1,938
Views
13
CrossRef citations to date
0
Altmetric
Research Articles

Impact of dimerization and N3 binding on molecular dynamics of SARS-CoV and SARS-CoV-2 main proteases

ORCID Icon &
Pages 6243-6254 | Received 08 Oct 2020, Accepted 19 Jan 2021, Published online: 02 Feb 2021

References

  • Adcock, S. A., & McCammon, J. A. (2006). Molecular dynamics: Survey of methods for simulating the activity of proteins. Chemical Reviews, 106(5), 1589–1615. https://doi.org/10.1021/cr040426m
  • Alamri, M. A., Tahir Ul Qamar, M., Mirza, M. U., Bhadane, R., Alqahtani, S. M., Muneer, I., Froeyen, M., & Salo-Ahen, O. M. H. (2020). Pharmacoinformatics and molecular dynamics simulation studies reveal potential covalent and FDA-approved inhibitors of SARS-CoV-2 main protease 3CL(pro). Journal of Biomolecular Structure and Dynamics. https://doi.org/10.1080/07391102.2020.1782768
  • Alazmi, M., & Motwalli, O. (2020). In silico virtual screening, characterization, docking and molecular dynamics studies of crucial SARS-CoV-2 proteins. Journal of Biomolecular Structure and Dynamics. https://doi.org/10.1080/07391102.2020.1803965
  • Bacha, U., Barrila, J., Velazquez-Campoy, A., Leavitt, S. A., & Freire, E. (2004). Identification of novel inhibitors of the SARS coronavirus main protease 3CLpro. Biochemistry, 43(17), 4906–4912. https://doi.org/10.1021/bi0361766
  • Barrila, J., Bacha, U., & Freire, E. (2006). Long-range cooperative interactions modulate dimerization in SARS 3CLpro. Biochemistry, 45(50), 14908–14916. https://doi.org/10.1021/bi0616302
  • Botello-Smith, W. M., & Luo, Y. (2019). Robust determination of protein allosteric signaling pathways. Journal of Chemical Theory and Computation, 15(4), 2116–2126. https://doi.org/10.1021/acs.jctc.8b01197
  • Chen, H., Wei, P., Huang, C., Tan, L., Liu, Y., & Lai, L. (2006). Only one protomer is active in the dimer of SARS 3C-like proteinase. The Journal of Biological Chemistry, 281(20), 13894–13898. https://doi.org/10.1074/jbc.M510745200
  • Chen, S., Chen, L., Tan, J., Chen, J., Du, L., Sun, T., Shen, J., Chen, K., Jiang, H., & Shen, X. (2005). Severe acute respiratory syndrome coronavirus 3C-like proteinase N terminus is indispensable for proteolytic activity but not for enzyme dimerization. Biochemical and thermodynamic investigation in conjunction with molecular dynamics simulations. The Journal of Biological Chemistry, 280(1), 164–173. https://doi.org/10.1074/jbc.M408211200
  • Chen, S., Hu, T., Zhang, J., Chen, J., Chen, K., Ding, J., Jiang, H., & Shen, X. (2008). Mutation of Gly-11 on the dimer interface results in the complete crystallographic dimer dissociation of severe acute respiratory syndrome coronavirus 3C-like protease: Crystal structure with molecular dynamics simulations. The Journal of Biological Chemistry, 283(1), 554–564. https://doi.org/10.1074/jbc.M705240200
  • Cui, W., Cui, S., Chen, C., Chen, X., Wang, Z., Yang, H., & Zhang, L. (2019). The crystal structure of main protease from mouse hepatitis virus A59 in complex with an inhibitor. Biochemical and Biophysical Research Communications, 511(4), 794–799. https://doi.org/10.1016/j.bbrc.2019.02.105
  • Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald - an N.Log(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
  • Di Paola, L., De Ruvo, M., Paci, P., Santoni, D., & Giuliani, A. (2013). Protein contact networks: An emerging paradigm in chemistry. Chemical Reviews, 113(3), 1598–1613. https://doi.org/10.1021/cr3002356
  • Dubanevics, I., & McLeish, T. C. B. (2021). Computational analysis of dynamic allostery and control in the SARS-CoV-2 main protease. Journal of the Royal Society Interface, 18, 20200591. http://doi.org/10.1098/rsif.2020.0591
  • Elbe, S., & Buckland-Merrett, G. (2017). Data, disease and diplomacy: GISAID's innovative contribution to global health. Global Challengers, 1(1), 33–46. https://doi.org/10.1002/gch2.1018
  • Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., & Pedersen, L. G. (1995). A smooth particle mesh Ewald method. The Journal of Chemical Physics, 103(19), 8577–8593. https://doi.org/10.1063/1.470117
  • Ghosh, R., Chakraborty, A., Biswas, A., & Chowdhuri, S. (2020). Identification of polyphenols from Broussonetia papyrifera as SARS CoV-2 main protease inhibitors using in silico docking and molecular dynamics simulation approaches. Journal of Biomolecular Structure and Dynamics. https://doi.org/10.1080/07391102.2020.1802347
  • Goyal, B., & Goyal, D. (2020). Targeting the dimerization of the main protease of coronaviruses: A potential broad-spectrum therapeutic strategy. ACS Combinatorial Science, 22(6), 297–305. https://doi.org/10.1021/acscombsci.0c00058
  • Gunasekaran, K., Ma, B., & Nussinov, R. (2004). Is allostery an intrinsic property of all dynamic proteins? Proteins, 57(3), 433–443. https://doi.org/10.1002/prot.20232
  • Hess, B. (2008). P-LINCS: A parallel linear constraint solver for molecular simulation. Journal of Chemical Theory and Computation, 4(1), 116–122. https://doi.org/10.1021/ct700200b
  • 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
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33. https://doi.org/10.1016/0263-7855(96)00018-5
  • Jakalian, A., Jack, D. B., & Bayly, C. I. (2002). Fast, efficient generation of high-quality atomic charges. AM1-BCC model: II. Parameterization and validation. Journal of Computational Chemistry, 23(16), 1623–1641. https://doi.org/10.1002/jcc.10128
  • Jin, Z., Du, X., Xu, Y., Deng, Y., Liu, M., Zhao, Y., Zhang, B., Li, X., Zhang, L., Peng, C., Duan, Y., Yu, J., Wang, L., Yang, K., Liu, F., Jiang, R., Yang, X., You, T., Liu, X., … Yang, H. (2020). Structure of M(pro) from COVID-19 virus and discovery of its inhibitors. Nature, 582(7811), 289–293. https://doi.org/10.1038/s41586-020-2223-y
  • Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics, 79(2), 926–935. https://doi.org/10.1063/1.445869
  • Karplus, M., & McCammon, J. A. (2002). Molecular dynamics simulations of biomolecules. Nature Structural Biology, 9(9), 646–652. https://doi.org/10.1038/nsb0902-646
  • Khan, M. T., Ali, A., Wang, Q., Irfan, M., Khan, A., Zeb, M. T., Zhang, Y. J., Chinnasamy, S., & Wei, D. Q. (2020). Marine natural compounds as potents inhibitors against the main protease of SARS-CoV-2-a molecular dynamic study. Journal of Biomolecular Structure and Dynamics. https://doi.org/10.1080/07391102.2020.1769733
  • Kumar, S., Sharma, P. P., Shankar, U., Kumar, D., Joshi, S. K., Pena, L., Durvasula, R., Kumar, A., Kempaiah, P., & Al, P. (2020). Discovery of new hydroxyethylamine analogs against 3CL(pro) protein target of SARS-CoV-2: Molecular docking, molecular dynamics simulation, and structure-activity relationship studies. Journal of Chemical Information and Modeling, 60(12), 5754-5770. https://doi.org/10.1021/acs.jcim.0c00326
  • Kurt Yilmaz, N., Swanstrom, R., & Schiffer, C. A. (2016). Improving viral protease inhibitors to counter drug resistance. Trends in Microbiology, 24(7), 547–557. https://doi.org/10.1016/j.tim.2016.03.010
  • Lange, O. F., & Grubmuller, H. (2006). Generalized correlation for biomolecular dynamics. Proteins, 62(4), 1053–1061. https://doi.org/10.1002/prot.20784
  • Lee, A. L. (2015). Contrasting roles of dynamics in protein allostery: NMR and structural studies of CheY and the third PDZ domain from PSD-95. Biophysical Reviews, 7(2), 217–226. https://doi.org/10.1007/s12551-015-0169-3
  • Li, C., Teng, X., Qi, Y., Tang, B., Shi, H., Ma, X., & Lai, L. (2016). Conformational flexibility of a short loop near the active site of the SARS-3CLpro is essential to maintain catalytic activity. Scientific Reports, 6, 20918. https://doi.org/10.1038/srep20918
  • Li, J., Shen, W., Liao, M., & Bartlam, M. (2007). Preliminary crystallographic analysis of avian infectious bronchitis virus main protease. Acta Crystallographica. Section F, Structural Biology and Crystallization Communications, 63(Pt 1), 24–26. https://doi.org/10.1107/S1744309106052341
  • Liang, J., Pitsillou, E., Karagiannis, C., Darmawan, K. K., Ng, K., Hung, A., & Karagiannis, T. C. (2020). Interaction of the prototypical α-ketoamide inhibitor with the SARS-CoV-2 main protease active site in silico: Molecular dynamic simulations highlight the stability of the ligand-protein complex. Computational Biology and Chemistry, 87, 107292. https://doi.org/10.1016/j.compbiolchem.2020.107292
  • Lim, L., Gupta, G., Roy, A., Kang, J., Srivastava, S., Shi, J., & Song, J. (2019). Structurally- and dynamically-driven allostery of the chymotrypsin-like proteases of SARS, Dengue and Zika viruses. Progress in Biophysics and Molecular Biology, 143, 52–66. https://doi.org/10.1016/j.pbiomolbio.2018.08.009
  • Lim, L., Shi, J., Mu, Y., & Song, J. (2014). Dynamically-driven enhancement of the catalytic machinery of the SARS 3C-like protease by the S284-T285-I286/A mutations on the extra domain. PLoS One, 9(7), e101941. https://doi.org/10.1371/journal.pone.0101941
  • Lindorff-Larsen, K., Piana, S., Palmo, K., Maragakis, P., Klepeis, J. L., Dror, R. O., & Shaw, D. E. (2010). Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins, 78(8), 1950–1958. https://doi.org/10.1002/prot.22711
  • Miyamoto, S., & Kollman, P. A. (1992). Settle - An analytical version of the SHAKE and RATTLE algorithm for rigid water models. Journal of Computational Chemistry, 13(8), 952–962. https://doi.org/10.1002/jcc.540130805
  • Negre, C. F. A., Morzan, U. N., Hendrickson, H. P., Pal, R., Lisi, G. P., Loria, J. P., Rivalta, I., Ho, J., & Batista, V. S. (2018). Eigenvector centrality for characterization of protein allosteric pathways. Proceedings of the National Academy of Sciences of the United States of America, 115(52), E12201–E12208. https://doi.org/10.1073/pnas.1810452115
  • Pall, S., Abraham, M. J., Kutzner, C., Hess, B., & Lindahl, E. (2015). Tackling Exascale software challenges in molecular dynamics simulations with GROMACS. Lecture Notes in Computer Science, 8759, 3.
  • Pang, Y. P. (2004). Three-dimensional model of a substrate-bound SARS chymotrypsin-like cysteine proteinase predicted by multiple molecular dynamics simulations: Catalytic efficiency regulated by substrate binding. Proteins, 57(4), 747–757. https://doi.org/10.1002/prot.20249
  • Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single-crystals - A new molecular-dynamics method. Journal of Applied Physics, 52(12), 7182–7190. https://doi.org/10.1063/1.328693
  • Penkler, D. L., Atilgan, C., & Tastan Bishop, O. (2018). Allosteric modulation of human Hsp90α conformational dynamics. Journal of Chemical Information and Modeling, 58(2), 383–404. https://doi.org/10.1021/acs.jcim.7b00630
  • Pronk, S., Páll, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., Shirts, M. R., Smith, J. C., Kasson, P. M., van der Spoel, D., Hess, B., & Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics (Oxford, England), 29(7), 845–854. https://doi.org/10.1093/bioinformatics/btt055
  • Saint-Martin, H., Hess, B., & Berendsen, H. J. (2004). An application of flexible constraints in Monte Carlo simulations of the isobaric–isothermal ensemble of liquid water and ice Ih with the polarizable and flexible mobile charge densities in harmonic oscillators model. The Journal of Chemical Physics, 120(23), 11133–11143. https://doi.org/10.1063/1.1747927
  • Sethi, A., Eargle, J., Black, A. A., & Luthey-Schulten, Z. (2009). Dynamical networks in tRNA:protein complexes. Proceedings of the National Academy of Sciences of the United States of America, 106(16), 6620–6625. https://doi.org/10.1073/pnas.0810961106
  • Sheik Amamuddy, O., Veldman, W., Manyumwa, C., Khairallah, A., Agajanian, S., Oluyemi, O., Verkhivker, G., & Tastan Bishop, O. (2020). Integrated computational approaches and tools for allosteric drug discovery. International Journal of Molecular Sciences. 21(3), 847.
  • Sheik Amamuddy, O., Verkhivker, G. M., & Tastan Bishop, O. (2020). Impact of early pandemic stage mutations on molecular dynamics of SARS-CoV-2 M(pro). Journal of Chemical Information and Modeling, 60(10), 5080-5102. https://doi.org/10.1021/acs.jcim.0c00634
  • Shi, J., & Song, J. (2006). The catalysis of the SARS 3C-like protease is under extensive regulation by its extra domain. The FEBS Journal, 273(5), 1035–1045. https://doi.org/10.1111/j.1742-4658.2006.05130.x
  • Shi, J., Han, N., Lim, L., Lua, S., Sivaraman, J., Wang, L., Mu, Y., & Song, J. (2011). Dynamically-driven inactivation of the catalytic machinery of the SARS 3C-like protease by the N214A mutation on the extra domain. PLoS Computational Biology, 7(2), e1001084. https://doi.org/10.1371/journal.pcbi.1001084
  • Shi, J., Sivaraman, J., & Song, J. (2008). Mechanism for controlling the dimer-monomer switch and coupling dimerization to catalysis of the severe acute respiratory syndrome coronavirus 3C-like protease. Journal of Virology, 82(9), 4620–4629. https://doi.org/10.1128/JVI.02680-07
  • Sousa da Silva, A., & Vranken, W. (2012). ACPYPE - AnteChamber PYthon Parser interfacE. BMC Research Notes, 5(1), 367. https://doi.org/10.1186/1756-0500-5-367
  • Suarez, D., & Diaz, N. (2020). SARS-CoV-2 main protease: A molecular dynamics study. Journal of Chemical Information and Modeling, 60(12), 5815-5831. https://doi.org/10.1021/acs.jcim.0c00575
  • Tahir Ul Qamar, M., Alqahtani, S. M., Alamri, M. A., & Chen, L. L. (2020). Structural basis of SARS-CoV-2 3CLpro and anti-COVID-19 drug discovery from medicinal plants. Journal of Pharmaceutical Analysis, 10(4), 313–319. https://doi.org/10.1016/j.jpha.2020.03.009
  • Tan, J., Verschueren, K. H. G., Anand, K., Shen, J., Yang, M., Xu, Y., Rao, Z., Bigalke, J., Heisen, B., Mesters, J. R., Chen, K., Shen, X., Jiang, H., & Hilgenfeld, R. (2005). pH-dependent conformational flexibility of the SARS-CoV main proteinase (M(pro)) dimer: Molecular dynamics simulations and multiple X-ray structure analyses. Journal of Molecular Biology, 354(1), 25–40. https://doi.org/10.1016/j.jmb.2005.09.012
  • Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718. https://doi.org/10.1002/jcc.20291
  • Van Wart, A. T., Durrant, J., Votapka, L., & Amaro, R. E. (2014). Weighted implementation of suboptimal paths (WISP): An optimized algorithm and tool for dynamical network analysis. Journal of Chemical Theory and Computation, 10(2), 511–517. https://doi.org/10.1021/ct4008603
  • Wang, F., Chen, C., Liu, X., Yang, K., Xu, X., & Yang, H. (2016). Crystal structure of feline infectious peritonitis virus main protease in complex with synergetic dual inhibitors. Journal of Virology, 90(4), 1910–1917. https://doi.org/10.1128/JVI.02685-15
  • Wang, F., Chen, C., Yang, K., Xu, Y., Liu, X., Gao, F., Liu, H., Chen, X., Zhao, Q., Liu, X., Cai, Y., & Yang, H. (2017). Michael acceptor-based peptidomimetic inhibitor of main protease from porcine epidemic diarrhea virus. Journal of Medicinal Chemistry, 60(7), 3212–3216. https://doi.org/10.1021/acs.jmedchem.7b00103
  • Wang, J., Wang, W., Kollman, P. A., & Case, D. A. (2006). Automatic atom type and bond type perception in molecular mechanical calculations. Journal of Molecular Graphics & Modelling, 25(2), 247–260. https://doi.org/10.1016/j.jmgm.2005.12.005
  • 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
  • Wei, P., Fan, K., Chen, H., Ma, L., Huang, C., Tan, L., Xi, D., Li, C., Liu, Y., Cao, A., & Lai, L. (2006). The N-terminal octapeptide acts as a dimerization inhibitor of SARS coronavirus 3C-like proteinase. Biochemical and Biophysical Research Communications, 339(3), 865–872. https://doi.org/10.1016/j.bbrc.2005.11.102
  • Xue, X., Yang, H., Shen, W., Zhao, Q., Li, J., Yang, K., Chen, C., Jin, Y., Bartlam, M., & Rao, Z. (2007). Production of authentic SARS-CoV M(pro) with enhanced activity: Application as a novel tag-cleavage endopeptidase for protein overproduction. Journal of Molecular Biology, 366(3), 965–975. https://doi.org/10.1016/j.jmb.2006.11.073
  • Yuan, Z., Zhao, J., & Wang, Z. X. (2003). Flexibility analysis of enzyme active sites by crystallographic temperature factors. Protein Engineering, 16(2), 109–114. https://doi.org/10.1093/proeng/gzg014
  • Zaki, M. J., & Meira, W. (2014). Data mining and analysis: Fundamental concepts and algorithms. New York: Cambridge University Press.
  • Zhang, L., Lin, D., Sun, X., Curth, U., Drosten, C., Sauerhering, L., Becker, S., Rox, K., & Hilgenfeld, R. (2020). Crystal structure of SARS-CoV-2 main protease provides a basis for design of improved α-ketoamide inhibitors. Science (New York, N.Y.), 368(6489), 409–412. https://doi.org/10.1126/science.abb3405
  • Zheng, K., Ma, G., Zhou, J., Zen, M., Zhao, W., Jiang, Y., Yu, Q., & Feng, J. (2007). Insight into the activity of SARS main protease: Molecular dynamics study of dimeric and monomeric form of enzyme. Proteins, 66(2), 467–479. https://doi.org/10.1002/prot.21160
  • Zhong, N., Zhang, S. N., Zou, P., Chen, J. X., Kang, X., Li, Z., Liang, C., Jin, C. W., & Xia, B. (2008). Without its N-finger, the main protease of severe acute respiratory syndrome coronavirus can form a novel dimer through its C-terminal domain. Journal of Virology, 82(9), 4227–4234. https://doi.org/10.1128/JVI.02612-07
  • Zhu, N., Zhang, D., Wang, W., Li, X., Yang, B., Song, J., Zhao, X., Huang, B., Shi, W., Lu, R., Niu, P., Zhan, F., Ma, X., Wang, D., Xu, W., Wu, G., Gao, G. F., & Tan, W., China Novel Coronavirus Investigating and Research Team (2020). A Novel coronavirus from patients with pneumonia in China, 2019. The New England Journal of Medicine, 382(8), 727–733. https://doi.org/10.1056/NEJMoa2001017

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.