Structural insights into the modulation of coronavirus spike tilting and infectivity by hinge glycans

Chmielewski, David; Wilson, Eric A.; Pintilie, Grigore; Zhao, Peng; Chen, Muyuan; Schmid, Michael F.; Simmons, Graham; Wells, Lance; Jin, Jing; Singharoy, Abhishek; Chiu, Wah

doi:10.1038/s41467-023-42836-9

Structural insights into the modulation of coronavirus spike tilting and infectivity by hinge glycans

Journal Article · Tue Nov 07 00:00:00 EST 2023 · Nature Communications

DOI:https://doi.org/10.1038/s41467-023-42836-9· OSTI ID:2204918

Chmielewski, David; ; Pintilie, Grigore; ; Chen, Muyuan; ; Simmons, Graham; ; ; ;

Abstract

Coronavirus spike glycoproteins presented on the virion surface mediate receptor binding, and membrane fusion during virus entry and constitute the primary target for vaccine and drug development. How the structure dynamics of the full-length spikes incorporated in viral lipid envelope correlates with the virus infectivity remains poorly understood. Here we present structures and distributions of native spike conformations on vitrified human coronavirus NL63 (HCoV-NL63) virions without chemical fixation by cryogenic electron tomography (cryoET) and subtomogram averaging, along with site-specific glycan composition and occupancy determined by mass spectrometry. The higher oligomannose glycan shield on HCoV-NL63 spikes than on SARS-CoV-2 spikes correlates with stronger immune evasion of HCoV-NL63. Incorporation of cryoET-derived native spike conformations into all-atom molecular dynamic simulations elucidate the conformational landscape of the glycosylated, full-length spike that reveals a role of hinge glycans in modulating spike bending. We show that glycosylation at N1242 at the upper portion of the stalk is responsible for the extensive orientational freedom of the spike crown. Subsequent infectivity assays implicated involvement of N1242-glyan in virus entry. Our results suggest a potential therapeutic target site for HCoV-NL63.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); National Science Foundation (NSF); USDOE; USDOE Advanced Research Projects Agency - Energy (ARPA-E)

Grant/Contract Number:: AC02-76SF00515; AC05-00OR22725

OSTI ID:: 2204918

Alternate ID(s):: OSTI ID: 2405206

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 14; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (82)

UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
CHARMM-GUI: A web-based graphical user interface for CHARMM Jo, Sunhwan; Kim, Taehoon; Iyer, Vidyashankara G. Journal of Computational Chemistry, Vol. 29, Issue 11 https://doi.org/10.1002/jcc.20945	journal	March 2008
CHARMM: The biomolecular simulation program Brooks, B. R.; Brooks, C. L.; Mackerell, A. D. Journal of Computational Chemistry, Vol. 30, Issue 10 https://doi.org/10.1002/jcc.21287	journal	July 2009
UCSF ChimeraX: Meeting modern challenges in visualization and analysis: UCSF ChimeraX Visualization System Goddard, Thomas D.; Huang, Conrad C.; Meng, Elaine C. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3235	journal	September 2017
CCBuilder 2.0: Powerful and accessible coiled‐coil modeling Wood, Christopher W.; Woolfson, Derek N. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3279	journal	September 2017
UCSF ChimeraX : Structure visualization for researchers, educators, and developers Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Protein Science, Vol. 30, Issue 1 https://doi.org/10.1002/pro.3943	journal	October 2020
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
Monoclonal antibody therapies against SARS-CoV-2 Focosi, Daniele; McConnell, Scott; Casadevall, Arturo The Lancet Infectious Diseases, Vol. 22, Issue 11 https://doi.org/10.1016/S1473-3099(22)00311-5	journal	November 2022
Exploitation of glycosylation in enveloped virus pathobiology Watanabe, Yasunori; Bowden, Thomas A.; Wilson, Ian A. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1863, Issue 10 https://doi.org/10.1016/j.bbagen.2019.05.012	journal	October 2019
Mechanisms of SecM-Mediated Stalling in the Ribosome Gumbart, James; Schreiner, Eduard; Wilson, Daniel N. Biophysical Journal, Vol. 103, Issue 2 https://doi.org/10.1016/j.bpj.2012.06.005	journal	July 2012
Molecular Architecture of the SARS-CoV-2 Virus Yao, Hangping; Song, Yutong; Chen, Yong Cell, Vol. 183, Issue 3 https://doi.org/10.1016/j.cell.2020.09.018	journal	October 2020
Structure, Function, and Antigenicity of the SARS-CoV-2 Spike Glycoprotein Walls, Alexandra C.; Park, Young-Jun; Tortorici, M. Alejandra Cell, Vol. 183, Issue 6 https://doi.org/10.1016/j.cell.2020.11.032	journal	December 2020
Cryo-ET of Env on intact HIV virions reveals structural variation and positioning on the Gag lattice Mangala Prasad, Vidya; Leaman, Daniel P.; Lovendahl, Klaus N. Cell, Vol. 185, Issue 4 https://doi.org/10.1016/j.cell.2022.01.013	journal	February 2022
Structure, receptor recognition, and antigenicity of the human coronavirus CCoV-HuPn-2018 spike glycoprotein Tortorici, M. Alejandra; Walls, Alexandra C.; Joshi, Anshu Cell, Vol. 185, Issue 13 https://doi.org/10.1016/j.cell.2022.05.019	journal	June 2022
Composition and Antigenic Effects of Individual Glycan Sites of a Trimeric HIV-1 Envelope Glycoprotein Behrens, Anna-Janina; Vasiljevic, Snezana; Pritchard, Laura K. Cell Reports, Vol. 14, Issue 11 https://doi.org/10.1016/j.celrep.2016.02.058	journal	March 2016
Conformational Freedom of the LRP6 Ectodomain Is Regulated by N-glycosylation and the Binding of the Wnt Antagonist Dkk1 Matoba, Kyoko; Mihara, Emiko; Tamura-Kawakami, Keiko Cell Reports, Vol. 18, Issue 1 https://doi.org/10.1016/j.celrep.2016.12.017	journal	January 2017
Stabilized coronavirus spike stem elicits a broadly protective antibody Hsieh, Ching-Lin; Werner, Anne P.; Leist, Sarah R. Cell Reports, Vol. 37, Issue 5 https://doi.org/10.1016/j.celrep.2021.109929	journal	November 2021
Structural basis and mode of action for two broadly neutralizing antibodies against SARS-CoV-2 emerging variants of concern Li, Wenwei; Chen, Yaozong; Prévost, Jérémie Cell Reports, Vol. 38, Issue 2 https://doi.org/10.1016/j.celrep.2021.110210	journal	January 2022
Automated electron microscope tomography using robust prediction of specimen movements Mastronarde, David N. Journal of Structural Biology, Vol. 152, Issue 1 https://doi.org/10.1016/j.jsb.2005.07.007	journal	October 2005
CryoFold: Determining protein structures and data-guided ensembles from cryo-EM density maps Shekhar, Mrinal; Terashi, Genki; Gupta, Chitrak Matter, Vol. 4, Issue 10 https://doi.org/10.1016/j.matt.2021.09.004	journal	October 2021
Structure and immune recognition of the porcine epidemic diarrhea virus spike protein Kirchdoerfer, Robert N.; Bhandari, Mahesh; Martini, Olnita Structure, Vol. 29, Issue 4 https://doi.org/10.1016/j.str.2020.12.003	journal	April 2021
Vaccine-elicited murine antibody WS6 neutralizes diverse beta-coronaviruses by recognizing a helical stem supersite of vulnerability Shi, Wei; Wang, Lingshu; Zhou, Tongqing Structure, Vol. 30, Issue 9 https://doi.org/10.1016/j.str.2022.06.004	journal	September 2022
A 3.4-Å cryo-electron microscopy structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles Zhang, Kaiming; Li, Shanshan; Pintilie, Grigore QRB Discovery, Vol. 1 https://doi.org/10.1017/qrd.2020.16	journal	January 2020
Developing a Fully Glycosylated Full-Length SARS-CoV-2 Spike Protein Model in a Viral Membrane Woo, Hyeonuk; Park, Sang-Jun; Choi, Yeol Kyo The Journal of Physical Chemistry B, Vol. 124, Issue 33 https://doi.org/10.1021/acs.jpcb.0c04553	journal	June 2020
Machine Learning Reveals the Critical Interactions for SARS-CoV-2 Spike Protein Binding to ACE2 Pavlova, Anna; Zhang, Zijian; Acharya, Atanu The Journal of Physical Chemistry Letters, Vol. 12, Issue 23 https://doi.org/10.1021/acs.jpclett.1c01494	journal	June 2021
Beyond Shielding: The Roles of Glycans in the SARS-CoV-2 Spike Protein Casalino, Lorenzo; Gaieb, Zied; Goldsmith, Jory A. ACS Central Science, Vol. 6, Issue 10 https://doi.org/10.1021/acscentsci.0c01056	journal	September 2020
Free Energy Landscapes from SARS-CoV-2 Spike Glycoprotein Simulations Suggest that RBD Opening Can Be Modulated via Interactions in an Allosteric Pocket Fallon, Lucy; Belfon, Kellon A. A.; Raguette, Lauren Journal of the American Chemical Society, Vol. 143, Issue 30 https://doi.org/10.1021/jacs.1c00556	journal	July 2021
Cryo-electron microscopy structures of the SARS-CoV spike glycoprotein reveal a prerequisite conformational state for receptor binding Gui, Miao; Song, Wenfei; Zhou, Haixia Cell Research, Vol. 27, Issue 1 https://doi.org/10.1038/cr.2016.152	journal	December 2016
Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus Li, Wenhui; Moore, Michael J.; Vasilieva, Natalya Nature, Vol. 426, Issue 6965 https://doi.org/10.1038/nature02145	journal	November 2003
Cryo-EM structures of MERS-CoV and SARS-CoV spike glycoproteins reveal the dynamic receptor binding domains Yuan, Yuan; Cao, Duanfang; Zhang, Yanfang Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15092	journal	April 2017
The I-TASSER Suite: protein structure and function prediction Yang, Jianyi; Yan, Renxiang; Roy, Ambrish Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3213	journal	December 2014
Glycan shield and epitope masking of a coronavirus spike protein observed by cryo-electron microscopy Walls, Alexandra C.; Tortorici, M. Alejandra; Frenz, Brandon Nature Structural & Molecular Biology, Vol. 23, Issue 10 https://doi.org/10.1038/nsmb.3293	journal	September 2016
Vulnerabilities in coronavirus glycan shields despite extensive glycosylation Watanabe, Yasunori; Berndsen, Zachary T.; Raghwani, Jayna Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16567-0	journal	May 2020
Cryo-EM analysis of the HCoV-229E spike glycoprotein reveals dynamic prefusion conformational changes Song, Xiyong; Shi, Yuejun; Ding, Wei Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-020-20401-y	journal	January 2021
A conserved immunogenic and vulnerable site on the coronavirus spike protein delineated by cross-reactive monoclonal antibodies Wang, Chunyan; van Haperen, Rien; Gutiérrez-Álvarez, Javier Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21968-w	journal	March 2021
In situ structure and dynamics of an alphacoronavirus spike protein by cryo-ET and cryo-EM Huang, Cheng-Yu; Draczkowski, Piotr; Wang, Yong-Sheng Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-32588-3	journal	August 2022
SARS-CoV-2 simulations go exascale to predict dramatic spike opening and cryptic pockets across the proteome Zimmerman, Maxwell I.; Porter, Justin R.; Ward, Michael D. Nature Chemistry, Vol. 13, Issue 7 https://doi.org/10.1038/s41557-021-00707-0	journal	May 2021
A glycan gate controls opening of the SARS-CoV-2 spike protein Sztain, Terra; Ahn, Surl-Hee; Bogetti, Anthony T. Nature Chemistry, Vol. 13, Issue 10 https://doi.org/10.1038/s41557-021-00758-3	journal	August 2021
SARS-CoV-2 variants, spike mutations and immune escape Harvey, William T.; Carabelli, Alessandro M.; Jackson, Ben Nature Reviews Microbiology, Vol. 19, Issue 7 https://doi.org/10.1038/s41579-021-00573-0	journal	June 2021
Structural basis of receptor recognition by SARS-CoV-2 Shang, Jian; Ye, Gang; Shi, Ke Nature, Vol. 581, Issue 7807 https://doi.org/10.1038/s41586-020-2179-y	journal	March 2020
Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor Lan, Jun; Ge, Jiwan; Yu, Jinfang Nature, Vol. 581, Issue 7807 https://doi.org/10.1038/s41586-020-2180-5	journal	March 2020
SARS-CoV-2 mRNA vaccine design enabled by prototype pathogen preparedness Corbett, Kizzmekia S.; Edwards, Darin K.; Leist, Sarah R. Nature, Vol. 586, Issue 7830 https://doi.org/10.1038/s41586-020-2622-0	journal	August 2020
Structures and distributions of SARS-CoV-2 spike proteins on intact virions Ke, Zunlong; Oton, Joaquin; Qu, Kun Nature, Vol. 588, Issue 7838 https://doi.org/10.1038/s41586-020-2665-2	journal	August 2020
BNT162b vaccines protect rhesus macaques from SARS-CoV-2 Vogel, Annette B.; Kanevsky, Isis; Che, Ye Nature, Vol. 592, Issue 7853 https://doi.org/10.1038/s41586-021-03275-y	journal	February 2021
Engineered ACE2 decoy mitigates lung injury and death induced by SARS-CoV-2 variants Zhang, Lianghui; Dutta, Soumajit; Xiong, Shiqin Nature Chemical Biology, Vol. 18, Issue 3 https://doi.org/10.1038/s41589-021-00965-6	journal	January 2022
A complete data processing workflow for cryo-ET and subtomogram averaging Chen, Muyuan; Bell, James M.; Shi, Xiaodong Nature Methods, Vol. 16, Issue 11 https://doi.org/10.1038/s41592-019-0591-8	journal	October 2019
Measurement of atom resolvability in cryo-EM maps with Q-scores Pintilie, Grigore; Zhang, Kaiming; Su, Zhaoming Nature Methods, Vol. 17, Issue 3 https://doi.org/10.1038/s41592-020-0731-1	journal	February 2020
Precise, fast and comprehensive analysis of intact glycopeptides and modified glycans with pGlyco3 Zeng, Wen-Feng; Cao, Wei-Qian; Liu, Ming-Qi Nature Methods, Vol. 18, Issue 12 https://doi.org/10.1038/s41592-021-01306-0	journal	November 2021
ColabFold: making protein folding accessible to all Mirdita, Milot; Schütze, Konstantin; Moriwaki, Yoshitaka Nature Methods, Vol. 19, Issue 6 https://doi.org/10.1038/s41592-022-01488-1	journal	May 2022
Structural basis for broad coronavirus neutralization Sauer, Maximilian M.; Tortorici, M. Alejandra; Park, Young-Jun Nature Structural & Molecular Biology, Vol. 28, Issue 6 https://doi.org/10.1038/s41594-021-00596-4	journal	May 2021
Structural definition of a pan-sarbecovirus neutralizing epitope on the spike S2 subunit Hurlburt, Nicholas K.; Homad, Leah J.; Sinha, Irika Communications Biology, Vol. 5, Issue 1 https://doi.org/10.1038/s42003-022-03262-7	journal	April 2022
Inhibitor binding influences the protonation states of histidines in SARS-CoV-2 main protease Pavlova, Anna; Lynch, Diane L.; Daidone, Isabella Chemical Science, Vol. 12, Issue 4 https://doi.org/10.1039/D0SC04942E	journal	January 2021
ACE2 glycans preferentially interact with SARS-CoV-2 over SARS-CoV Acharya, Atanu; Lynch, Diane L.; Pavlova, Anna Chemical Communications, Vol. 57, Issue 48 https://doi.org/10.1039/D1CC02305E	journal	January 2021
Exploring cryo-electron microscopy with molecular dynamics Vant, John W.; Sarkar, Daipayan; Nguyen, Jonathan Biochemical Society Transactions, Vol. 50, Issue 1 https://doi.org/10.1042/BST20210485	journal	February 2022
Covid-19 Vaccines — Immunity, Variants, Boosters Barouch, Dan H. New England Journal of Medicine, Vol. 387, Issue 11 https://doi.org/10.1056/NEJMra2206573	journal	September 2022
Conformational transition of SARS-CoV-2 spike glycoprotein between its closed and open states Gur, Mert; Taka, Elhan; Yilmaz, Sema Zeynep The Journal of Chemical Physics, Vol. 153, Issue 7 https://doi.org/10.1063/5.0011141	journal	August 2020
Scalable molecular dynamics on CPU and GPU architectures with NAMD Phillips, James C.; Hardy, David J.; Maia, Julio D. C. The Journal of Chemical Physics, Vol. 153, Issue 4 https://doi.org/10.1063/5.0014475	journal	July 2020
Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry Hofmann, H.; Pyrc, K.; van der Hoek, L. Proceedings of the National Academy of Sciences, Vol. 102, Issue 22 https://doi.org/10.1073/pnas.0409465102	journal	May 2005
Crystal structure of NL63 respiratory coronavirus receptor-binding domain complexed with its human receptor Wu, K.; Li, W.; Peng, G. Proceedings of the National Academy of Sciences, Vol. 106, Issue 47 https://doi.org/10.1073/pnas.0908837106	journal	November 2009
Structure of the Lassa virus glycan shield provides a model for immunological resistance Watanabe, Yasunori; Raghwani, Jayna; Allen, Joel D. Proceedings of the National Academy of Sciences, Vol. 115, Issue 28 https://doi.org/10.1073/pnas.1803990115	journal	June 2018
Influenza hemagglutinin membrane anchor Benton, Donald J.; Nans, Andrea; Calder, Lesley J. Proceedings of the National Academy of Sciences, Vol. 115, Issue 40 https://doi.org/10.1073/pnas.1810927115	journal	September 2018
Cryo-EM analysis of a feline coronavirus spike protein reveals a unique structure and camouflaging glycans Yang, Tzu-Jing; Chang, Yen-Chen; Ko, Tzu-Ping Proceedings of the National Academy of Sciences, Vol. 117, Issue 3 https://doi.org/10.1073/pnas.1908898117	journal	January 2020
Engineered ACE2 receptor traps potently neutralize SARS-CoV-2 Glasgow, Anum; Glasgow, Jeff; Limonta, Daniel Proceedings of the National Academy of Sciences, Vol. 117, Issue 45 https://doi.org/10.1073/pnas.2016093117	journal	October 2020
Posttranslational modifications optimize the ability of SARS-CoV-2 spike for effective interaction with host cell receptors Kapoor, Karan; Chen, Tianle; Tajkhorshid, Emad Proceedings of the National Academy of Sciences, Vol. 119, Issue 28 https://doi.org/10.1073/pnas.2119761119	journal	June 2022
Conformational preferences of triantennary and tetraantennary hybrid N-glycans in aqueous solution: Insights from 20 μs long atomistic molecular dynamic simulations Roy, Rajarshi; Poddar, Sayan; Sk, Md Fulbabu Journal of Biomolecular Structure and Dynamics, Vol. 41, Issue 8 https://doi.org/10.1080/07391102.2022.2047109	journal	March 2022
Human Coronavirus NL63 Molecular Epidemiology and Evolutionary Patterns in Rural Coastal Kenya Kiyuka, Patience K.; Agoti, Charles N.; Munywoki, Patrick K. The Journal of Infectious Diseases, Vol. 217, Issue 11 https://doi.org/10.1093/infdis/jiy098	journal	March 2018
electronic Ligand Builder and Optimization Workbench ( eLBOW ): a tool for ligand coordinate and restraint generation Moriarty, Nigel W.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 10 https://doi.org/10.1107/S0907444909029436	journal	September 2009
Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation Wrapp, Daniel; Wang, Nianshuang; Corbett, Kizzmekia S. Science, Vol. 367, Issue 6483 https://doi.org/10.1126/science.abb2507	journal	February 2020
Site-specific glycan analysis of the SARS-CoV-2 spike Watanabe, Yasunori; Allen, Joel D.; Wrapp, Daniel Science, Vol. 369, Issue 6501 https://doi.org/10.1126/science.abb9983	journal	May 2020
In situ structural analysis of SARS-CoV-2 spike reveals flexibility mediated by three hinges Turoňová, Beata; Sikora, Mateusz; Schürmann, Christoph Science, Vol. 370, Issue 6513 https://doi.org/10.1126/science.abd5223	journal	August 2020
De novo design of picomolar SARS-CoV-2 miniprotein inhibitors Cao, Longxing; Goreshnik, Inna; Coventry, Brian Science, Vol. 370, Issue 6515 https://doi.org/10.1126/science.abd9909	journal	September 2020
Broad betacoronavirus neutralization by a stem helix–specific human antibody Pinto, Dora; Sauer, Maximilian M.; Czudnochowski, Nadine Science, Vol. 373, Issue 6559 https://doi.org/10.1126/science.abj3321	journal	September 2021
A human antibody reveals a conserved site on beta-coronavirus spike proteins and confers protection against SARS-CoV-2 infection Zhou, Panpan; Yuan, Meng; Song, Ge Science Translational Medicine, Vol. 14, Issue 637 https://doi.org/10.1126/scitranslmed.abi9215	journal	March 2022
Multivalent designed proteins neutralize SARS-CoV-2 variants of concern and confer protection against infection in mice Hunt, Andrew C.; Case, James Brett; Park, Young-Jun Science Translational Medicine, Vol. 14, Issue 646 https://doi.org/10.1126/scitranslmed.abn1252	journal	May 2022
An engineered ACE2 decoy neutralizes the SARS-CoV-2 Omicron variant and confers protection against infection in vivo Ikemura, Nariko; Taminishi, Shunta; Inaba, Tohru Science Translational Medicine, Vol. 14, Issue 650 https://doi.org/10.1126/scitranslmed.abn7737	journal	June 2022
Cryo-Electron Microscopy Structure of Porcine Deltacoronavirus Spike Protein in the Prefusion State Shang, Jian; Zheng, Yuan; Yang, Yang Journal of Virology, Vol. 92, Issue 4 https://doi.org/10.1128/JVI.01556-17	journal	February 2018
Structure, Function, and Evolution of Coronavirus Spike Proteins Li, Fang Annual Review of Virology, Vol. 3, Issue 1 https://doi.org/10.1146/annurev-virology-110615-042301	journal	September 2016
Coronavirus Disease-19 (COVID-19): A Perspective of New Scenario Niaz, Kamal; Nisar, Muhammad Farrukh https://doi.org/10.2174/97816810890721210201	book	October 2021
Characterization of Structural and Energetic Differences between Conformations of the SARS-CoV-2 Spike Protein Moreira, Rodrigo A.; Guzman, Horacio V.; Boopathi, Subramanian Materials, Vol. 13, Issue 23 https://doi.org/10.3390/ma13235362	journal	November 2020
Molecular dynamics-based refinement and validation for sub-5 Å cryo-electron microscopy maps Singharoy, Abhishek; Teo, Ivan; McGreevy, Ryan eLife, Vol. 5 https://doi.org/10.7554/eLife.16105	journal	July 2016
The human coronavirus HCoV-229E S-protein structure and receptor binding Li, Zhijie; Tomlinson, Aidan CA; Wong, Alan HM eLife, Vol. 8 https://doi.org/10.7554/eLife.51230	journal	October 2019
Evidence for adaptive evolution in the receptor-binding domain of seasonal coronaviruses OC43 and 229e Kistler, Kathryn E.; Bedford, Trevor eLife, Vol. 10 https://doi.org/10.7554/eLife.64509	journal	January 2021

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