{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T16:14:21Z","timestamp":1791562461609,"version":"4.3.4"},"reference-count":74,"publisher":"MDPI AG","issue":"20","license":[{"start":{"date-parts":[[2025,10,21]],"date-time":"2025-10-21T00:00:00Z","timestamp":1761004800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"College of Health & Life Sciences, Hamad Bin Khalifa University"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The SARS-CoV-2 spike protein, through its receptor binding domain (S1-RBD), binds to the angiotensin-converting enzyme 2 (ACE2) receptor on the host cell membrane, leading to viral infection. Several mutations in S1-RBD in SARS-CoV-2 variants are known to enhance infection through an increased affinity for ACE2. While many reports are available describing the SARS-CoV-2 infection mechanism, there is a dearth of studies towards understanding the initial interaction of the S1-RBD with ACE2 on living host cells and the role of endocytosis and cytoskeleton in the process. Here, we reconstituted the interaction between S1-RBD- and ACE2-expressing host cells in a hybrid live cell-supported lipid bilayer (SLB) platform enabling live monitoring of the interaction between S1-RBD on SLBs and the ACE2 receptor on living cells and showed that cells depleted Omicron S1-RBD from SLB corrals, likely through endocytosis. Specifically, interaction of living host cells with S1-RBD-functionalized SLB substrates resulted in the enrichment of S1-RBD and ACE2 at the cell\u2013SLB interface. Interaction of host cells with wild type (WT), Omicron, and Omicron Revertant S1-RBD functionalized on micron-scale SLB corrals, which mimic viral membranes but are flat, also resulted in their enrichment. However, cells interacting with Omicron S1-RBD revealed a depletion of the protein from many corrals, which was generally not observed with the WT S1-RBD and was reduced with the Omicron Revertant, which contains the Q493R mutation reversion, S1-RBD. Further, S1-RBD depletion coincided with the localization of the early endosomal marker EEA1. Importantly, treatment of cells with the clathrin inhibitor, pitstop 2, but not the myosin II inhibitor, blebbistatin, significantly reduced Omicron S1-RBD depletion. Collectively, these observations suggest that the SARS-CoV-2 Omicron variant has evolved, through mutations in its S1-RBD, to take advantage of the cellular endocytic pathway for enhanced infection, which is not observed with the parental SARS-CoV-2 and appears to be lost in the Omicron Revertant variant. Additionally, these results underscore the significance of the hybrid live cell\u2013SLB platform in studying SARS-CoV-2 S1-RBD-ACE2 interaction and the potential impact of mutations in the S1-RBD on adapting to a specific cellular entry mechanism.<\/jats:p>","DOI":"10.3390\/ijms262010216","type":"journal-article","created":{"date-parts":[[2025,10,21]],"date-time":"2025-10-21T13:42:03Z","timestamp":1761054123000},"page":"10216","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Selective Endocytosis-Mediated Omicron S1-RBD Internalization Revealed by Reconstitution of ACE2-S1-RBD Interaction on Micropatterned Membrane Substrates"],"prefix":"10.3390","volume":"26","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7222-4669","authenticated-orcid":false,"given":"Angelin M.","family":"Philip","sequence":"first","affiliation":[{"name":"College of Health & Life Sciences, Hamad Bin Khalifa University, Doha, Qatar"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0006-4264-2302","authenticated-orcid":false,"given":"S. M. Nasir","family":"Uddin","sequence":"additional","affiliation":[{"name":"College of Health & Life Sciences, Hamad Bin Khalifa University, Doha, Qatar"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5444-3910","authenticated-orcid":false,"given":"Zeyaul","family":"Islam","sequence":"additional","affiliation":[{"name":"Qatar Biomedical Research Institute, Hamad Bin Khalifa University, Doha, Qatar"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Prasanna R.","family":"Kolatkar","sequence":"additional","affiliation":[{"name":"Qatar Biomedical Research Institute, Hamad Bin Khalifa University, Doha, Qatar"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9194-4127","authenticated-orcid":false,"given":"Kabir H.","family":"Biswas","sequence":"additional","affiliation":[{"name":"College of Health & Life Sciences, Hamad Bin Khalifa University, Doha, Qatar"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,10,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1038\/s41579-023-00878-2","article-title":"The evolution of SARS-CoV-2","volume":"21","author":"Markov","year":"2023","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1038\/s41591-020-0820-9","article-title":"The proximal origin of SARS-CoV-2","volume":"26","author":"Andersen","year":"2020","journal-title":"Nat. Med."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1141","DOI":"10.1038\/s41401-020-0485-4","article-title":"Structural and functional properties of SARS-CoV-2 spike protein: Potential antivirus drug development for COVID-19","volume":"41","author":"Huang","year":"2020","journal-title":"Acta Pharmacol. Sin."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Hoter, A., and Naim, H.Y. (2022). Biochemical Characterization of SARS-CoV-2 Spike RBD Mutations and Their Impact on ACE2 Receptor Binding. Front. Mol. Biosci., 9.","DOI":"10.3389\/fmolb.2022.893843"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2713","DOI":"10.1007\/s11033-022-08193-4","article-title":"Interactions of angiotensin-converting enzyme-2 (ACE2) and SARS-CoV-2 spike receptor-binding domain (RBD): A structural perspective","volume":"50","author":"Borkotoky","year":"2023","journal-title":"Mol. Biol. Rep."},{"key":"ref_6","first-page":"162","article-title":"SARS-CoV-2 variant biology: Immune escape, transmission and fitness","volume":"21","author":"Carabelli","year":"2023","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Chang, X., Liu, X., Martina, B., Zeltins, A., Augusto, G., Vogel, M., Mohsen, M.O., Speiser, D.E., and Bachmann, M.F. (2023). Vaccination using mutated receptor binding domains of SARS-CoV-2: Evidence for partial immune escape but not serotype formation. Front. Immunol., 14.","DOI":"10.3389\/fimmu.2023.1114396"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1016\/j.cell.2022.12.018","article-title":"Alarming antibody evasion properties of rising SARS-CoV-2 BQ and XBB subvariants","volume":"186","author":"Wang","year":"2023","journal-title":"Cell"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1038\/s41586-022-04980-y","article-title":"BA.2.12.1, BA.4 and BA.5 escape antibodies elicited by Omicron infection","volume":"608","author":"Cao","year":"2022","journal-title":"Nature"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"31","DOI":"10.56782\/pps.292","article-title":"BioNTech\/Pfizer (BNT162b2) COVID-19 mRNA vaccine: Manufacturing, immunogenicity, efficacy and safety","volume":"23","author":"Alkhalil","year":"2025","journal-title":"Prospect. Pharm. Sci."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Ahmed, W.S., Philip, A.M., and Biswas, K.H. (2022). Decreased Interfacial Dynamics Caused by the N501Y Mutation in the SARS-CoV-2 S1 Spike:ACE2 Complex. Front. Mol. Biosci., 9.","DOI":"10.3389\/fmolb.2022.846996"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1966","DOI":"10.1016\/j.csbj.2023.02.019","article-title":"Reversal of the unique Q493R mutation increases the affinity of Omicron S1-RBD for ACE2","volume":"21","author":"Philip","year":"2023","journal-title":"Comput. Struct. Biotechnol. J."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"100991","DOI":"10.1016\/j.xcrm.2023.100991","article-title":"An updated atlas of antibody evasion by SARS-CoV-2 Omicron sub-variants including BQ.1.1 and XBB","volume":"4","author":"He","year":"2023","journal-title":"Cell Rep. Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1038\/s41421-023-00584-6","article-title":"Evolving spike mutations in SARS-CoV-2 Omicron variants facilitate evasion from breakthrough infection-acquired antibodies","volume":"9","author":"Chen","year":"2023","journal-title":"Cell Discov."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1038\/s41586-020-2179-y","article-title":"Structural basis of receptor recognition by SARS-CoV-2","volume":"581","author":"Shang","year":"2020","journal-title":"Nature"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1016\/j.cell.2020.02.052","article-title":"SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor","volume":"181","author":"Hoffmann","year":"2020","journal-title":"Cell"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Bayati, A., Kumar, R., Francis, V., and McPherson, P.S. (2021). SARS-CoV-2 infects cells after viral entry via clathrin-mediated endocytosis. J. Biol. Chem., 296.","DOI":"10.1016\/j.jbc.2021.100306"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Nejat, R., Torshizi, M.F., and Najafi, D.J. (2023). S Protein, ACE2 and Host Cell Proteases in SARS-CoV-2 Cell Entry and Infectivity; Is Soluble ACE2 a Two Blade Sword? A Narrative Review. Vaccines, 11.","DOI":"10.3390\/vaccines11020204"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1135","DOI":"10.1080\/22221751.2022.2059403","article-title":"SARS-CoV-2 pseudovirus enters the host cells through spike protein-CD147 in an Arf6-dependent manner","volume":"11","author":"Zhou","year":"2022","journal-title":"Emerg. Microbes Infect."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/j.chembiol.2023.02.001","article-title":"SIM imaging resolves endocytosis of SARS-CoV-2 spike RBD in living cells","volume":"30","author":"Miao","year":"2023","journal-title":"Cell Chem. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1613","DOI":"10.1242\/jcs.073395","article-title":"Endocytic adaptors\u2014Social networking at the plasma membrane","volume":"124","author":"Reider","year":"2011","journal-title":"J. Cell Sci."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Kamentseva, R., Kosheverova, V., Kharchenko, M., Zlobina, M., Salova, A., Belyaeva, T., Nikolsky, N., and Kornilova, E. (2020). Functional cycle of EEA1-positive early endosome: Direct evidence for pre-existing compartment of degradative pathway. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0232532"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1038\/s41422-020-00460-y","article-title":"AXL is a candidate receptor for SARS-CoV-2 that promotes infection of pulmonary and bronchial epithelial cells","volume":"31","author":"Wang","year":"2021","journal-title":"Cell Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1185","DOI":"10.1038\/s41567-023-02009-3","article-title":"Two-component molecular motor driven by a GTPase cycle","volume":"19","author":"Singh","year":"2023","journal-title":"Nat. Phys."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"706","DOI":"10.1038\/s41586-022-04474-x","article-title":"Altered TMPRSS2 usage by SARS-CoV-2 Omicron impacts infectivity and fusogenicity","volume":"603","author":"Meng","year":"2022","journal-title":"Nature"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1972","DOI":"10.1016\/S0006-3495(95)80067-6","article-title":"Electric field-induced concentration gradients in planar supported bilayers","volume":"69","author":"Groves","year":"1995","journal-title":"Biophys. J."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2716","DOI":"10.1016\/S0006-3495(96)79462-6","article-title":"Electrical manipulation of glycan-phosphatidyl inositol-tethered proteins in planar supported bilayers","volume":"71","author":"Groves","year":"1996","journal-title":"Biophys. J."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1126\/science.275.5300.651","article-title":"Micropatterning fluid lipid bilayers on solid supports","volume":"275","author":"Groves","year":"1997","journal-title":"Science"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1191","DOI":"10.1126\/science.1119238","article-title":"Altered TCR signaling from geometrically repatterned immunological synapses","volume":"310","author":"Mossman","year":"2005","journal-title":"Science"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1146\/annurev-biophys-070317-033330","article-title":"Hybrid Live Cell-Supported Membrane Interfaces for Signaling Studies","volume":"48","author":"Biswas","year":"2019","journal-title":"Annu. Rev. Biophys."},{"key":"ref_31","first-page":"E5696","article-title":"Spatially modulated ephrinA1:EphA2 signaling increases local contractility and global focal adhesion dynamics to promote cell motility","volume":"115","author":"Chen","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"8672","DOI":"10.1038\/ncomms9672","article-title":"Integrin-beta3 clusters recruit clathrin-mediated endocytic machinery in the absence of traction force","volume":"6","author":"Yu","year":"2015","journal-title":"Nat. Commun."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1016\/j.yexcr.2017.02.037","article-title":"Early events in the assembly of E-cadherin adhesions","volume":"358","author":"Biswas","year":"2017","journal-title":"Exp. Cell Res."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Biswas, K.H., Zhongwen, C., Dubey, A.K., Oh, D., and Groves, J.T. (2018). Multicomponent Supported Membrane Microarray for Monitoring Spatially Resolved Cellular Signaling Reactions. Adv. Biosyst., 2.","DOI":"10.1002\/adbi.201800015"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1044","DOI":"10.1016\/j.bpj.2016.06.027","article-title":"Sustained alpha-catenin Activation at E-cadherin Junctions in the Absence of Mechanical Force","volume":"111","author":"Biswas","year":"2016","journal-title":"Biophys. J."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"9781","DOI":"10.1021\/acs.langmuir.8b01364","article-title":"Fabrication of multicomponent, spatially segregated DNA and protein functionalized supported membrane microarray","volume":"34","author":"Biswas","year":"2018","journal-title":"Langmuir"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Chen, Z., Biswas, K.H., and Groves, J.T. (2022). Patterned Substrate of Mobile and Immobile Ligands to Probe EphA2 Receptor Clustering. Bio-Protocol, 12.","DOI":"10.21769\/BioProtoc.4434"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"10932","DOI":"10.1073\/pnas.1513775112","article-title":"E-cadherin junction formation involves an active kinetic nucleation process","volume":"112","author":"Biswas","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1380","DOI":"10.1126\/science.1181729","article-title":"Restriction of receptor movement alters cellular response: Physical force sensing by EphA2","volume":"327","author":"Salaita","year":"2010","journal-title":"Science"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"3286","DOI":"10.1529\/biophysj.107.119099","article-title":"T cell receptor microcluster transport through molecular mazes reveals mechanism of translocation","volume":"94","author":"DeMond","year":"2008","journal-title":"Biophys. J."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Yamazaki, V., Sirenko, O., Schafer, R.J., Nguyen, L., Gutsmann, T., Brade, L., and Groves, J.T. (2005). Cell membrane array fabrication and assay technology. BMC Biotechnol., 5.","DOI":"10.1186\/1472-6750-5-18"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1038\/nchembio737","article-title":"Neuronal synapse interaction reconstituted between live cells and supported lipid bilayers","volume":"1","author":"Pautot","year":"2005","journal-title":"Nat. Chem. Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1299\/jbse.17-00699","article-title":"Regulation of \u03b1-catenin conformation at cadherin adhesions","volume":"13","author":"Biswas","year":"2018","journal-title":"J. Biomech. Sci. Eng."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"e67379","DOI":"10.7554\/eLife.67379","article-title":"Probing the effect of clustering on EphA2 receptor signaling efficiency by subcellular control of ligand-receptor mobility","volume":"10","author":"Chen","year":"2021","journal-title":"eLife"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Knyazev, E., Nersisyan, S., and Tonevitsky, A. (2021). Endocytosis and Transcytosis of SARS-CoV-2 Across the Intestinal Epithelium and Other Tissue Barriers. Front. Immunol., 12.","DOI":"10.3389\/fimmu.2021.636966"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"e202400253","DOI":"10.1002\/cmdc.202400253","article-title":"Inhibition Clathrin Mediated Endocytosis: Pitstop 1\u2009and Pitstop 2 Chimeras","volume":"19","author":"Prichard","year":"2024","journal-title":"ChemMedChem"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e2415313121","DOI":"10.1073\/pnas.2415313121","article-title":"Stepwise assembly of the AP2 endocytic clathrin adaptor complex","volume":"121","author":"Hollopeter","year":"2024","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"35557","DOI":"10.1074\/jbc.M405319200","article-title":"Mechanism of Blebbistatin Inhibition of Myosin II *","volume":"279","author":"Sellers","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"13593","DOI":"10.18632\/aging.205297","article-title":"Uncovering a unique pathogenic mechanism of SARS-CoV-2 omicron variant: Selective induction of cellular senescence","volume":"15","author":"Hornung","year":"2023","journal-title":"Aging"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Fujimoto, A., Kawai, H., Kawamura, R., and Kitamura, A. (2024). Interaction of Receptor-Binding Domain of the SARS-CoV-2 Omicron Variant with hACE2 and Actin. Cells, 13.","DOI":"10.3390\/cells13161318"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"2254","DOI":"10.1038\/s41467-024-46490-7","article-title":"Distinct evolution of SARS-CoV-2 Omicron XBB and BA.2.86\/JN.1 lineages combining increased fitness and antibody evasion","volume":"15","author":"Planas","year":"2024","journal-title":"Nat. Commun."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1055","DOI":"10.1016\/j.str.2024.06.012","article-title":"Spike structures, receptor binding, and immune escape of recently circulating SARS-CoV-2 Omicron BA.2.86, JN.1, EG.5, EG.5.1, and HV.1 sub-variants","volume":"32","author":"Li","year":"2024","journal-title":"Structure"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1002\/jcc.27025","article-title":"Binding of human ACE2 and RBD of Omicron enhanced by unique interaction patterns among SARS-CoV-2 variants of concern","volume":"44","author":"Kim","year":"2023","journal-title":"J. Comput. Chem."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1016\/j.cell.2021.12.046","article-title":"SARS-CoV-2 Omicron-B.1.1.529 leads to widespread escape from neutralizing antibody responses","volume":"185","author":"Dejnirattisai","year":"2022","journal-title":"Cell"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1038\/s41586-021-04386-2","article-title":"Broadly neutralizing antibodies overcome SARS-CoV-2 Omicron antigenic shift","volume":"602","author":"Cameroni","year":"2022","journal-title":"Nature"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"113444","DOI":"10.1016\/j.celrep.2023.113444","article-title":"Evolution of the SARS-CoV-2 Omicron spike","volume":"42","author":"Parsons","year":"2023","journal-title":"Cell Rep."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1080\/22221751.2021.2023329","article-title":"SARS-CoV-2 Omicron variant shows less efficient replication and fusion activity when compared with Delta variant in TMPRSS2-expressed cells","volume":"11","author":"Zhao","year":"2022","journal-title":"Emerg. Microbes Infect."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1038\/s41586-021-04266-9","article-title":"Enhanced fusogenicity and pathogenicity of SARS-CoV-2 Delta P681R mutation","volume":"602","author":"Saito","year":"2022","journal-title":"Nature"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1021\/acsnanoscienceau.3c00060","article-title":"Single-Molecule Investigation of the Binding Interface Stability of SARS-CoV-2 Variants with ACE2","volume":"4","author":"Ray","year":"2024","journal-title":"ACS Nanosci. Au"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1038\/s41586-022-05053-w","article-title":"Antibody evasion by SARS-CoV-2 Omicron subvariants BA.2.12.1, BA.4 and BA.5","volume":"608","author":"Wang","year":"2022","journal-title":"Nature"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"108299","DOI":"10.1016\/j.isci.2023.108299","article-title":"Impact of mutations defining SARS-CoV-2 Omicron subvariants BA.2.12.1 and BA.4\/5 on Spike function and neutralization","volume":"26","author":"Pastorio","year":"2023","journal-title":"iScience"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1512","DOI":"10.1016\/j.chom.2022.09.002","article-title":"Antigenic characterization of the SARS-CoV-2 Omicron subvariant BA.2.75","volume":"30","author":"Wang","year":"2022","journal-title":"Cell Host Microbe"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"30710","DOI":"10.1073\/pnas.2000942117","article-title":"mGreenLantern: A bright monomeric fluorescent protein with rapid expression and cell filling properties for neuronal imaging","volume":"117","author":"Campbell","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1612","DOI":"10.1038\/s41592-022-01660-7","article-title":"Chemically stable fluorescent proteins for advanced microscopy","volume":"19","author":"Campbell","year":"2022","journal-title":"Nat. Methods"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1897","DOI":"10.1016\/j.bpj.2022.04.015","article-title":"Competition for shared downstream signaling molecules establishes indirect negative feedback between EGFR and EphA2","volume":"121","author":"Oh","year":"2022","journal-title":"Biophys. J."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1098","DOI":"10.1126\/science.aau5721","article-title":"A molecular assembly phase transition and kinetic proofreading modulate Ras activation by SOS","volume":"363","author":"Huang","year":"2019","journal-title":"Science"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"6775","DOI":"10.1021\/acs.langmuir.6b01377","article-title":"A Microbead Supported Membrane-Based Fluorescence Imaging Assay Reveals Intermembrane Receptor-Ligand Complex Dimension with Nanometer Precision","volume":"32","author":"Biswas","year":"2016","journal-title":"Langmuir"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/S0091-679X(10)97008-8","article-title":"Protein micropatterns: A direct printing protocol using deep UVs","volume":"97","author":"Azioune","year":"2010","journal-title":"Methods Cell Biol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"10764","DOI":"10.1021\/acs.langmuir.8b01348","article-title":"Membrane Reconstitution of Monoamine Oxidase Enzymes on Supported Lipid Bilayers","volume":"34","author":"Wang","year":"2018","journal-title":"Langmuir"},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Taylor, M.J., Perrais, D., and Merrifield, C.J. (2011). A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol., 9.","DOI":"10.1371\/journal.pbio.1000604"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"3711","DOI":"10.1038\/s41467-020-17486-w","article-title":"In vivo cell biological screening identifies an endocytic capture mechanism for T-tubule formation","volume":"11","author":"Hall","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1919","DOI":"10.1038\/ncomms2865","article-title":"A nanometre-scale resolution interference-based probe of interfacial phenomena between microscopic objects and surfaces","volume":"4","author":"Ugaz","year":"2013","journal-title":"Nat. Commun."},{"key":"ref_73","first-page":"e63377","article-title":"Simultaneous Visualization of the Dynamics of Crosslinked and Single Microtubules In Vitro by TIRF Microscopy","volume":"180","author":"Mani","year":"2022","journal-title":"J. Vis. Exp."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: An open-source platform for biological-image analysis","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nat. 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