Research, 30(3), 269–271. https://doi.org/10.1038/s41422-020-0282-0
  • Wang, L.-F., Lin, Y.-S., Huang, N.-C., Yu, C.-Y., Tsai, W.-L., Chen, J.-J., Kubota, T., Matsuoka, M., Chen, S.-R., Yang, C.-S., Lu, R.-W., Lin, Y.-L., & Chang, T.-H. (2015). Hydroxychloroquine-inhibited dengue virus is associated with host defense machinery. Journal of Interferon & Cytokine Research, 35(3), 143–156. https://doi.org/10.1089/jir.2014.0038
  • Yao, X., Ye, F., Zhang, M., Cui, C., Huang, B., Niu, P., Liu, X., Zhao, L., Dong, E., Song, C., Zhan, S., Lu, R., Li, H., Tan, W., & Liu, D. (2020). In Vitro Antiviral Activity and Projection of Optimized Dosing Design of Hydroxychloroquine for the Treatment of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2). Clinical Infectious Diseases : An Official Publication of the Infectious Diseases Society of America, 71(15), 732–739. https://doi.org/10.1093/cid/ciaa237

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