PMC:7219429 / 10046-25140 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7219429","sourcedb":"PMC","sourceid":"7219429","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7219429","text":"3 Results\n\n3.1 Molecular mimicry between ATM and ganglioside GM1\nThe chemical structure of ATM is shown in Fig. 1 a. The molecule contains two sugar-like pyranyl rings, one with a nitrogen-containing group (N-pyr), the other with an acetyl group (Ac-pyr). The remaining part of the molecule is cyclic, so that its overall conformational flexibility, although significant, is restricted to a limited spatial volume of 2082 Å3 (Fig. 1b). Interestingly, this volume is almost the same as that of the saccharide part of ganglioside GM1 (2293 Å3, Fig. 1b), a lipid raft ganglioside that plays a critical role in the binding and endocytosis of respiratory viruses [26], including pathogenic human coronaviruses [27]. Beyond their similar spatial volume, the saccharide part of GM1 and ATM also share some analogous chemical features, including sugar rings and a solvent-accessible surface dotted with several CH and OH groups (Fig. 1b). This molecular similarity is further illustrated in Figure S1 where ATM is superimposed on the saccharide part of GM1.\nFig. 1 Structures of azithromycin (ATM) and SARS-CoV-2 spike protein trimer. (a) ATM, with both sugar-like pyranyl groups N-pyr and Ac-pyr indicated. The molecules are shown in chemical, tube and sphere rendering (carbon in green, nitrogen in blue, oxygen in red, hydrogen in white). (b) Molecular structure similarity between ATM and the saccharide part of ganglioside GM1. Both structures can adopt a globular shape the surface of which is covered with a patchwork of OH (arrows 1 and 2) and CH groups (arrow 3). The volume occupied by ATM and the saccharide part of GM1 can be estimated to be 2082 and 2293 Å3, respectively. (c) front and above views of the trimeric spike, each spike protein subunit with a distinct surface colour (cyan for chain A, yellow for chain B, purple for chain C). Atoms belonging to the ganglioside-binding domain of each subunit are visible underneath the slightly transparent surface. The ganglioside-binding domains, the NTD and the RBD are indicated.\nGiven that the SARS-CoV-2 spike protein displays a ganglioside-binding site at the tip of its NTD [10], the possibility that ATM, as a “ganglioside mimic”, could also bind to this site was considered. The structural features of the SARS-CoV-2 spike in the prefusion conformation [20] are shown in Fig. 1c. It consists of three interdigitated spike proteins that provide the virus its typical corona-like shape in electron microscopy images. In each subunit, the most distant part from the viral envelope is divided into two separate domains, the NTD and the RBD. The NTD has a flat surface available for ganglioside binding [10], and this process is independent from the ACE-2 receptor recognition, which occurs at the tip of the RBD [11,20]. When seen from above, the viral spike has a typical triangle shape, with a ganglioside-binding domain at each apex. Thus, the spike central area is devoted to ACE-2 binding, leaving three peripheric flat surface areas available for ganglioside attachment. Such dual ganglioside/receptor binding is commonly used by pathogenic viruses such as HIV-1 [28], [29], [30] and bacterial neurotoxins [16]. By combining the high affinity for a single protein receptor with multiple low affinity attachment sites, these pathogens have selected a very efficient pathway to gain entry into host cells.\n\n3.2 Characterization of an ATM binding site at the tip of SARS-CoV-2 spike protein\nWhen ATM molecules were merged with the SARS-CoV-2 spike protein, there was a very good fit for one particular pose at the tip of protein (Fig. 2 ). All other docking attempts on the NTD or the RBD of the spike protein were unsuccessful (Figure S2) as they did not satisfy the minimum cut-off values. Not surprisingly, their trajectories started destabilizing before 10 ns. In contrast, ATM #1 (coloured in yellow in Figure S2) remained bound to the spike protein throughout the simulation process (Fig. 3 ). Interestingly, a significant movement of the drug was observed from its docked pose to a stable MD pose (dock-to-MD transition), particularly during the first 10-ns of simulations (Figure S3). A stable complex association was then reached after 10 ns. Three amino acid residues, referred to as the “QFN triad”, exhibited significant conformational rearrangement during the binding process: Q-134, F-135 and N-137 (Fig. 3). The principal moves comprised a significant reorientation of the aromatic ring of F-135, from suboptimal stacking to stabilized T-shape CH-π interaction, and a concomitant retraction of the Q-134 side chain. Fluctuations during the 10 to 50 ns period did not affect the overall geometry of the complex, which converged to a mean energy of interaction of 92.4 ± 5.8 kJ.mol−1 as determined from triplicate MD simulations (Table S1). Schematically, the binding site is formed by two discontinuous regions of the protein, including the QFN triad with additional C-136, D-138, R-158 and S-161 residues (Fig. 4, Fig. 5 ). These seven amino acid residues accounted for almost 90% of the whole energy of interaction (Table S1 and Fig. 5).\nFig. 2 Molecular complex between the SARS-CoV-2 spike protein trimer and ATM. (a) Detailed view of ATM bound to the NTD tip of SARS-CoV-2 spike protein chain A, shown at two distinct magnifications and orientations (left and right panels). Note that the NTD tip displays a complementary landing surface for ATM (highlighted in red). The protein stretch 134-138, which contains the QFN triad, is highlighted in green. (b) The trimeric structure of the SARS-CoV-2 spike is represented in surface rendition with subunit (protein chain A, B and C) in cyan, yellow and purple, respectively. AMT (in red) is bound to the tip of the NTD domain of the A subunit (left panel). The ribbon structure of the cyan (chain A) subunit is shown in the right panel. (c) Above views of the spike-ATM complex. Note that the B and C subunits also display a fully accessible ATM binding site (red asterisk).\nFig. 3 Induced-fit conformational rearrangements during binding of ATM on the spike protein. (a) Docking of ATM on the spike protein (time = 0). ATM is in yellow spheres, and the protein segment 134-137 is in balls and sticks rendition. Three parts of the ATM molecule are marked with asterisks. The orientation of the side chains of residues 134-137 is shown under the complex. (b) ATM bound to the spike protein after MD simulations (time = 50 ns). Note that the complex has evolved according to a typical induced-fit mechanism. The asterisks on ATM help visualize its conformational changes. Reorientation of amino acid side chains is also clearly visible in the ATM-spike complex and in the isolated 134-137 fragment shown under the complex.\nFig. 4 Schematic of ATM interaction at the tip of the spike protein. Residues lining cavity under 3.5Å are shown. Hydrogen bonds and CH-π stacking interactions are indicated. Note that Q-134 (Gln-134) and S-161 (Ser-161) are linked by a hydrogen bond, which stabilizes the ATM-spike complex.\nFig. 5 Energy of interaction of spike protein-ATM and spike-GM1 complexes. Results are expressed by amino acid residue as mean ± SD of three distinct MD simulations (50 ns) with the same starting docking conditions. In the case of GM1, the simulations are done in presence of sphingomyelin and cholesterol to mimic a lipid raft plasma membrane domain. Each bar corresponds to a single amino acid residue, as indicated in the horizontal axis. Detailed values and statistics are shown in Table S1.\nThe complex was stabilized by hydrogen bonds, CH-π and van der Waals interactions distributed over the whole ATM molecule (Fig. 4).\n\n3.3 SARS-CoV-2 spike protein interactions with gangliosides in a lipid raft domain\nBased on recent in-silico data that led to the characterization of ganglioside-spike protein interactions [10], MD simulations were performed with GM1 gangliosides surrounded by typical raft lipids, i.e. sphingomyelin and cholesterol (Figs. 5 and 6 ). These new data confirmed and extended our previous results obtained with isolated gangliosides [10]. Indeed, cholesterol and sphingomyelin appeared to stabilize the typical chalice-shaped GM1 dimer, which serves as a landing platform for the SARS-CoV-2 spike protein (Fig. 6). Moreover, the histograms of Fig. 5 show that all amino acid residues of the spike protein that are involved in ATM binding, including the QFN triad, are also essential for GM1 binding in the lipid raft environment (Table S1 and Fig. 5). Taken together, these data indicate that the NTD of the viral glycoprotein may display a common ganglioside/ATM binding site, in agreement with our working hypothesis. Sequence alignments revealed that this common binding site, including the QFN triad, is totally conserved among clinical isolates of SARS-CoV-2 from various geographical origins worldwide (Fig. 7 ). It is also conserved in bat RaTG13, which further illustrates the close relationship between this bat coronavirus and the SARS-CoV-2 strains that are currently circulating the world. This region of the NTD should therefore be considered for SARS-CoV-2 vaccine strategies. However, the motif has a different sequence signature in other animal- and human-related SARS coronaviruses (Fig. 7), indicating a recent evolution that may be linked to the higher contagiousness of SARS-CoV-2 compared with other human coronaviruses.\nFig. 6 MD simulations of GM1-spike protein interaction in a lipid raft domain. Two GM1 gangliosides were merged with eight cholesterol (chol) and two sphingomyelin (SM) lipids. After initial docking, MD simulations were performed for 50 ns. Two distinct views of the complex are shown. Cholesterol and sphingomyelin stabilize a dimer of GM1 clamped by the NTD of the spike protein.\nFig. 7 Amino acid sequence alignments of the ganglioside/ATM binding domain of the SARS-CoV-2 spike protein. The first group of sequences includes clinical SARS-CoV-2 isolates from various geographical origins aligned with the reference sequence (6VSB_A, fragment 111-162). The QFN triad is highlighted in yellow. The second group of sequences includes human and animal viruses compared with SARS-CoV-2. Deletions are highlighted in green, amino acid changes are highlighted in blue, conserved residues of the QFN triad are highlighted in yellow. The degree of conservation observed in each column is symbolized by an asterisk (*) when the residue is fully conserved, a colon (:) for distinct residues with strongly similar properties (scoring \u003e 0.5 in the Gonnet PAM 250 matrix), and a period (.) for distinct residues with weakly similar properties (scoring ≤ 0.5 in the Gonnet PAM 250 matrix).\n\n3.4 Synergistic antiviral effects of ATM and CLQ-OH\nOverall, these molecular modelling studies are consistent with the notion that ATM might inhibit SARS-CoV-2 infection through direct binding to the virus spike and subsequent neutralization of the infection process, which requires spike protein recognition and attachment to gangliosides. This mechanism of action is illustrated in Fig. 8 . Comparing the models in Figs. 8a and 8b shows that both ATM and gangliosides bind to the same site of the spike protein, centred on the QFN triad. Thus, in the presence of ATM, the virus spike would not reach gangliosides on the host plasma membrane (Fig. 8c). To the best of our knowledge, it is the first time that such a mechanism of action is proposed to explain the antiviral effect of ATM.\nFig. 8 CLQ-OH/ATM combination therapy at the molecular level. (a) ATM bound to the SARS-CoV-2 spike protein trimer. (b) Ganglioside dimer (two symmetrically arranged GM1 molecules in a typical chalice-like shape, just like the one observed in lipid raft simulations) bound to SARS-CoV-2 spike protein trimer. Note that both ATM and gangliosides share the same binding region. (c) ATM prevents ganglioside binding to the SARS-CoV-2 spike protein trimer. CLQ-OH, once bound to gangliosides (blue and orange surfaces), also prevents any interaction with the viral spike. (d) 4 CLQ-OH molecules bound to a ganglioside dimer. Each GM1 molecule is blocked by two CLQ-OH molecules (blue and orange surfaces), which wrap around the saccharide part. (e) Detail of the 134-138 SARS-CoV-2 spike protein stretch bound to GM1. Note that the ganglioside interacts with Q-134 and F-135, but not with D-138. (f) Detail of the 134-138 SARS-CoV-2 spike protein stretch bound to ATM. In this case, the binding site includes D-138 in addition to Q-134 and F-135. Note that N-137, which interacts with both ATM and GM1, is not visible in these representations as it is located behind.\nThis study also looked at CLQ-OH and its interaction with GM1. We recently published a model describing a complex formed by one GM1 and two CLQ-OH molecules [10]. For comparison, the same molecular modelling approaches as for ATM (in the presence of surrounding raft lipids) were applied to this model. A stable complex formed by a ganglioside dimer, each monomer being associated with two CLQ-OH molecules, was obtained (Fig. 8d). The stability of this complex is reinforced by a rearrangement of CLQ-OH molecules that interact with each other as well as interacting with the saccharide part of GM1. Consequently, the surface of the ganglioside is almost completely masked, so that the ganglioside dimer can no longer be recognized by the viral spike (Fig. 8c). In the presence of both ATM and CLQ-OH, virus-ganglioside interactions are efficiently blocked, preventing any close contact between the virus and the plasma membrane of host cells. The molecular details of this synergistic antiviral effect are worth mentioning. As shown in Figs. 5 and 8e and Table S1, the QFN triad of the virus spike protein is predicted to interact with the central region of the ganglioside dimer. If the dimer is compared metaphorically to a butterfly, this region corresponds to the insect's head between the wings. For its part, CLQ-OH binds to the wings (Fig. 8d), whereas ATM neutralizes the QFN triad of the virus spike protein (Fig. 8f). Indeed, all attempts to obtain a stable raft-spike protein complex aborted when GM1 was covered by CLMQ-OH and when ATM was bound to the spike protein. In the case of ATM, these data confirm that the QFN triad is critical for GM1 recognition and that although other residues are involved (Fig. 5 and Table S1), the whole binding process is fully controlled by the primary interaction driven by the QFN triad. In agreement with this notion, mutating the QFN triad with alanine residues resulted in an aborted ATM binding process at the post-docking steps. Taken together, these molecular modelling studies indicate that CLQ-OH and ATM, when bound to their respective targets, totally mask the complementary surfaces provided by the lipid raft and the virus spike (Fig. 8c): CLQ-OH binds to GM1 and covers the wing, ATM binds to the virus spike and prevents any interaction with the central area of the ganglioside dimer. Hence, both drugs act as competitive inhibitors of SARS-CoV-2 attachment to the host-cell 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