PMC:7443692 / 35545-44713 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":"Discussion\nWe have defined the glycomics-informed, site-specific microheterogeneity of 22 sites of N-linked glycosylation per monomer on a SARS-CoV-2 trimer and the six sites of N-linked glycosylation on a soluble version of its human ACE2 receptor by using a combination of mass spectrometry approaches coupled with evolutionary and variant sequence analyses to provide a detailed understanding of the glycosylation states of these glycoproteins (Figures 1, 2, 3, 4, 5, and 6). Our results suggest essential roles for glycosylation in mediating receptor binding, antigenic shielding, and potentially the evolution/divergence of these glycoproteins.\nThe highly glycosylated SARS-CoV-2 Spike protein, unlike several other viral proteins including HIV-1 (Watanabe et al., 2019) but in agreement with another recent report (Watanabe et al., 2020a), presents significantly more processing of N-glycans toward complex glycosylation, suggesting that steric hindrance to processing enzymes is not a major factor at most sites (Figures 2 and 3). However, the N-glycans still provide considerable shielding of the peptide backbone (Figure 4). Our glycomics-guided glycoproteomic data are generally in strong agreement with the trimer immunogen data recently published by Crispin (Watanabe et al., 2020a), although we also observed sulfated N-linked glycans; were able to differentiate branching, bisected, and diLacNAc containing structures by glycomics; and observed less occupancy on the two most C-terminal N-linked sites by using a different approach. Our detection of sulfated N-linked glycans at multiple sites on S is in agreement with a recent manuscript re-analyzing the Crispin data (https://www.biorxiv.org/content/10.1101/2020.05.31.125302v1). Sulfated N-linked glycans could potentially play key roles in immune regulation and receptor binding as in other viruses (Wang et al., 2009). This result is especially significant in that sulfated N-glycans were not observed when we performed glycomics on ACE2. At each individual site, the glycans we observed on our immunogen appear to be slightly more processed, but the overlap between our analysis and the Crispin’s group results (Watanabe et al., 2020a) at each site in terms of major features are nearly superimposable. This agreement differs substantially when comparing our and Crispin’s data (Watanabe et al., 2020a) to that of the Azadi group (Shajahan et al., 2020), which analyzed S1 and S2 that had been expressed individually. When expressed as two separate polypeptides and not purified for trimers, several unoccupied sites of N-linked glycosylation were observed and processing at several sites was significantly different (Shajahan et al., 2020) than we and others (Watanabe et al., 2020a) observed. Although O-glycosylation has recently been reported for individually expressed S1 and S2 domains of the Spike glycoprotein (Shajahan et al., 2020), in trimeric form the level of O-glycosylation is extremely low, with the highest level of occupancy we observed being 11% at T0323 (Figure 4E). The low level of O-linked occupancy we observed is in agreement with the Crispin group’s analysis of a Spike Trimer immunogen (Watanabe et al., 2020a) but differs significantly from the Azadi group’s analyses of individually expressed S1 and S2 (Shajahan et al., 2020). Thus, the context in which the Spike protein is expressed and purified before analysis significantly alters the glycosylation of the protomer that is reminiscent of previous studies looking at expression of the HIV-1 envelope Spike (Behrens et al., 2017; Watanabe et al., 2019). The soluble ACE2 protein examined here contains six highly utilized sites of N-linked glycosylation dominated by complex type N-linked glycans (Figure 5). O-glycans were also present on this glycoprotein but at very low levels of occupancy at all sites (\u003c2%).\nOur glycomics-informed glycoproteomics allowed us to assign defined sets of glycans to specific glycosylation sites on 3D-structures of S and ACE2 glycoproteins based on experimental evidence (Figures 4 and 6). Similar to almost all glycoproteins, microheterogeneity is evident at most glycosylation sites of S and ACE2; each glycosylation site can be modified with one of several glycan structures, generating site-specific glycosylation portfolios. For modeling purposes, however, explicit structures must be placed at each glycosylation site. In order to capture the impact of microheterogeneity on S and ACE2 MD we chose to generate glycoforms for modeling that represented reasonable portfolios of glycan types. Using three glycoform models for S (Abundance, Oxford Class, and Processed) and two models for ACE2 (Abundance, which was equivalent to Oxford Class, and Processed), we generated three MD simulations of the co-complexes of these two glycoproteins (Figure 7; Videos S5, S6, and S7). The observed interactions over time allowed us to evaluate glycan-protein contacts between the two proteins and examine potential glycan-glycan interactions (Figure 7).\nWe observed glycan-mediated interactions between the S trimer and glycans at N090, N322, and N546 of ACE2. Thus, variations in glycan occupancy or processing at these sites could alter the affinity of the SARS-CoV-2–ACE2 interaction and modulate infectivity. It is well established that glycosylation states vary depending on tissue and cell type as well as in the case of humans, on age (Krištić et al., 2014), underlying disease (Pavić et al., 2018; Rudman et al., 2019), and ethnicity (Gebrehiwot et al., 2018). Thus, glycosylation portfolios could in part be responsible for tissue tropism and individual susceptibility to infection. The importance of glycosylation for S binding to ACE2 is even more emphatically demonstrated by the direct glycan-glycan interactions observed (Figure 7) between S glycans (at N0074 and N0165) and an ACE2 receptor glycan (at N546), adding an additional layer of complexity for interpreting the impact of glycosylation on individual susceptibility.\nSeveral emerging variants of the virus appear to be altering N-linked glycosylation occupancy by disrupting N-linked sequons. Interestingly, the two N-linked sequons in SARS-CoV-2 S directly impacted by variants, N0074 and N0149, are in divergent insert regions 1 and 2, respectively, of SARS-CoV-2 S in comparison with SARS-CoV-1 S (Figure 4A). The N0074, in particular, is one of the S glycans that interact directly with ACE2 glycan (at N546; Figure 7), suggesting that glycan-glycan interactions could contribute to the unique infectivity differences between SARS-CoV-2 and SARS-CoV-1. These sequon variants will also be important to examine in terms of glycan shielding that could influence immunogenicity and efficacy of neutralizing antibodies, as well as interactions with the host cell receptor ACE2. Naturally occurring amino acid-changing SNPs in the ACE2 gene generate a number of variants including one variant, with a frequency of three in 10,000 humans, that eliminates a site of N-linked glycosylation at N546 (Figure 6). Understanding the impact of ACE2 variants on glycosylation and more importantly on S binding, especially for N546S, which impacts the glycan-glycan interaction between S and ACE2 (Figure 7), should be prioritized in light of efforts to develop ACE2 as a potential decoy therapeutic. Intelligent manipulation of ACE2 glycosylation could lead to more potent biologics capable of acting as better competitive inhibitors of S binding.\nThe data presented here, and related similar recent findings (Casalino et al., 2020; Watanabe et al., 2020a; Wrobel et al., 2020), provide a framework to facilitate the production of immunogens, vaccines, antibodies, and inhibitors as well as additional information regarding mechanisms by which glycan microheterogeneity is achieved. However, considerable efforts still remain in order to fully understand the role of glycans in SARS-CoV-2 infection and pathogenicity. Although HEK-expressed S and ACE2 provide a useful window for understanding human glycosylation of these proteins, glycoproteomic characterization after expression in cell lines of more direct relevance to disease and target tissue is sorely needed. Although site occupancy could change depending on presentation and cell type (Struwe et al., 2018), processing of N-linked glycans will almost certainly be altered in a cell-type-dependent fashion. Thus, analyses of the Spike trimer extracted from pseudoviruses, virion-like particles, and ultimately from infectious SARS-CoV-2 virions harvested from airway cells or patients will provide the most accurate view of how trimer immunogens reflect the true glycosylation pattern of the virus. Detailed analyses of the impact of emerging variants in S and natural and designed-for-biologics variants of ACE2 on glycosylation and binding properties are important next steps for developing therapeutics. Finally, it will be important to monitor the slow evolution of the virus to determine if existing sites of glycosylation are lost or new sites emerge with selective pressure that might alter the efficacy of vaccines, neutralizing antibodies, and/or 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