Synthetic virions reveal fatty acid-coupled adaptive immunogenicity of SARS-CoV-2 spike glycoprotein.
A549 Cells
Allosteric Site
/ genetics
Amino Acid Sequence
Antibodies, Neutralizing
/ immunology
Antibodies, Viral
/ immunology
Binding Sites
/ genetics
COVID-19
/ immunology
Cells, Cultured
Cryoelectron Microscopy
/ methods
Electron Microscope Tomography
/ methods
Fatty Acid-Binding Proteins
/ immunology
Fatty Acids
/ immunology
Humans
MCF-7 Cells
Microscopy, Confocal
/ methods
Protein Binding
SARS-CoV-2
/ immunology
Sequence Homology, Amino Acid
Spike Glycoprotein, Coronavirus
/ genetics
Virion
/ immunology
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
14 02 2022
14 02 2022
Historique:
received:
09
07
2021
accepted:
24
01
2022
entrez:
15
2
2022
pubmed:
16
2
2022
medline:
1
3
2022
Statut:
epublish
Résumé
SARS-CoV-2 infection is a major global public health concern with incompletely understood pathogenesis. The SARS-CoV-2 spike (S) glycoprotein comprises a highly conserved free fatty acid binding pocket (FABP) with unknown function and evolutionary selection advantage
Identifiants
pubmed: 35165285
doi: 10.1038/s41467-022-28446-x
pii: 10.1038/s41467-022-28446-x
pmc: PMC8844029
doi:
Substances chimiques
Antibodies, Neutralizing
0
Antibodies, Viral
0
Fatty Acid-Binding Proteins
0
Fatty Acids
0
Spike Glycoprotein, Coronavirus
0
spike glycoprotein, SARS-CoV
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
868Subventions
Organisme : Bundesministerium für Bildung und Forschung (Federal Ministry of Education and Research)
ID : MaxSynBio Consortium
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : SFB 1129
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : Gottfried-Wilhelm-Leibniz Program
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Max-Planck-Gesellschaft (Max Planck Society)
ID : Max Planck School Matter to Life
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/L01386X/1
Pays : United Kingdom
Informations de copyright
© 2022. The Author(s).
Références
Toelzer, C. et al. Free fatty acid binding pocket in the locked structure of SARS-CoV-2 spike protein. Science 370, 725–730 (2020).
pubmed: 32958580
pmcid: 8050947
doi: 10.1126/science.abd3255
Bangaru, S. et al. Structural analysis of full-length SARS-CoV-2 spike protein from an advanced vaccine candidate. Science 370, 1089–1094 (2020).
pubmed: 33082295
pmcid: 7857404
doi: 10.1126/science.abe1502
Shang, J. et al. Structural basis of receptor recognition by SARS-CoV-2. Nature 581, 221–224 (2020).
pubmed: 32225175
pmcid: 7328981
doi: 10.1038/s41586-020-2179-y
Benton, D. J. et al. Receptor binding and priming of the spike protein of SARS-CoV-2 for membrane fusion. Nature 588, 327–330 (2020).
pubmed: 32942285
pmcid: 7116727
doi: 10.1038/s41586-020-2772-0
Piccoli, L. et al. Mapping neutralizing and immunodominant sites on the SARS-CoV-2 spike receptor-binding domain by structure-guided high-resolution serology. Cell 183, 1024–1042.e1021 (2020).
pubmed: 32991844
pmcid: 7494283
doi: 10.1016/j.cell.2020.09.037
Grant, O. C., Montgomery, D., Ito, K. & Woods, R. J. Analysis of the SARS-CoV-2 spike protein glycan shield reveals implications for immune recognition. Sci. Rep. 10, 14991 (2020).
pubmed: 32929138
pmcid: 7490396
doi: 10.1038/s41598-020-71748-7
Wrapp, D. et al. Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation. Science 367, 1260–1263 (2020).
pubmed: 32075877
pmcid: 7164637
doi: 10.1126/science.abb2507
Walls, A. C. et al. Structure, function, and antigenicity of the SARS-CoV-2 spike glycoprotein. Cell 181, 281–292.e286 (2020).
pubmed: 32155444
pmcid: 7102599
doi: 10.1016/j.cell.2020.02.058
Xu, C. et al. Conformational dynamics of SARS-CoV-2 trimeric spike glycoprotein in complex with receptor ACE2 revealed by cryo-EM. Sci. Adv. 7, eabe5575 (2021).
pubmed: 33277323
pmcid: 7775788
doi: 10.1126/sciadv.abe5575
Ke, Z. et al. Structures and distributions of SARS-CoV-2 spike proteins on intact virions. Nature 588, 498–502 (2020).
pubmed: 32805734
pmcid: 7116492
doi: 10.1038/s41586-020-2665-2
Casari, I., Manfredi, M., Metharom, P. & Falasca, M. Dissecting lipid metabolism alterations in SARS-CoV-2. Prog. Lipid Res. https://doi.org/10.1016/j.plipres.2021.101092 (2021).
Yan, B. et al. Characterization of the lipidomic profile of human coronavirus-infected cells: implications for lipid metabolism remodeling upon coronavirus replication. Viruses 11, 73 (2019).
pmcid: 6357182
doi: 10.3390/v11010073
Zheng, H. et al. Metabolomics reveals sex-specific metabolic shifts and predicts the duration from positive to negative in non-severe COVID-19 patients during recovery process. Comput. Struct. Biotechnol. J. https://doi.org/10.1016/j.csbj.2021.03.039 (2021).
Doaei, S. et al. The effect of omega-3 fatty acid supplementation on clinical and biochemical parameters of critically ill patients with COVID-19: a randomized clinical trial. J. Transl. Med. 19, 128 (2021).
pubmed: 33781275
pmcid: 8006115
doi: 10.1186/s12967-021-02795-5
Jonsson, S., Mendenhall, M. & Jonsson, C. Case Study Using Nebulized Isomerized Linoleic Acid (LA) for Outpatient Treatment of Symptomatic COVID-19. https://doi.org/10.2139/ssrn.3733231 (SSRN, 2020).
Hammock, B. D., Wang, W., Gilligan, M. M. & Panigrahy, D. Eicosanoids: The overlooked storm in coronavirus disease 2019 (COVID-19)? Am. J. Pathol. 190, 1782–1788 (2020).
pubmed: 32650004
pmcid: 7340586
doi: 10.1016/j.ajpath.2020.06.010
Tay, M. Z., Poh, C. M., Rénia, L., MacAry, P. A. & Ng, L. F. P. The trinity of COVID-19: immunity, inflammation and intervention. Nat. Rev. Immunol. 20, 363–374 (2020).
pubmed: 32346093
doi: 10.1038/s41577-020-0311-8
Kratzer, B., Hofer, S., Zabel, M. & Pickl, W. F. All the small things: how virus-like particles and liposomes modulate allergic immune responses. Eur. J. Immunol. 50, 17–32 (2020).
pubmed: 31799700
doi: 10.1002/eji.201847810
Mandala, V. S. et al. Structure and drug binding of the SARS-CoV-2 envelope protein transmembrane domain in lipid bilayers. Nat. Struct. Mol. Biol. 27, 1202–1208 (2020).
pubmed: 33177698
pmcid: 7718435
doi: 10.1038/s41594-020-00536-8
Bar-On, Y. M., Flamholz, A., Phillips, R. & Milo, R. SARS-CoV-2 (COVID-19) by the numbers. Elife https://doi.org/10.7554/eLife.57309 (2020).
Abhishek, S. et al. Electroceutical fabric lowers zeta potential and eradicates coronavirus infectivity upon contact. ChemRxiv https://doi.org/10.26434/chemrxiv.12307214.v1 (2020).
Zhang, Q. et al. ACE2 inhibits breast cancer angiogenesis via suppressing the VEGFa/VEGFR2/ERK pathway. J. Exp. Clin. Cancer Res. 38, 173–173 (2019).
pubmed: 31023337
pmcid: 6482513
doi: 10.1186/s13046-019-1156-5
Schneider, M. et al. Severe acute respiratory syndrome coronavirus replication is severely impaired by MG132 due to proteasome-independent inhibition of M-calpain. J. Virol. 86, 10112–10122 (2012).
pubmed: 22787216
pmcid: 3446591
doi: 10.1128/JVI.01001-12
Cortese, M. et al. Integrative imaging reveals SARS-CoV-2-induced reshaping of subcellular morphologies. Cell Host Microbe 28, 853–866.e855 (2020).
pubmed: 33245857
pmcid: 7670925
doi: 10.1016/j.chom.2020.11.003
Ramanathan, M., Ferguson, I. D., Miao, W. & Khavari, P. A. SARS-CoV-2 B.1.1.7 and B.1.351 spike variants bind human ACE2 with increased affinity. bioRxiv https://doi.org/10.1101/2021.02.22.432359 (2021).
Richieri, G. V. & Kleinfeld, A. M. Unbound free fatty acid levels in human serum. J. Lipid Res. 36, 229–240 (1995).
pubmed: 7751810
doi: 10.1016/S0022-2275(20)39899-0
Archambault, A.-S. et al. Lipid storm within the lungs of severe COVID-19 patients: extensive levels of cyclooxygenase and lipoxygenase-derived inflammatory metabolites. medRxiv https://doi.org/10.1101/2020.12.04.20242115 (2020).
Hoffmann, M. et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell 181, 271–280.e278 (2020).
pubmed: 32142651
pmcid: 7102627
doi: 10.1016/j.cell.2020.02.052
Hoffmann, M. et al. Camostat mesylate inhibits SARS-CoV-2 activation by TMPRSS2-related proteases and its metabolite GBPA exerts antiviral activity. EBioMedicine https://doi.org/10.1016/j.ebiom.2021.103255 (2021).
Jaimes, J. A., André, N. M., Chappie, J. S., Millet, J. K. & Whittaker, G. R. Phylogenetic analysis and structural modeling of SARS-CoV-2 spike protein reveals an evolutionary distinct and proteolytically sensitive activation loop. J. Mol. Biol. 432, 3309–3325 (2020).
pubmed: 32320687
pmcid: 7166309
doi: 10.1016/j.jmb.2020.04.009
Ozono, S. et al. SARS-CoV-2 D614G spike mutation increases entry efficiency with enhanced ACE2-binding affinity. Nat. Commun. 12, 848 (2021).
pubmed: 33558493
pmcid: 7870668
doi: 10.1038/s41467-021-21118-2
Johnson, B. A. et al. Loss of furin cleavage site attenuates SARS-CoV-2 pathogenesis. Nature 591, 293–299 (2021).
pubmed: 33494095
pmcid: 8175039
doi: 10.1038/s41586-021-03237-4
Makowski, L., Olson-Sidford, W. & W-Weisel, J. Biological and clinical consequences of integrin binding via a rogue RGD motif in the SARS CoV-2 spike protein. Viruses https://doi.org/10.3390/v13020146 (2021).
Maginnis, M. S. et al. Beta1 integrin mediates internalization of mammalian reovirus. J. Virol. 80, 2760–2770 (2006).
pubmed: 16501085
pmcid: 1395463
doi: 10.1128/JVI.80.6.2760-2770.2006
Shoemark, D. K. et al. Molecular simulations suggest vitamins, retinoids and steroids as ligands of the free Fatty acid pocket of the SARS-CoV-2 spike protein**. Angew. Chem. Int. Ed. 60, 7098–7110 (2021).
Dofferhoff, A. S. M. et al. Reduced vitamin K status as a potentially modifiable risk factor of severe COVID-19. Clin. Infect. Dis. https://doi.org/10.1093/cid/ciaa1258 (2020).
The RECOVERY Collaborative Group. Dexamethasone in hospitalized patients with Covid-19. N. Engl. J. Med. 384, 693–704 (2020).
Zhang, S. et al. Bat and pangolin coronavirus spike glycoprotein structures provide insights into SARS-CoV-2 evolution. Nat. Commun. 12, 1607 (2021).
pubmed: 33707453
pmcid: 7952905
doi: 10.1038/s41467-021-21767-3
Cevik, M. et al. SARS-CoV-2, SARS-CoV, and MERS-CoV viral load dynamics, duration of viral shedding, and infectiousness: a systematic review and meta-analysis. Lancet Microbe 2, e13–e22 (2021).
pubmed: 33521734
doi: 10.1016/S2666-5247(20)30172-5
Hermesh, T., Moltedo, B., López, C. B. & Moran, T. M. Buying time-the immune system determinants of the incubation period to respiratory. Viruses. Viruses 2, 2541–2558 (2010).
pubmed: 21994630
doi: 10.3390/v2112541
Greaney, A. J. et al. Complete mapping of mutations to the SARS-CoV-2 spike receptor-binding domain that escape antibody recognition. Cell Host Microbe 29, 44–57.e49 (2021).
pubmed: 33259788
pmcid: 7676316
doi: 10.1016/j.chom.2020.11.007
Wrobel, A. G. et al. Antibody-mediated disruption of the SARS-CoV-2 spike glycoprotein. Nat. Commun. 11, 5337 (2020).
pubmed: 33087721
pmcid: 7577971
doi: 10.1038/s41467-020-19146-5
Atyeo, C. et al. Dissecting strategies to tune the therapeutic potential of SARS-CoV-2-specific monoclonal antibody CR3022. JCI Insight 6, e143129 https://doi.org/10.1172/jci.insight.143129 (2021).
Greaney, A. J. et al. Comprehensive mapping of mutations in the SARS-CoV-2 receptor-binding domain that affect recognition by polyclonal human plasma antibodies. Cell Host Microbe 29, 463–476.e466 (2021).
pubmed: 33592168
pmcid: 7869748
doi: 10.1016/j.chom.2021.02.003
Schaffitzel, C. et al. In vitro selection and evolution of protein-ligand interactions by ribosome display. in Protein-Protein Interactions: A Molecular Cloning Manual (ed. Golemis, E. Adams, P.). Ch. 27, (Cold Spring Harbor Laboratory Press, 2005).
Brash, A. R. Arachidonic acid as a bioactive molecule. J. Clin. Invest. 107, 1339–1345 (2001).
pubmed: 11390413
pmcid: 209328
doi: 10.1172/JCI13210
Adam, L. et al. Dynamics of SARS-CoV-2 host cell interactions inferred from transcriptome analyses. bioRxiv https://doi.org/10.1101/2021.07.04.450986 (2021).
Tan, H.-X. et al. Immunogenicity of prime-boost protein subunit vaccine strategies against SARS-CoV-2 in mice and macaques. Nat. Commun. 12, 1403 (2021).
pubmed: 33658497
pmcid: 7930087
doi: 10.1038/s41467-021-21665-8
Pombo, J. P. & Sanyal, S. Perturbation of intracellular cholesterol and fatty acid homeostasis during flavivirus infections. Front. Immunol. https://doi.org/10.3389/fimmu.2018.01276 (2018).
Staufer, O. et al. Microfluidic production and characterization of biofunctionalized giant unilamellar vesicles for targeted intracellular cargo delivery. Biomaterials 264, 120203 (2021).
pubmed: 32987317
doi: 10.1016/j.biomaterials.2020.120203
Staufer, O. et al. Bottom-up assembly of biomedical relevant fully synthetic extracellular vesicles. Sci. Adv. 7, eabg6666 (2021).
pubmed: 34516902
pmcid: 8442894
doi: 10.1126/sciadv.abg6666
Berger, I., Fitzgerald, D. J. & Richmond, T. J. Baculovirus expression system for heterologous multiprotein complexes. Nat. Biotechnol. 22, 1583–1587 (2004).
pubmed: 15568020
doi: 10.1038/nbt1036
Frampton, D. et al. Genomic characteristics and clinical effect of the emergent SARS-CoV-2 B.1.1.7 lineage in London, UK: a whole-genome sequencing and hospital-based cohort study. Lancet Infect. Dis. https://doi.org/10.1016/S1473-3099(21)00170-5 .
Schaffitzel, C., Hanes, J., Jermutus, L. & Plückthun, A. Ribosome display: an in vitro method for selection and evolution of antibodies from libraries. J. Immunol. Methods 231, 119–135 (1999).
pubmed: 10648932
doi: 10.1016/S0022-1759(99)00149-0
Els Conrath, K., Lauwereys, M., Wyns, L. & Muyldermans, S. Camel single-domain antibodies as modular building units in bispecific and bivalent antibody constructs. J. Biol. Chem. 276, 7346–7350 (2001).
pubmed: 11053416
doi: 10.1074/jbc.M007734200
Staufer, O., Schroter, M., Platzman, I. & Spatz, J. P. Bottom-up assembly of functional intracellular synthetic organelles by droplet-based microfluidics. Small https://doi.org/10.1002/smll.201906424 (2020).
Staufer, O. et al. Adhesion stabilized en masse intracellular electrical recordings from multicellular assemblies. Nano Lett. 19, 3244–3255 (2019).
pubmed: 30950627
pmcid: 6727598
doi: 10.1021/acs.nanolett.9b00784
Staufer, O. et al. Functional fusion of living systems with synthetic electrode interfaces. Beilstein J. Nanotechnol. 7, 296–301 (2016).
pubmed: 26977386
pmcid: 4778514
doi: 10.3762/bjnano.7.27
Zivanov, J. et al. New tools for automated high-resolution cryo-EM structure determination in RELION-3. Elife https://doi.org/10.7554/eLife.42166 (2018).
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
pubmed: 28250466
pmcid: 5494038
Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71–76 (1996).
pubmed: 8742726
doi: 10.1006/jsbi.1996.0013
Keller, C. A. & Kasemo, B. Surface specific kinetics of lipid vesicle adsorption measured with a quartz crystal microbalance. Biophys. J. 75, 1397–1402 (1998).
pubmed: 9726940
pmcid: 1299813
doi: 10.1016/S0006-3495(98)74057-3
Briand, E., Zäch, M., Svedhem, S., Kasemo, B. & Petronis, S. Combined QCM-D and EIS study of supported lipid bilayer formation and interaction with pore-forming peptides. Analyst 135, 343–350 (2010).
pubmed: 20098769
doi: 10.1039/B918288H
Wintjens, R., Bifani, A. M. & Bifani, P. Impact of glycan cloud on the B-cell epitope prediction of SARS-CoV-2 Spike protein. npj Vaccines 5, 81 (2020).
pubmed: 32944295
pmcid: 7474083
doi: 10.1038/s41541-020-00237-9
Marsh, J. A. & Teichmann, S. A. Relative solvent accessible surface area predicts protein conformational changes upon binding. Structure 19, 859–867 (2011).
pubmed: 21645856
pmcid: 3145976
doi: 10.1016/j.str.2011.03.010
Sehnal, D. et al. Mol* Viewer: modern web app for 3D visualization and analysis of large biomolecular structures. Nucleic Acids Res. 49, W431–W437 (2021).
pubmed: 33956157
pmcid: 8262734
doi: 10.1093/nar/gkab314
Else, P. L. The highly unnatural fatty acid profile of cells in culture. Prog. Lipid Res. 77, 101017 (2020).
pubmed: 31809755
doi: 10.1016/j.plipres.2019.101017
Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods (San. Diego, Calif.) 25, 402–408 (2001).
doi: 10.1006/meth.2001.1262