PMC:7443692 / 1853-9602 JSONTXT

{"target":"http://pubannotation.org/docs/sourcedb/PMC/sourceid/7443692","sourcedb":"PMC","sourceid":"7443692","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7443692","text":"Introduction\nThe SARS-CoV-2 coronavirus, a positive-sense single-stranded RNA virus, is responsible for the severe acute respiratory syndrome referred to as COVID-19 that was first reported in China in December 2019 (Zhou et al., 2020). In approximately six months, this betacoronavirus has spread globally, with more than 14 million people testing positive worldwide resulting in greater than 600,000 deaths as of July 20, 2020 (https://coronavirus.jhu.edu/map.html). The SARS-CoV-2 coronavirus is highly similar (nearly 80% identical at the genomic level) to SARS-CoV-1, which was responsible for the severe acute respiratory syndrome outbreak that began in 2002 (Lu et al., 2020; Zhong et al., 2003). Furthermore, human SARS-CoV-2 at the whole-genome level is \u003e95% identical to a bat coronavirus (RaTG13), the natural reservoir host for multiple coronaviruses (Xia, 2020; Zhang et al., 2020; Zhou et al., 2020). Given the rapid appearance and spread of this virus, there is no current validated vaccine or SARS-CoV-2-specific targeting therapy that is clinically approved, although statins, heparin, and steroids look promising for lowering fatality rates, and antivirals likely reduce the duration of symptomatic disease presentation (Alijotas-Reig et al., 2020; Beigel et al., 2020; Beun et al., 2020; Dashti-Khavidaki and Khalili, 2020; Fedson et al., 2020; Shi et al., 2020; Tang et al., 2020).\nSARS-CoV-2, like SARS-CoV-1, utilizes the host angiotensin-converting enzyme 2 (ACE2) for binding and entry into host cells (Hoffmann et al., 2020; Li et al., 2003). Like many viruses, SARS-CoV-2 utilizes a Spike glycoprotein trimer for recognition and binding to the host cell entry receptor and for membrane fusion (Watanabe et al., 2019). Given the importance of viral Spike proteins for targeting and entry into host cells along with their location on the viral surface, Spike proteins are often used as immunogens for vaccines to generate neutralizing antibodies and frequently targeted for inhibition by small molecules that might block host receptor binding and/or membrane fusion (Li, 2016; Watanabe et al., 2019). In similar fashion, wild-type or catalytically impaired ACE2 has also been investigated as a potential therapeutic biologic that might interfere with the infection cycle of ACE2-targeting coronaviruses (Lei et al., 2020; Monteil et al., 2020). Thus, a detailed understanding of SARS-CoV-2 Spike binding to ACE2 is critical for elucidating mechanisms of viral binding and entry, as well as for undertaking the rational design of effective therapeutics.\nThe SARS-CoV-2 Spike glycoprotein consists of two subunits, a receptor binding subunit (S1) and a membrane fusion subunit (S2) (Lu et al., 2020; Zhou et al., 2020). The Spike glycoprotein assembles into stable homotrimers that together possess 66 canonical sequons for N-linked glycosylation (N-X-S/T, where X is any amino acid except P) as well as a number of potential O-linked glycosylation sites (Watanabe et al., 2020a; Watanabe et al., 2020b). Interestingly, coronaviruses virions bud into the lumen of the endoplasmic reticulum-Golgi intermediate compartment, ERGIC, raising unanswered questions regarding the precise mechanisms by which viral surface glycoproteins are processed as they traverse the secretory pathway (Stertz et al., 2007; Ujike and Taguchi, 2015). Although this and similar studies (Shajahan et al., 2020; Watanabe et al., 2020a) analyze recombinant proteins, a previous study on SARS-CoV-1 suggested that glycosylation of the Spike can be impacted by this intracellular budding, and this remains to be investigated in SARS-CoV-2 (Ritchie et al., 2010). Nonetheless, it has been proposed that this virus, and others, acquires a glycan coat sufficient and similar enough to endogenous host protein glycosylation that it serves as a glycan shield, facilitating immune evasion by masking non-self viral peptides with self-glycans (Stertz et al., 2007; Ujike and Taguchi, 2015; Watanabe et al., 2020b; Watanabe et al., 2019). In parallel with their potential masking functions, glycan-dependent epitopes can elicit specific, even neutralizing, antibody responses, as has been described for HIV-1 (Duan et al., 2018; Escolano et al., 2019; Pinto et al., 2020; Seabright et al., 2020; Watanabe et al., 2019; Yu et al., 2018; https://www.biorxiv.org/content/10.1101/2020.06.30.178897v1). Thus, understanding the glycosylation of the viral Spike trimer is fundamental for the development of efficacious vaccines, neutralizing antibodies, and therapeutic inhibitors of infection.\nACE2 is an integral membrane metalloproteinase that regulates the renin-angiotensin system (Tikellis et al., 2011). Both SARS-CoV-1 and SARS-CoV-2 have co-opted ACE2 to function as the receptor by which these viruses attach and fuse with host cells (Hoffmann et al., 2020; Li et al., 2003). ACE2 is cleavable by ADAM proteases at the cell surface (Lambert et al., 2005), resulting in the shedding of a soluble ectodomain that can be detected in apical secretions of various epithelial layers (gastric, airway, etc.) and in serum (Epelman et al., 2009). The N-terminal extracellular domain of ACE2 contains six canonical sequons for N-linked glycosylation and several potential O-linked sites. Several nonsynonymous single-nucleotide polymorphisms (SNPs) in the ACE2 gene have been identified in the human population and could potentially alter ACE2 glycosylation and/or affinity of the receptor for the viral Spike protein (Li et al., 2005). Given that glycosylation can affect the half-life of circulating glycoproteins in addition to modulating the affinity of their interactions with receptors and immune/inflammatory signaling pathways (Marth and Grewal, 2008; Varki, 2017), understanding the impact of glycosylation of ACE2 with respect to its binding of SARS-CoV-2 Spike glycoprotein is of high importance. The proposed use of soluble extracellular domains of ACE2 as decoy, competitive inhibitors for SARS-CoV-2 infection emphasizes the critical need for understanding the glycosylation profile of ACE2 so that optimally active biologics can be produced (Lei et al., 2020; Monteil et al., 2020).\nTo accomplish the task of characterizing site-specific glycosylation of the trimer Spike of SARS-CoV-2 and the host receptor ACE2, we began by expressing and purifying a stabilized, soluble trimer Spike glycoprotein mimetic immunogen (that we define here and forward as S, [Yu et al., 2020]) and a soluble version of the ACE2 glycoprotein from a human cell line. We utilized multiple mass-spectrometry-based approaches, including glycomic and glycoproteomic approaches, to determine occupancy and site-specific heterogeneity of N-linked glycans. Occupancy (i.e., the percent of any given residue being modified by a glycan) is an important consideration when developing neutralizing antibodies against a glycan-dependent epitope. We also identified sites of O-linked glycosylation and the heterogeneity of the O-linked glycans on S and ACE2. We leveraged this rich dataset, along with existing 3D-structures of both glycoproteins, to generate static and molecular dynamics (MD) models of S alone, and in complex with the glycosylated, soluble ACE2 receptor. By combining bioinformatics characterization of viral evolution and variants of S and ACE2 with MD simulations of the glycosylated S-ACE2 interaction, we identified important roles for glycans in multiple processes, including receptor-viral binding and glycan shielding of S. Our rich characterization of the recombinant, glycosylated S trimer mimetic immunogen of SARS-CoV-2 in complex with the soluble human ACE2 receptor provides a detailed platform for guiding rational vaccine, antibody, and inhibitor 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