197
Views
3
CrossRef citations to date
0
Altmetric
Research Articles

Functional binding dynamics relevant to the evolution of zoonotic spillovers in endemic and emergent Betacoronavirus strains

, , , & ORCID Icon
Pages 10978-10996 | Received 20 Apr 2021, Accepted 04 Jul 2021, Published online: 21 Jul 2021

References

  • Ahamad, S., Kanipakam, H., & Gupta, D. (2020). Insights into the structural and dynamical changes of spike glycoprotein mutations associated with SARS-CoV-2 host receptor binding. Journal of Biomolecular Structure and Dynamics, 1–13.
  • Ali, A., & Vijayan, R. (2020). Dynamics of the ACE2-SARS-CoV-2/SARS-CoV spike protein interface reveal unique mechanisms. Scientific Reports, 10(1), 14214. https://doi.org/10.1038/s41598-020-71188-3
  • Ali, F., Kasry, A., & Amin, M. (2021). The new SARS-CoV-2 strain shows a stronger binding affinity to ACE2 due to N501Y mutant. Medicine in Drug Discovery, 10, 100086. https://doi.org/10.1016/j.medidd.2021.100086
  • Al-Khafaji, K., Al-Duhaidahawi, D., & Tok, T. T. (2020). Using integrated computational approaches to identify safe and rapid treatment for SARS-CoV-2. Journal of Biomolecular Structure and Dynamics, 39(9), 1–9.
  • Allen, J. D., Watanabe, Y., Chawla, H., Newby, M. L., & Crispin, M. (2021). Subtle influence of ACE2 glycan processing on SARS-CoV-2 recognition. Journal of Molecular Biology, 433(4), 166762. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7744274/
  • Andersen, H. C. (1980). Molecular dynamics simulations at constant pressure and/or temperature. Journal of Chemical Physics, 72(4), 2384–2393. https://doi.org/10.1063/1.439486
  • Babbitt, G. A., Fokoue, E. P., Evans, J. R., Diller, K. I., & Adams, L. E. (2020). DROIDS 3.0-detecting genetic and drug class variant impact on conserved protein binding dynamics. Biophysical Journal, 118(3), 541–551. https://doi.org/10.1016/j.bpj.2019.12.008
  • Babbitt, G. A., Lynch, M. L., McCoy, M., Fokoue, E. P., & Hudson, A. O. (2020). Function and evolution of B-Raf loop dynamics relevant to cancer recurrence under drug inhibition. Journal of Biomolecular Structure and Dynamics, 1–16.
  • Babbitt, G. A., Mortensen, J. S., Coppola, E. E., Adams, L. E., & Liao, J. K. (2018). DROIDS 1.20: A GUI-based pipeline for GPU-accelerated comparative protein dynamics. Biophysical Journal, 114(5), 1009–1017. https://doi.org/10.1016/j.bpj.2018.01.020
  • Barros, E. P., Casalino, L., Gaieb, Z., Dommer, A. C., Wang, Y., Fallon, L., Raguette, L., Belfon, K., Simmerling, C., & Amaro, R. E. (2021). The flexibility of ACE2 in the context of SARS-CoV-2 infection. Biophysical Journal, 120(6), 1072–1084. https://doi.org/10.1016/j.bpj.2020.10.036
  • Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological), 57(1), 289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
  • Breiman, L. (2001). Random forests. Machine Learning, 45(1), 5–32. https://doi.org/10.1023/A:1010933404324
  • Cantuti-Castelvetri, L., Ojha, R., Pedro, L. D., Djannatian, M., Franz, J., Kuivanen, S., van der Meer, F., Kallio, K., Kaya, T., Anastasina, M., Smura, T., Levanov, L., Szirovicza, L., Tobi, A., Kallio-Kokko, H., Österlund, P., Joensuu, M., Meunier, F. A., Butcher, S. J., … Simons, M. (2020). Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity. Science (New York, N.Y.), 370(6518), 856–860. https://doi.org/10.1126/science.abd2985
  • Case, D. A., Cheatham, T. E., Darden, T., Gohlke, H., Luo, R., Merz, K. M., Onufriev, A., Simmerling, C., Wang, B., & Woods, R. J. (2005). The Amber biomolecular simulation programs. Journal of Computational Chemistry, 26(16), 1668–1688. https://doi.org/10.1002/jcc.20290
  • Cohen-Khait, R., Dym, O., Hamer-Rogotner, S., & Schreiber, G. (2017). Promiscuous protein binding as a function of protein stability. Structure, 25(12), 1867–1874.e3. https://doi.org/10.1016/j.str.2017.11.002
  • Corbett, K. S., Edwards, D. K., Leist, S. R., Abiona, O. M., Boyoglu-Barnum, S., Gillespie, R. A., Himansu, S., Schäfer, A., Ziwawo, C. T., DiPiazza, A. T., Dinnon, K. H., Elbashir, S. M., Shaw, C. A., Woods, A., Fritch, E. J., Martinez, D. R., Bock, K. W., Minai, M., Nagata, B. M., … Graham, B. S. (2020). SARS-CoV-2 mRNA vaccine design enabled by prototype pathogen preparedness. Nature, 586(7830), 567–571. https://doi.org/10.1038/s41586-020-2622-0
  • Culp, M., Johnson, K., & Michailidis, G. (2016). ada: An R package for stochastic boosting.
  • Daly, J. L., Simonetti, B., Klein, K., Chen, K.-E., Williamson, M. K., Antón-Plágaro, C., Shoemark, D. K., Simón-Gracia, L., Bauer, M., Hollandi, R., Greber, U. F., Horvath, P., Sessions, R. B., Helenius, A., Hiscox, J. A., Teesalu, T., Matthews, D. A., Davidson, A. D., Collins, B. M., Cullen, P. J., & Yamauchi, Y. (2020). Neuropilin-1 is a host factor for SARS-CoV-2 infection. Science (New York, N.Y.), 370(6518), 861–865. https://doi.org/10.1126/science.abd3072
  • Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N⋅log(N) method for Ewald sums in large systems. Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
  • Ewald, P. P. (1921). Die Berechnung optischer und elektrostatischer Gitterpotentiale. Annalen Der Physik, 369(3), 253–287. https://doi.org/10.1002/andp.19213690304
  • Faria, N. R., Morales Claro, I., Candido, D., Moyses Franco, L. A., Andrade, P. S., Coletti, T. M., Silva, C. A., Sales, F. C., Manuli, E. R., & Aguiar, R. S. (2021). Genomic characterisation of an emergent SARS-CoV-2 lineage in Manaus: Preliminary findings. Virological [Internet]. https://virological.org/t/genomic-characterisation-of-an-emergent-sars-cov-2-lineage-in-manaus-preliminary-findings/586
  • Fiser, A., Do, R. K., & Sali, A. (2000). Modeling of loops in protein structures. Protein Science, 9(9), 1753–1773. https://doi.org/10.1110/ps.9.9.1753
  • Follis, K. E., York, J., & Nunberg, J. H. (2006). Furin cleavage of the SARS coronavirus spike glycoprotein enhances cell-cell fusion but does not affect virion entry. Virology, 350(2), 358–369. https://doi.org/10.1016/j.virol.2006.02.003
  • Fung, T. S., & Liu, D. X. (2019). Human coronavirus: Host-pathogen interaction. Annual Review of Microbiology, 73, 529–557. https://doi.org/10.1146/annurev-micro-020518-115759
  • Götz, A. W., Williamson, M. J., Xu, D., Poole, D., Le Grand, S., & Walker, R. C. (2012). Routine microsecond molecular dynamics simulations with AMBER on GPUs. 1. Generalized Born. Journal of Chemical Theory and Computation, 8(5), 1542–1555. https://doi.org/10.1021/ct200909j
  • Haan, C. d., Vennema, H., & Rottier, P. J. M. (2000). Assembly of the Coronavirus envelope: Homotypic interactions between the M proteins. Journal of Virology, 74(11), 4967–4978. https://doi.org/10.1128/.74.11.4967-4978.2000
  • Härdle, W., & Simar, L. (Eds.). (2007). Canonical correlation analysis. In Applied multivariate statistical analysis (pp. 321–330). Berlin, Heidelberg: Springer. https://doi.org/10.1007/978-3-540-72244-1_14
  • Hofmann, H., Pyrc, K., van der Hoek, L., Geier, M., Berkhout, B., & Pöhlmann, S. (2005). Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry. Proceedings of the National Academy of Sciences of the United States of America, 102(22), 7988–7993. https://doi.org/10.1073/pnas.0409465102
  • Hoffmann, M., Hofmann-Winkler, H., & Pöhlmann, S. (2018). Priming time: How cellular proteases arm coronavirus spike proteins. In E. Böttcher-Friebertshäuser, W. Garten, & H. Klenk (Eds.), Activation of Viruses by Host Proteases (pp. 71–98). Springer.
  • Hoffmann, M., Kleine-Weber, H., & Pöhlmann, S. (2020). A multibasic cleavage site in the spike protein of SARS-CoV-2 is essential for infection of human lung cells. Molecular Cell, 78(4), 779–784.e5. https://doi.org/10.1016/j.molcel.2020.04.022
  • Karatzoglou, A., Smola, A., Hornik, K., & Zeileis, A. (2004). kernlab - An S4 package for Kernel methods in R. Journal of Statistical Software, 11, 1–20.
  • Kuba, K., Imai, Y., Rao, S., Gao, H., Guo, F., Guan, B., Huan, Y., Yang, P., Zhang, Y., Deng, W., Bao, L., Zhang, B., Liu, G., Wang, Z., Chappell, M., Liu, Y., Zheng, D., Leibbrandt, A., Wada, T., … Penninger, J. M. (2005). A crucial role of angiotensin converting enzyme 2 (ACE2) in SARS coronavirus-induced lung injury. Nature Medicine, 11(8), 875–879. https://doi.org/10.1038/nm1267
  • Kullback, S., & Leibler, R. A. (1951). On Information and Sufficiency. The Annals of Mathematical Statistics, 22(1), 79–86. https://doi.org/10.1214/aoms/1177729694
  • Li, F., Li, W., Farzan, M., & Harrison, S. C. (2005). Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science (New York, N.Y.), 309(5742), 1864–1868. https://doi.org/10.1126/science.1116480
  • Liang, D., Song, M., Niu, Z., Zhang, P., Rafailovich, M., & Deng, Y. (2021). Supervised machine learning approach to molecular dynamics forecast of SARS-CoV-2 spike glycoproteins at varying temperatures. MRS Advances [Internet]. https://doi.org/10.1557/s43580-021-00021-4
  • Liaw, A., & Wiener, M. (2002). Classification and regression by randomForest. R News, 18–22.
  • Li, W., Zhang, C., Sui, J., Kuhn, J. H., Moore, M. J., Luo, S., Wong, S.-K., Huang, I.-C., Xu, K., Vasilieva, N., Murakami, A., He, Y., Marasco, W. A., Guan, Y., Choe, H., & Farzan, M. (2005). Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. The EMBO Journal, 24(8), 1634–1643. https://doi.org/10.1038/sj.emboj.7600640
  • Lubin, J. H., Zardecki, C., Dolan, E. M., Lu, C., Shen, Z., Dutta, S., Westbrook, J. D., Hudson, B. P., Goodsell, D. S., & Williams, J. K. (2020). Evolution of the SARS-CoV-2 proteome in three dimensions (3D) during the first six months of the COVID-19 pandemic. BioRxiv: The Preprint Server for Biology.
  • 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
  • Mao, Y., & Zhang, Y. (2012). Thermal conductivity, shear viscosity and specific heat of rigid water models. Chemical Physics Letters, 542, 37–41. https://doi.org/10.1016/j.cplett.2012.05.044
  • Melero, R., Sorzano, C. O. S., Foster, B., Vilas, J.-L., Martínez, M., Marabini, R., Ramírez-Aportela, E., Sanchez-Garcia, R., Herreros, D., & Del Caño, L. (2020). Continuous flexibility analysis of SARS-CoV-2 spike prefusion structures. IUCrJ, 7(6),‌ 1059–1069.
  • Mittal, A., Manjunath, K., Ranjan, R. K., Kaushik, S., Kumar, S., & Verma, V. (2020). COVID-19 pandemic: Insights into structure, function, and hACE2 receptor recognition by SARS-CoV-2. PLoS Pathogens [Internet], 16. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7444525/
  • Muralidharan, N., Sakthivel, R., Velmurugan, D., & Gromiha, M. M. (2020). Computational studies of drug repurposing and synergism of lopinavir, oseltamivir and ritonavir binding with SARS-CoV-2 protease against COVID-19. Journal of Biomolecular Structure and Dynamics, 39(7), 2573–2678.
  • Ou, X., Guan, H., Qin, B., Mu, Z., Wojdyla, J. A., Wang, M., Dominguez, S. R., Qian, Z., & Cui, S. (2017). Crystal structure of the receptor binding domain of the spike glycoprotein of human betacoronavirus HKU1. Nature Communications, 8, 15216. https://doi.org/10.1038/ncomms15216
  • Ou, X., Liu, Y., Lei, X., Li, P., Mi, D., Ren, L., Guo, L., Guo, R., Chen, T., Hu, J., Xiang, Z., Mu, Z., Chen, X., Chen, J., Hu, K., Jin, Q., Wang, J., & Qian, Z. (2020). Characterization of spike glycoprotein of SARS-CoV-2 on virus entry and its immune cross-reactivity with SARS-CoV. Nature Communications, 11(1), 1620. https://doi.org/10.1038/s41467-020-15562-9
  • Oudit, G. Y., Crackower, M. A., Backx, P. H., & Penninger, J. M. (2003). The role of ACE2 in cardiovascular physiology. Trends in Cardiovascular Medicine, 13(3), 93–101. https://doi.org/10.1016/s1050-1738(02)00233-5
  • Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera-a visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
  • Pierce, L. C. T., Salomon-Ferrer, R., de Oliveira, C. A. F., McCammon, J. A., & Walker, R. C. (2012). Routine access to millisecond time scale events with accelerated molecular dynamics. Journal of Chemical Theory and Computation, 8(9), 2997–3002. https://doi.org/10.1021/ct300284c
  • Pierri, C. L. (2020). SARS-CoV-2 spike protein: Flexibility as a new target for fighting infection. Signal Transduction and Targeted Therapy, 5, 1–3.
  • Planas, D., Bruel, T., Grzelak, L., Guivel-Benhassine, F., Staropoli, I., Porrot, F., Planchais, C., Buchrieser, J., Rajah, M. M., & Bishop, E. (2021). Sensitivity of infectious SARS-CoV-2 B.1.1.7 and B.1.351 variants to neutralizing antibodies. Nature Medicine, 27, 917–924.
  • Rambaut, A., Loman, N., Pybus, O., Barclay, W., Barrett, J., Carabelli, A., Connor, T., Peacock, T., Robertson, D. L., & Volz, E. (2020). Preliminary genomic characterisation of an emergent SARS-CoV-2 lineage in the UK defined by a novel set of spike mutations. Virological [Internet]. https://virological.org/t/preliminary-genomic-characterisation-of-an-emergent-sars-cov-2-lineage-in-the-uk-defined-by-a-novel-set-of-spike-mutations/563
  • Randhawa, G. S., Soltysiak, M. P. M., Roz, H. E., Souza, C. P. E., de Hill, K. A., & Kari, L. (2020). Machine learning using intrinsic genomic signatures for rapid classification of novel pathogens: COVID-19 case study. PLOS ONE, 16(1), e0246465.
  • Roe, D. R., & Cheatham, T. E. (2013). PTRAJ and CPPTRAJ: Software for processing and analysis of molecular dynamics trajectory data. Journal of Chemical Theory and Computation, 9(7), 3084–3095. https://doi.org/10.1021/ct400341p
  • Sali, A., & Blundell, T. L. (1993). Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology, 234(3), 779–815. https://doi.org/10.1006/jmbi.1993.1626
  • Salomon-Ferrer, R., Götz, A. W., Poole, D., Le Grand, S., & Walker, R. C. (2013). Routine microsecond molecular dynamics simulations with AMBER on GPUs. 2. Explicit solvent particle mesh Ewald. Journal of Chemical Theory and Computation, 9(9), 3878–3888. https://doi.org/10.1021/ct400314y
  • Sanda, M., Morrison, L., & Goldman, R. (2021). N- and O-glycosylation of the SARS-CoV-2 spike protein. Analytical Chemistry, 93(4), 2003–2009. https://doi.org/10.1021/acs.analchem.0c03173
  • Shang, J., Wan, Y., Luo, C., Ye, G., Geng, Q., Auerbach, A., & Li, F. (2020). Cell entry mechanisms of SARS-CoV-2. Proceedings of the National Academy of Sciences of the United States of America, 117(21), 11727–11734. https://doi.org/10.1073/pnas.2003138117
  • Song, W., Gui, M., Wang, X., & Xiang, Y. (2018). Cryo-EM structure of the SARS coronavirus spike glycoprotein in complex with its host cell receptor ACE2. PLoS Pathogens, 14(8), e1007236. https://doi.org/10.1371/journal.ppat.1007236
  • Tegally, H., Wilkinson, E., Giovanetti, M., Iranzadeh, A., Fonseca, V., Giandhari, J., Doolabh, D., Pillay, S., San, E. J., Msomi, N., Mlisana, K., von Gottberg, A., Walaza, S., Allam, M., Ismail, A., Mohale, T., Glass, A. J., Engelbrecht, S., Van Zyl, G., … de Oliveira, T. (2021). Detection of a SARS-CoV-2 variant of concern in South Africa. Nature, 592(7854), 438–443. https://doi.org/10.1038/s41586-021-03402-9
  • 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. (2019). Structural basis for human coronavirus attachment to sialic acid receptors. Nature Structural & Molecular Biology, 26(6), 481–489. https://doi.org/10.1038/s41594-019-0233-y
  • Venables, W. N., & Ripley, B. D. (2010). Modern applied statistics with S. Springer Publishing Company, Incorporated.
  • Wang, Q., Qi, J., Yuan, Y., Xuan, Y., Han, P., Wan, Y., Ji, W., Li, Y., Wu, Y., Wang, J., Iwamoto, A., Woo, P. C. Y., Yuen, K.-Y., Yan, J., Lu, G., & Gao, G. F. (2014). Bat origins of MERS-CoV supported by bat coronavirus HKU4 usage of human receptor CD26. Cell Host & Microbe, 16(3), 328–337. https://doi.org/10.1016/j.chom.2014.08.009
  • Wang, Y., Liu, M., & Gao, J. (2020). Enhanced receptor binding of SARS-CoV-2 through networks of hydrogen-bonding and hydrophobic interactions. Proceedings of the National Academy of Sciences of the United States of America, 117(25), 13967–13974. https://doi.org/10.1073/pnas.2008209117
  • Yan, R., Zhang, Y., Li, Y., Xia, L., Guo, Y., & Zhou, Q. (2020). Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2. Science (New York, N.Y.), 367(6485), 1444–1448. https://doi.org/10.1126/science.abb2762
  • Yang, Q., Hughes, T. A., Kelkar, A., Yu, X., Cheng, K., Park, S., Huang, W.-C., Lovell, J. F., & Neelamegham, S. (2020). Inhibition of SARS-CoV-2 viral entry upon blocking N- and O-glycan elaboration. McConville MJ, Kana BD, McConville MJ, Thaysen-Andersen M, editors. eLife, 9:e61552.
  • Yu, J., Qiao, S., Guo, R., & Wang, X. (2020). Cryo-EM structures of HKU2 and SADS-CoV spike glycoproteins provide insights into coronavirus evolution. Nature Communications, 11(1), 3070. https://doi.org/10.1038/s41467-020-16876-4
  • Yuan, Y., Cao, D., Zhang, Y., Ma, J., Qi, J., Wang, Q., Lu, G., Wu, Y., Yan, J., Shi, Y., Zhang, X., & Gao, G. F. (2017). Cryo-EM structures of MERS-CoV and SARS-CoV spike glycoproteins reveal the dynamic receptor binding domains. Nature Communications, 8, 15092. https://doi.org/10.1038/ncomms15092
  • Zhang, Y., Zhao, W., Mao, Y., Chen, Y., Wang, S., Zhong, Y., Su, T., Gong, M., Du, D., Lu, X., Cheng, J., & Yang, H. (2021). Site-specific N-glycosylation characterization of recombinant SARS-CoV-2 spike proteins. Molecular & Cellular Proteomics, 20, 100058. https://doi.org/10.1074/mcp.RA120.002295
  • Zhao, X., Chen, D., Szabla, R., Zheng, M., Li, G., Du, P., Zheng, S., Li, X., Song, C., & Li, R. (2020). Broad and differential animal angiotensin-converting enzyme 2 receptor usage by SARS-CoV-2. Journal of Virology, 94(18), e00940-20. https://jvi.asm.org/content/94/18/e00940-20

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.