PMC:7253482 / 27038-36048 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7253482","sourcedb":"PMC","sourceid":"7253482","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7253482","text":"Methods\n\nExpression and purification of coronavirus spike glycoproteins\nHuman embryonic kidney 293 Freestyle (HEK293F) cells were transfected with mammalian-codon-optimised genes encoding 2P-stabilised SARS MERS and HKU1 S proteins containing a C-terminal T4 fibritin trimerization domain, an HRV3C cleavage site, an 8xHis-tag and a Twin-Strep-tag41. H3N2 Victoria 2011 hemagglutinin was also expressed in the HEK293F cells. The 200 ml cultures were harvested 6 days after transfection, filtered and purified by nickel-affinity chromatography and size exclusion chromatography using a SuperdexTM 16/600 75 pg column (GE Healthcare).\n\nRelease and labelling of N-linked glycans\nExcised coronavirus S gel bands were washed alternately with acetonitrile and water before drying in a vacuum centrifuge. The bands were rehydrated with 100 μL of water and incubated with PNGase F at 37 °C overnight. Aliquots of released N-linked glycans were also fluorescently labelled with procainamide, by adding 100 μL of labelling mixture (110 mg/mL procainamide and 60 mg/mL sodium cyanoborohydrate in 70% DMSO and 30% glacial acetic acid) and incubating for 4 h at 65 °C. Procainamide labelled glycans were purified using Spe-ed Amide 2 columns (Applied Separations).\n\nGlycan analysis by HILIC-UPLC\nLabelled glycans were analysed using a 2.1 mm × 150 mm Acquity BEH Glycan column (Waters) on an Acquity H-Class UPLC instrument (Waters), with fluorescence measurements occurring at λex = 310 nm and λem = 370 nm. The following gradient was used: time (t) = 0: 22% A, 78% B (flow rate = 0.5 mL/min); t = 38.5: 44.1% A, 55.9% B (0.5 mL/min); t = 39.5: 100% A, 0% B (0.25 mL/min); t = 44.5: 100% A, 0% B (0.25 mL/min); t = 46.5: 22% A, 78% B (0.5 mL/min), where solvent A was 50 mM ammonium formate (pH 4.4) and B was acetonitrile. Quantification of oligomannose-type glycans was achieved by digestion of fluorescently labelled glycans with Endo H, and clean-up using a PVDF protein-binding membrane (Millipore). Empower 3 software (Waters) was used for data processing.\n\nMass spectrometry of glycans\nPrior to ion-mobility electrospray ionisation MS and tandem MS analysis, PNGase F released N-linked glycans were purified on a Nafion® 117 membrane (Sigma-Aldrich) and a trace amount of ammonium phosphate was added to promote phosphate adduct formation. Glycans were analyzed by direct infusion using a Synapt G2Si instrument (Waters) with the following settings: capillary voltage, 0.8–1.0 kV; sample cone, 150 V; extraction cone, 150 V; cone gas, 40 l/h; source temperature, 80 °C; trap collision voltage, 4–160 V; transfer collision voltage, 4 V; trap DC bias, 60 V; IMS wave velocity, 450 m/s; IMS wave height, 40 V; trap gas flow, 2 ml/min; IMS gas flow, 80 ml/min. Data were acquired and processed with MassLynx v4.1 and Driftscope version 2.8 software (Waters).\n\nMass spectrometry of glycopeptides\nAliquots of 30–50 μg of coronavirus spikes were denatured, reduced and alkylated as described previously36. Proteins were proteolytically digested with trypsin (Promega), chymotrypsin (Promega), alpha-lytic protease (Sigma-Aldrich) and Glu-C (Promega). Reaction mixtures were dried and peptides/glycopeptides were extracted using C18 Zip-tip (MerckMilipore) following the manufacturer’s protocol. Samples were resuspended in 0.1% formic acid prior to analysis by liquid chromatography-mass spectrometry using an Easy-nLC 1200 system coupled to an Orbitrap Fusion mass spectrometer (Thermo Fisher Scientific). Glycopeptides were separated using an EasySpray PepMap RSLC C18 column (75 μm × 75 cm) with a 240-min linear solvent gradient of 0–32% acetonitrile in 0.1% formic acid, followed by 35 min of 80% acetonitrile in 0.1% formic acid. Other settings include an LC flow rate of 200 nL/min, spray voltage of 2.8 kV, capillary temperature of 275 °C, and an HCD collision energy of 50%. Precursor and fragmentation detection were performed using an Orbitrap at the following resolution: MS1 = 100,000 and MS2 = 30,000. The automatic gain control (AGC) targets were MS1 = 4e5 and MS2 = 5e4, and injection times were MS1 = 50 and MS2 = 54. The following cleavage sites were used for the respective proteases; trypsin=R/K, chymotrypsin=F/Y/W, alpha lytic protease=T/A/S/V, Glu C=E/D. Number of missed cleavages were set at 3. The following modifications were also included: Carbamidomethyl (+57.021464, target=C, fine control=fixed), Oxidation (+15.994915, target=M, fine control=variable rare 1), Glu to pyro-Glu (−18.010565, target=peptide N-term E, fine control=variable rare 1), and Gln to pyro-Glu (−17.026549, target peptide N-term Q, fine control=variable rare 1). Glycopeptide fragmentation data were extracted form raw files using ByonicTM (Version 3.5.0) and ByologicTM (Version 3.5-15; Protein Metrics Inc.). Glycopeptide fragmentation data were manually evaluated with true-positive assignments given when correct b- and y-fragments and oxonium ions corresponding to the peptide and glycan, respectively, were observed. The precursor mass tolerance was set at 4 ppm for precursor ions and 10 ppm for fragment ions. MS data were searched using a glycan library (SI Fig. 9) with the identical peptide sequence. A 1% false discovery rate (FDR) was applied. The extracted ion chromatographic areas for each true-positive glycopeptide, with the same amino-acid sequence, were compared to determine the relative quantitation of glycoforms at each specific N-linked glycan site.\n\nModel construction\nStructural models of N-linked glycan presentation on SARS, MERS and HKU1 S were created using electron microscopy structures (PDB ID 5X58, 5X59, and 5I08, respectively)9,11, along with complex-, hybrid-, and oligomannose-type N-linked glycans (PDB ID 4BYH, 4B7I, and 2WAH). The most dominant glycoform presented at each site was modelled on to the N-linked carbohydrate attachment sites in Coot68.\n\nMolecular evolution analysis\nPublicly available sequences encoding full-length GPC spike gene for SARS-CoV (3765 bp) were downloaded from GenBank and manually aligned. For MERS-CoV, we leveraged the whole genome alignment collated by Dudas et al.69. Specifically, the alignment corresponding to the spike gene was extracted (4059 bp), excluding sequences isolated from humans. Final alignments for SARS- and MERS-CoV corresponded to 70 and 100 sequences, respectively.\nFor the dN/dS analysis, we first estimated Bayesian molecular clock phylogenies for SARS- and MERS-CoV independently using BEAST v 1.8.470. For both viruses, we assumed an uncorrelated log-normal distributed molecular clock71, Bayesian Skyline coalescent prior72 and a codon-structured substitution model73. Multiple independent MCMC runs of 10–20 million steps were executed to ensure that stationarity and convergence had been achieved. Empirical distributions of time-scaled phylogenies were obtained by combining (after the removal of burnin) the posterior tree distributions from the separate runs, which were subsequently used to estimate dN/dS ratios using the renaissance counting approach74,75 implemented in BEAST v 1.8.4. We also estimated per-site amino-acid diversity, which was calculated as the average number of amino-acid difference between two sequences at an amino-acid position in all possible pairs in the sequence alignment.\n\nCryo-EM data analysis and visualization\nSingle-particle cryo-EM data analysis of BG505 SOSIP.664 in complex with RM20A3 Fab was reproduced directly from Berndsen et al.51. Data for the SARS-CoV S 2P ectodomain was previously published52 and the final particle stack and alignment parameters from the published reconstruction were used for 3D variability analysis in the SPARX software package76,77. All metadata for these reconstructions along with raw data images and FSC resolution curves can be found in the original publications. In summary, both datasets were acquired on a FEI Titan Krios (Thermo Fisher) operating at 300 KeV equipped with a K2 Summit Direct Electron Detector (Gatan). Movie micrographs were aligned and dose weighted with MotionCor278 and CTF estimation was performed with Gctf79. Single-particle data processing was performed using CryoSparc v.280 and Relion v.381. Maps were low-pass filtered using a Gaussian kernel and visualized in UCSF chimera82. A detailed description of the auto-thresholding method used to set the isosurface value for visualisation of low-pass filtered maps can be found in Berndsen et al.51.\n\nClustering analysis of viral glycan shields\nSolvent-accessible residues and interactions between N-linked glycans and amino-acid residues were calculated using Proteins, Interfaces, Structures and Assemblies (PISA) European Bioinformatics Institute (EBI)83. Glycan shield density was calculated by the number of amino-acid residues interacting with glycans divided by the total number of solvent-accessible amino-acid residues.\n\nReporting summary\nFurther information on research design is available in the Nature Research Reporting Summary linked to this 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