PMC:7443692 / 9604-35543 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7443692","sourcedb":"PMC","sourceid":"7443692","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7443692","text":"Results\n\nExpression, Purification, and Characterization of SARS-CoV-2 Spike Glycoprotein Trimer and Soluble Human ACE2\nA trimer-stabilized, soluble variant of the SARS-CoV-2 S that contains 22 canonical N-linked glycosylation sequons per protomer and a soluble version of human ACE2 that contains six, lacking the most C-terminal seventh, canonical N-linked glycosylation sequons (Figure 1 A) were purified from the media of transfected HEK293 cells, and the quaternary structure confirmed by negative EM staining for the S trimer (Figure 1B) and purity examined by SDS-PAGE Coomassie G-250 stained gels for both (Figure 1C). In addition, proteolytic digestions followed by proteomic analyses confirmed that the proteins were highly purified (Table S12). Finally, the N terminus of both the mature S and the soluble mature ACE2 were empirically determined via proteolytic digestions and liquid chromatography-tandem mass spectrometry (LC-MS/MS) analyses. These results confirmed that both the secreted, mature forms of S protein and ACE2 begin with an N-terminal glutamine that has undergone condensation to form pyroglutamine at residues 14 and 18, respectively (Figures 1D and S1). The N-terminal peptide observed for S also contains a glycan at Asn-0017 (Figure 1D), and mass spectrometry analysis of non-reducing proteolytic digestions confirmed that Cys-0015 of S is in a disulfide linkage with Cys-0136 (Figure S2; Table S2). Given that SignalP (Almagro Armenteros et al., 2019) predicts signal sequence cleavage between Cys-0015 and Val-0016 but we observed cleavage between Ser-0013 and Gln-0014, we examined the possibility that an in-frame upstream methionine to the proposed start methionine (Figure 1A) might be used to initiate translation (Figure S3). If one examines the predicted signal sequence cleavage using the in-frame Met that is encoded nine amino acids upstream, SignalP now predicts cleavage between the Ser and Gln that we observed in our studies (Figure S3). To examine whether this impacted S expression, we expressed constructs that contained or did not contain the upstream 27 nucleotides in a pseudovirus (VSV) system expressing SARS-CoV-2 S (Figure S4) and in our HEK293 system (data not shown). Both expression systems produced a similar amount of S regardless of which expression construct was utilized (Figure S4). Thus, while the translation initiation start site has still not been fully defined, allowing for earlier translation in expression construct design did not have a significant impact on the generation of S.\nFigure 1 Expression and Characterization of SARS-CoV-2 Spike Glycoprotein Trimer Immunogen and Soluble Human ACE2\n(A) Sequences of SARS-CoV-2 S immunogen and soluble human ACE2. The N-terminal pyroglutamines for both mature protein monomers are bolded, underlined, and shown in green. The canonical N-linked glycosylation sequons are bolded, underlined, and shown in red.\n(B and C) Negative stain electron microscopy of the purified trimer (B) and Coomassie G-250-stained reducing SDS-PAGE gels (C) confirmed purity of the SARS-CoV-2 S protein trimer and of the soluble human ACE2. MWM, molecular weight markers.\n(D) A representative Step-HCD fragmentation spectrum from mass-spectrometry analysis of a tryptic digest of S annotated manually based on search results from pGlyco 2.2. This spectrum defines the N terminus of the mature protein monomer as (pyro-)glutamine 0014. A representative N-glycan consistent with this annotation and our glycomics data (Figure 2) is overlaid by using the Symbol Nomenclature For Glycans (SNFG) code. This complex glycan occurs at N0017. Note, that as expected, the cysteine is carbamidomethylated, and the mass accuracy of the assigned peptide is 0.98 ppm. On the sequence of the N-terminal peptide and in the spectrum, the assigned b (blue) and y (red) ions are shown. In the spectrum, purple highlights glycan oxonium ions and green marks intact peptide fragment ions with various partial glycan sequences still attached. Note that the green-labeled ions allow for limited topology to be extracted including defining that the fucose is on the core and not the antennae of the glycopeptide.\n\nGlycomics-Informed Glycoproteomics Reveals Site-Specific Microheterogeneity of SARS-CoV-2 S Glycosylation\nWe utilized multiple approaches to examine glycosylation of the SARS-CoV-2 S trimer. First, the portfolio of glycans linked to SARS-CoV-2 S trimer immunogen was analyzed after their release from the polypeptide backbone. N-glycans were released from protein by treatment with PNGase F- and O-glycans were subsequently released by beta-elimination. After permethylation to enhance detection sensitivity and structural characterization, released glycans were analyzed by multi-stage mass spectrometry (MSn) (Aoki et al., 2007; Aoki et al., 2008). Mass spectra were processed by GRITS Toolbox, and the resulting annotations were validated manually (Weatherly et al., 2019). Glycan assignments were grouped by type and by additional structural features for relative quantification of profile characteristics (Figure 2 A; Table S3). This analysis quantified 49 N-glycans and revealed that 55% of the total glycan abundance was of the complex type, 17% was of the hybrid type, and 28% was high mannose. Among the complex and hybrid N-glycans, we observed a high degree of core fucosylation and significant abundance of bisected and LacDiNAc structures. We also observed sulfated N-linked glycans by using negative mode MSn analyses (Table S13), although signal intensity was too low in positive ion mode (at least 10-fold lower than any of the non-sulfated glycans) for accurate quantification. In addition, we detected 15 O-glycans released from the S trimer (Figure S5; Table S4).\nFigure 2 Glycomics-Informed Glycoproteomics Reveals Substantial Site-Specific Microheterogeneity of N-linked Glycosylation on SARS-CoV-2 S\n(A) Glycans released from SARS-CoV-2 S protein trimer immunogen were permethylated and analyzed by MSn. Structures were assigned and grouped by type and structural features, and prevalence was determined based on ion current. The pie chart shows basic division by broad N-glycan type. The bar graph provides additional detail about the glycans detected. The most abundant structure with a unique categorization by glycomics for each N-glycan type in the pie chart, or above each feature category in the bar graph, is indicated.\n(B–E) Glycopeptides were prepared from SARS-CoV-2 S protein trimer immunogen by using multiple combinations of proteases, analyzed by LC-MSn, and the resulting data were searched by using several different software packages. Four representative sites of N-linked glycosylation with specific features of interest were chosen and are presented here. N0074 (B) and N0149 (C) are shown that occur in variable insert regions of S compared to SARS-CoV and other related coronaviruses, and there are emerging variants of SARS-CoV-2 that disrupt these two sites of glycosylation in S. N0234 (D) contains the most high-mannose N-linked glycans. N0801 (D) is an example of glycosylation in the S2 region of the immunogen and displays a high degree of hybrid glycosylation compared to other sites. The abundance of each composition is graphed in terms of assigned spectral counts. Representative glycans (as determined by glycomics analysis) for several abundant compositions are shown in SNFG format. The abbreviations used here and throughout the manuscript are as follows: N, HexNAc; H, hexose; F, fucose; A, Neu5Ac; S, sulfation. Note that the graphs for the other 18 sites and other graphs grouping the microheterogeneity observed by other properties are presented in Supplemental Information.\nTo determine occupancy of N-linked glycans at each site, we employed a sequential deglycoslyation approach by using Endoglycosidase H and PNGase F in the presence of 18O-H2O after tryptic digestion of S (Wang et al., 2020; Yu et al., 2018). After LC-MS/MS analyses, the resulting data confirmed that 19 of the canonical sequons had occupancies greater than 95% (Table S5). One canonical sequence, N0149, had insufficient spectral counts for quantification by this method, but subsequent analyses described below suggested high occupancy. The two most C-terminal N-linked sites, N1173 and N1194, had reduced occupancy, 52% and 82% respectively. Reduced occupancy at these sites could reflect hindered en bloc transfer by the oligosaccharyltransferase (OST) due to primary amino acid sequences at or near the N-linked sequon. Alternatively, this could reflect these two sites being post-translationally modified after release of the protein by the ribosome by a less efficient STT3B-containing OST, either due to activity or initial folding of the polypeptide, as opposed to co-translationally modified by the STT3A-containing OST (Ruiz-Canada et al., 2009). None of the non-canonical sequons (three N-X-C sites and four N-G-L/I/V sites; Zielinska et al., 2010) showed significant occupancy (\u003e5%), except for N0501, which showed moderate (19%) conversion to 18O-Asp that could be due to deamidation that is facilitated by glycine at the +1 position (Table S5) (Palmisano et al., 2012). Further analysis of this site (see below) by direct glycopeptide analyses allowed us to determine that N0501 undergoes deamidation but is not glycosylated. Thus, all, and only the, 22 canonical sequences for N-linked glycosylation (N-X-S/T) are utilized, with only N1173 and N1194 demonstrating occupancies below 95%.\nNext, we applied three different proteolytic digestion strategies to the SARS-CoV-2 S immunogen to maximize glycopeptide coverage by subsequent LC-MS/MS analyses. Extended gradient nanoflow reverse-phase LC-MS/MS was carried out on a ThermoFisher Lumos Tribrid instrument using Step-HCD fragmentation on each of the samples (see STAR Methods for details, as well as Duan et al., 2018; Escolano et al., 2019; Wang et al., 2020; Yu et al., 2018; Zhou et al., 2017). After data analyses using pGlyco 2.2.2 (Liu et al., 2017), Byonic (Bern et al., 2012), and manual validation of glycan compositions against our released glycomics findings (Figure 2A; Tables S3 and S13), we were able to determine the microheterogeneity at each of the 22 canonical sites (Figures 2B–2E; Table S6). Notably, none of the non-canonical consensus sequences, including N0501, displayed any quantifiable glycans. The N-glycosites N0074 (Figure 2B) and N0149 (Figure 2C) are highly processed and display a typical mammalian N-glycan profile. N0149 is, however, modified with several hybrid N-glycan structures, whereas N0074 is not. N0234 (Figure 2D) and N0801 (Figure 2E) have N-glycan profiles more similar to those found on other viruses such as HIV (Watanabe et al., 2019) that are dominated by high-mannose structures. N0234 (Figure 2D) displays an abundance of Man7-Man9 high-mannose structures, suggesting stalled processing by early-acting ER and cis-Golgi mannosidases. In contrast, N0801 (Figure 2E) is processed more efficiently to Man5 high-mannose and hybrid structures, suggesting that access to the glycan at this site by MGAT1 and α-Mannosidase II is hindered. In general, for all 22 sites (Figures 2B–2E; Table S6), we observed underprocessing of complex glycan antennae (i.e., under-galactosylation and under-sialylation) and a high degree of core fucosylation in agreement with released glycan analyses (Figure 2A; Table S3). We also observed a small percent of sulfated N-linked glycans at several sites (Tables S6 and S8). Based on the assignments and the spectral counts for each topology, we were able to determine the percent of total N-linked glycan types (high-mannose, hybrid, or complex) present at each site (Figure 3 ; Table S7). Notably, three of the sites (N0234, N0709, and N0717) displayed more than 50% high-mannose glycans, whereas 11 other sites (N0017, N0074, N0149, N0165, N0282, N0331, N0657, N1134, N1158, N1173, and N1194) were more than 90% complex when occupied. The other eight sites were distributed between these two extremes. Notably, only one site (N0717 at 45%), which also had greater than 50% high mannose (55%), had greater than 33% hybrid structures. To further evaluate the heterogeneity, we grouped all the topologies into the 20 classes recently described by the Crispin laboratory, adding two categories (sulfated and unoccupied) that we refer to here as the Oxford classification (Table S8) (Watanabe et al., 2020a). Among other features observed, this classification allowed us to observe that although most sites with high-mannose structures were dominated by the Man5GlcNAc2 structure, N0234 and N0717 were dominated by the higher Man structures of Man8GlcNAc2 and Man7GlcNAc2, respectively (Figure S7; Table S8). Limited processing at N0234 is in agreement with a recent report suggesting that high-mannose structures at this site help to stabilize the receptor-binding domain of S (www.biorxiv.org/content/10.1101/2020.06.11.146522v1). Furthermore, applying the Oxford classifications to our dataset clearly demonstrates that the three most C-terminal sites (N1158, N1173, and N1194), dominated by complex-type glycans, were more often further processed (i.e., multiple antennae) and elaborated (i.e., galactosylation and sialylation) than other sites (Table S8).\nFigure 3 SARS-CoV-2 S Immunogen N-glycan Sites Are Predominantly Modified by Complex N-glycans\nN-glycan topologies were assigned to all 22 sites of the S protomer and the spectral counts for each of the three types of N-glycans (high-mannose, hybrid, and complex), as well as the unoccupied peptide spectral match counts at each site, were summed and visualized as pie charts. Note that only N1173 and N1194 show an appreciable amount of the unoccupied amino acid.\nWe also analyzed our generated mass spectrometry data for the presence of O-linked glycans based on our glycomic findings (Figure S5; Table S4) and a recent manuscript suggesting significant levels of O-glycosylation of S1 and S2 when expressed independently (Shajahan et al., 2020). We were able to confirm sites of O-glycan modification with microheterogeneity observed for the vast majority of these sites (Table S9). However, occupancy at each site, determined by spectral counts, was observed to be very low (below 4%), except for Thr0323, which had a modestly higher but still low 11% occupancy (Figure S6; Table S10).\n\n3D Structural Modeling of Glycosylated SARS-CoV-2 Trimer Immunogen Enables Predictions of Epitope Accessibility and Other Key Features\nA 3D structure of the S trimer was generated by using a homology model of the S trimer described previously (based on PDB: 6VSB; Wrapp et al., 2020). Onto this 3D structure, we installed explicitly defined glycans at each glycosylated sequon based on one of three separate sets of criteria, thereby generating three different glycoform models for comparison that we denote as “Abundance,” “Oxford Class,” and “Processed” models (STAR Methods; Table S1). These criteria were chosen in order to generate glycoform models that represent reasonable expectations for glycosylation microheterogeneity and integrate cross-validating glycomic and glycoproteomic characterization of S and ACE2.\nThe three glycoform models were subjected to multiple all-atom MD simulations with explicit water. Information from analyses of these structures is presented in Figure 4 A along with the sequence of the SARS-CoV-2 S protomer. We also determined variants in S that are emerging in the virus that have been sequenced to date (Table S11). The inter-residue distances were measured between the most α-carbon-distal atoms of the N-glycan sites and Spike glycoprotein population variant sites in 3D space (Figure 4B). Notable from this analysis, there are several variants that don’t ablate the N-linked sequon but are sufficiently close in 3D space to N-glycosites, such as D138H, H655Y, S939F, and L1203F, to warrant further investigation.\nFigure 4 3D Structural Modeling of Glycosylated SARS-CoV-2 Spike Trimer Immunogen Reveals Predictions for Antigen Accessibility and Other Key Features\nResults from glycomics and glycoproteomics experiments were combined with results from bioinformatics analyses and used to model several versions of glycosylated SARS-CoV-2 S trimer immunogen.\n(A) Sequence of the SARS-CoV-2 S immunogen displaying computed antigen accessibility and other information. Antigen accessibility is indicated by red shading across the amino acid sequence.\n(B) Emerging variants confirmed by independent sequencing experiments were analyzed based on the 3D structure of SARS-CoV-2 S to generate a proximity chart to the determined N-linked glycosylation sites.\n(C) SARS-CoV-2 S trimer immunogen model from MD simulation displaying abundance glycoforms and antigen accessibility shaded in red for most accessible, white for partial, and black for inaccessible (see Video S1).\n(D) SARS-CoV-2 S trimer immunogen model from MD simulation displaying Oxford Class glycoforms and sequence variants. Asterisk indicates not visible, whereas the box represents three amino acid variants that are clustered together in 3D space.\n(E) SARS-CoV-2 S trimer immunogen model from MD simulation displaying processed glycoforms plus shading of Thr-323 that has O-glycosylation at low stoichiometry in yellow.\nThe percentage of simulation time that each S protein residue is accessible to a probe that approximates the size of an antibody variable domain was calculated for a model of the S trimer by using the Abundance glycoforms (Table S1) (Ferreira et al., 2018). The predicted antibody accessibility is visualized across the sequence, as well as mapped onto the 3D surface, via color shading (Figures 4A and 4C; Table S13; Video S1). Additionally, the Oxford Class glycoforms model (Table S1), which is arguably the most encompassing means for representing glycan microheterogeneity because it captures abundant structural topologies (Table S8), is shown with the sequence variant information (Figure 4D; Table S11). A substantial number of these variants occur (directly by comparison to Figure 4A or visually by comparison to Figure 4C) in regions of high calculated epitope accessibility (e.g., N74K, T76I, R78M, D138H, H146Y, S151I, D253G, V483A, etc.; Table S14), suggesting potential selective pressure to avoid host immune response. Also, it is interesting to note that three of the emerging variants would eliminate N-linked sequons in S; N74K and T76I would eliminate N-glycosylation of N74 (found in the insert variable region 1 of CoV-2 S compared to CoV-1 S), and S151I eliminates N-glycosylation of N149 (found in the insert variable region 2) (Figures 4A and S7; Table S11). Lastly, the SARS-CoV-2 S Processed glycoform model is shown (Table S1), along with marking amino acid T0323 that has a modest (11% occupancy, Figure S6; Table S10) amount of O-glycosylation to represent the most heavily glycosylated form of S (Figure 4E).\nVideo S1. Glycosylated S Antigen Accessibility, Related to Figure 4C\n\nGlycomics-Informed Glycoproteomics Reveals Complex N-linked Glycosylation of ACE2\nWe also analyzed ACE2 glycosylation utilizing the same glycomic and glycoproteomic approaches described for S protein. Glycomic analyses of released N-linked glycans (Figure 5 A; Table S3) revealed that the majority of glycans on ACE2 are complex with limited high-mannose and hybrid glycans, and we were unable to detect sulfated N-linked glycans. Glycoproteomic analyses revealed that occupancy was high (\u003e 75%) at all six sites, and significant microheterogeneity dominated by complex N-glycans was observed for each site (Figures 5B–5G; Tables S5–S8). We also observed, consistent with the O-glycomics (Figure S5; Table S4), that Ser 155 and several S/T residues at the C terminus of ACE2 outside of the peptidase domain were O-glycosylated, but stoichiometry was extremely low (less than 2%; Tables S9 and S10).\nFigure 5 Glycomics-Informed Glycoproteomics of Soluble Human ACE2 Reveals High Occupancy, Complex N-linked Glycosylation\n(A) Glycans released from soluble, purified ACE2 were permethylated and analyzed by MSn. Structures were assigned, grouped by type and structural features, and prevalence was determined based on ion current. The pie chart shows basic division by broad N-glycan type. The bar graph provides additional detail about the glycans detected. The most abundant structure with a unique categorization by glycomics for each N-glycan type in the pie chart, or above each feature category in the bar graph, is indicated.\n(B–G) Glycopeptides were prepared from soluble human ACE2 by using multiple combinations of proteases, analyzed by LC-MSn, and the resulting data were searched by using several different software packages. All six sites of N-linked glycosylation are presented here. Displayed in the bar graphs are the individual compositions observed graphed in terms of assigned spectral counts. Representative glycans (as determined by glycomics analysis) for several abundant compositions are shown in SNFG format. The pie chart (analogous to Figure 3 for SARS-CoV-2 S) for each site is displayed in the upper corner of each panel.\n(B) N053.\n(C) N090.\n(D) N103.\n(E) N322.\n(F) N432.\n(G) N546, a site that does not exist in three in 10,000 people.\n\n3D Structural Modeling of Glycosylated, Soluble, ACE2-Highlighting Glycosylation and Variants\nWe integrated our glycomics, glycoproteomics, and population variant analyses results with a 3D model of Ace 2 (based on PDB: 6M0J (Lan et al., 2020; see STAR Methods for details) to generate two versions of the soluble glycosylated ACE2 for visualization and MD simulations. We visualized the ACE2 glycoprotein with the Abundance glycoform model simulated at each site as well as highlighting the naturally occurring variants observed in the human population (Figure 6 A; Video S2; Table S11). Note, that the Abundance glycoform model and the Oxford Class glycoform model for ACE2 are identical (Tables S1 and S8). Notably, one site of N-linked glycosylation (N546) is predicted to not be present in three out of 10,000 humans based on naturally occurring variation in the human population (Table S11). We also modeled ACE2 using the Processed glycoform model (Figure 6B). In both models, the interaction domain with S is defined (Figures 6A and 6B; Video S2).\nFigure 6 3D Structural Modeling of Glycosylated Soluble Human ACE2\nResults from glycomics and glycoproteomics experiments were combined with results from bioinformatics analyses and used to model several versions of glycosylated soluble human ACE2.\n(A) Soluble human ACE2 model from MD simulations displaying abundance glycoforms, interaction surface with S, and sequence variants. N546 variant is boxed that would remove N-linked glycosylation at that site (see Video S2).\n(B) Soluble human ACE2 model from MD simulations displaying processed glycoforms and interaction surface with S.\nVideo S2. Glycosylated ACE2 with Variants, Related to Figure 6A\n\nMD Simulation of the Glycosylated Trimer Spike of SARS-CoV-2 in Complex with Glycosylated, Soluble, Human Ace 2 Reveals Protein and Glycan Interactions\nMD simulations were performed to examine the co-complex (generated from a crystal structure of the ACE2-RBD co-complex, PDB: 6M0J; Lan et al., 2020) of glycosylated S with glycosylated ACE2 with the three different glycoforms models (Abundance, Oxford Class, and Processed; Table S1; Videos S5, S6, and S7). Information from these analyses is laid out along the primary structure (sequence) of the SARS-CoV-2 S protomer and ACE2 highlighting regions of glycan-protein interaction observed in the MD simulations (Table S14; Videos S5, S6, and S7). Interestingly, two glycans on ACE2 (at N090 and N322), which are highlighted in Figure 7 A and shown in a more close-up view in Figure 7B, are predicted to form interactions with the S protein (Table S15). The N322 glycan interaction with the S trimer is outside of the receptor-binding domain, and the interaction is observed across multiple simulations and throughout each simulation (Figures 7A and 7B; Video S5, S6, and S7). The ACE2 glycan at N090 is close enough to the S trimer surface to repeatedly form interactions; however, the glycan arms interact with multiple regions of the surface over the course of the simulations, reflecting the relatively high degree of glycan dynamics (Figures 7A and 7B; Video S3). Inter-molecule glycan-glycan interactions are also observed repeatedly between the glycan at N546 of ACE2 and those in the S protein at residues N0074 and N0165 (Figure 7D; Table S16). Finally, a full view of the ACE2-S complex with Oxford class glycoforms on ACE2 illustrates the extensive glycosylation at the interface of the complex (Figure 7C; Video S4).\nFigure 7 Interactions of Glycosylated Soluble Human ACE2 and Glycosylated SARS-CoV-2 S Trimer Immunogen Revealed By 3D-Structural Modeling and MD Simulations\n(A) MD simulation of glycosylated soluble human ACE2 and glycosylated SARS-CoV-2 S trimer immunogen interaction (see Videos S5, S6, and S7). ACE2 (top) is colored red with glycans in pink, whereas S is colored white with glycans in dark gray. Highlighted are ACE2 glycans that interact with S that are magnified to the right.\n(B) Magnification of ACE2-S interface highlighting ACE2 glycan interactions by using 3D-SNFG icons (Thieker et al., 2016) with S protein (pink) as well as ACE2-S glycan-glycan interactions.\n(C) Magnification of dynamics trajectory of glycans at the interface of soluble human ACE2 and S (see Videos S3 and S4).\nVideo S3. Interface of ACE2-S Complex, Related to Figure 7C\nVideo S4. The Glycosylated ACE2-S Complex, Related to Figure 7C\nVideo S5. Abundance Glycoforms on ACE2-S Complex, Related to Figure 7A\nVideo S6. Oxford Class Glycoforms on ACE2-S Complex, Related to Figure 7A\nVideo S7. 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