{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,27]],"date-time":"2026-05-27T21:28:03Z","timestamp":1779917283047,"version":"3.53.1"},"reference-count":87,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2025,3,20]],"date-time":"2025-03-20T00:00:00Z","timestamp":1742428800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000057","name":"NIGMS","doi-asserted-by":"publisher","award":["R35GM133552"],"award-info":[{"award-number":["R35GM133552"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Vanderbilt University","award":["R35GM133552"],"award-info":[{"award-number":["R35GM133552"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>SARS-CoV-2 virus and its variants remain a global health threat, due to their capacity for rapid evolution. Variants throughout the COVID-19 pandemic exhibited variations in virulence, impacting vaccine protection and disease severity. Investigating nonstructural protein variants is critical to understanding viral evolution and manipulation of host protein interactions. We focus on nonstructural protein 3 (nsp3), with multiple domains with different activities, including viral polyprotein cleavage, host deubiquitylation, de-ISGylation, and double-membrane vesicle formation. Using affinity purification\u2013mass spectrometry (AP-MS), we identify differential protein interactions in nsp3 caused by mutations found in variants identified between 2019 and 2024: Alpha 20I, Beta 20H, Delta 21I, Delta 21J, Gamma 20J, Kappa 21B, Lambda 21G, Omicron 21K, and Omicron 21L. A small set of amino acid substitutions in the N-terminal region of nsp3 (nsp3.1) could be traced to increased interactions with RNA-binding proteins, which are vital in viral replication. Meanwhile, variants of the central region of nsp3 (nsp3.2) were found to share interactions with protein quality control machinery, including ER-associated degradation. In this construct, shared trends in interactor enrichment are observed between Omicron 21K and Delta 21I. These results underscore how minor mutations reshape host interactions, emphasizing the evolutionary arms race between the host and virus. We provide a roadmap to track the interaction changes driven by SARS-CoV-2 variant evolution.<\/jats:p>","DOI":"10.3390\/v17030447","type":"journal-article","created":{"date-parts":[[2025,3,20]],"date-time":"2025-03-20T07:59:54Z","timestamp":1742457594000},"page":"447","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Comparative Interactome Profiling of Nonstructural Protein 3 Across SARS-CoV-2 Variants Emerged During the COVID-19 Pandemic"],"prefix":"10.3390","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9645-9948","authenticated-orcid":false,"given":"Valeria","family":"Garcia Lopez","sequence":"first","affiliation":[{"name":"Department of Biological Sciences, Vanderbilt University, Nashville, TN 37240, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4363-6116","authenticated-orcid":false,"given":"Lars","family":"Plate","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, Vanderbilt University, Nashville, TN 37240, USA"},{"name":"Department of Chemistry, Vanderbilt University, Nashville, TN 37240, USA"},{"name":"Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, TN 37232, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,3,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1038\/s41586-021-03777-9","article-title":"Reduced Sensitivity of SARS-CoV-2 Variant Delta to Antibody Neutralization","volume":"596","author":"Planas","year":"2021","journal-title":"Nature"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1038\/s41586-021-04389-z","article-title":"Considerable Escape of SARS-CoV-2 Omicron to Antibody Neutralization","volume":"602","author":"Planas","year":"2021","journal-title":"Nature"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1016\/j.cell.2020.06.043","article-title":"Tracking Changes in SARS-CoV-2 Spike: Evidence That D614G Increases Infectivity of the COVID-19 Virus","volume":"182","author":"Korber","year":"2020","journal-title":"Cell"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1016\/j.cell.2021.12.032","article-title":"The Omicron Variant Is Highly Resistant against Antibody-Mediated Neutralization: Implications for Control of the COVID-19 Pandemic","volume":"185","author":"Hoffmann","year":"2022","journal-title":"Cell"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Chatterjee, S., Bhattacharya, M., Nag, S., Dhama, K., and Chakraborty, C. (2023). A Detailed Overview of SARS-CoV-2 Omicron: Its Sub-Variants, Mutations and Pathophysiology, Clinical Characteristics, Immunological Landscape, Immune Escape, and Therapies. Viruses, 15.","DOI":"10.3390\/v15010167"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"835","DOI":"10.1016\/j.cmi.2023.03.017","article-title":"Clinical Outcomes of the Severe Acute Respiratory Syndrome Coronavirus 2 Omicron and Delta Variant: Systematic Review and Meta-Analysis of 33 Studies Covering 6 037 144 Coronavirus Disease 2019\u2013Positive Patients","volume":"29","author":"Hu","year":"2023","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_7","first-page":"215","article-title":"Coronaviruses","volume":"120","author":"Denison","year":"2011","journal-title":"RNA Biol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"710","DOI":"10.1016\/j.molcel.2020.07.027","article-title":"Coronavirus RNA Proofreading: Molecular Basis and Therapeutic Targeting","volume":"79","author":"Robson","year":"2020","journal-title":"Mol. Cell"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e1009226","DOI":"10.1371\/journal.ppat.1009226","article-title":"The Coronavirus Proofreading Exoribonuclease Mediates Extensive Viral Recombination","volume":"17","author":"Gribble","year":"2021","journal-title":"PLoS Pathog."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"884","DOI":"10.1093\/cid\/ciaa219","article-title":"2019 Novel Coronavirus Is Undergoing Active Recombination","volume":"71","author":"Yi","year":"2020","journal-title":"Clin. Infect. Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"104212","DOI":"10.1016\/j.meegid.2020.104212","article-title":"Full-Genome Evolutionary Analysis of the Novel Corona Virus (2019-NCoV) Rejects the Hypothesis of Emergence as a Result of a Recent Recombination Event","volume":"79","author":"Paraskevis","year":"2020","journal-title":"Infect. Genet. Evol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"e00002-13","DOI":"10.1128\/mBio.00002-13","article-title":"Human Coronavirus EMC Is Not the Same as Severe Acute Respiratory Syndrome Coronavirus","volume":"4","author":"Perlman","year":"2013","journal-title":"MBio"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1038\/s41564-020-0688-y","article-title":"Functional Assessment of Cell Entry and Receptor Usage for SARS-CoV-2 and Other Lineage B Betacoronaviruses","volume":"5","author":"Letko","year":"2020","journal-title":"Nat. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1016\/S0022-2836(03)00865-9","article-title":"Unique and Conserved Features of Genome and Proteome of SARS-Coronavirus, an Early Split-off From the Coronavirus Group 2 Lineage","volume":"331","author":"Snijder","year":"2003","journal-title":"J. Mol. Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"166725","DOI":"10.1016\/j.jmb.2020.11.024","article-title":"Structural Insights into SARS-CoV-2 Proteins","volume":"433","author":"Arya","year":"2021","journal-title":"J. Mol. Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"3174","DOI":"10.1021\/acsinfecdis.0c00500","article-title":"Comparative Multiplexed Interactomics of SARS-CoV-2 and Homologous Coronavirus Nonstructural Proteins Identifies Unique and Shared Host-Cell Dependencies","volume":"6","author":"Davies","year":"2020","journal-title":"ACS Infect. Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1038\/s41586-021-03493-4","article-title":"Multilevel Proteomics Reveals Host Perturbations by SARS-CoV-2 and SARS-CoV","volume":"594","author":"Stukalov","year":"2021","journal-title":"Nature"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1038\/s41586-020-2286-9","article-title":"A SARS-CoV-2 Protein Interaction Map Reveals Targets for Drug Repurposing","volume":"583","author":"Gordon","year":"2020","journal-title":"Nature"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"eabe9403","DOI":"10.1126\/science.abe9403","article-title":"Comparative Host-Coronavirus Protein Interaction Networks Reveal Pan-Viral Disease Mechanisms","volume":"370","author":"Gordon","year":"2020","journal-title":"Science"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1931","DOI":"10.1016\/j.cell.2018.11.028","article-title":"Comparative Flavivirus-Host Protein Interaction Mapping Reveals Mechanisms of Dengue and Zika Virus Pathogenesis","volume":"175","author":"Shah","year":"2018","journal-title":"Cell"},{"key":"ref_21","first-page":"365","article-title":"Global Landscape of HIV\u2013Human Protein Complexes","volume":"481","author":"Cimermancic","year":"2011","journal-title":"Nature"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1038\/nature11289","article-title":"Viral Immune Modulators Perturb the Human Molecular Network by Common and Unique Strategies","volume":"487","author":"Pichlmair","year":"2012","journal-title":"Nature"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"100120","DOI":"10.1016\/j.mcpro.2021.100120","article-title":"Comparative Host Interactomes of the SARS-CoV-2 Nonstructural Protein 3 and Human Coronavirus Homologs","volume":"20","author":"Almasy","year":"2021","journal-title":"Mol. Cell. Proteom."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Samavarchi-Tehrani, P., Abdouni, H., Knight, J.D.R., Astori, A., Samson, R., Lin, Z.-Y., Kim, D.-K., Knapp, J.J., St-Germain, J., and Go, C.D. (2020). A SARS-CoV-2\u2014Host Proximity Interactome. bioRxiv.","DOI":"10.1101\/2020.09.03.282103"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"May, D.G., Martin-Sancho, L., Anschau, V., Liu, S., Chrisopulos, R.J., Scott, K.L., Halfmann, C.T., Pe\u00f1a, R.D., Pratt, D., and Campos, A.R. (2022). A BioID-Derived Proximity Interactome for SARS-CoV-2 Proteins. Viruses, 14.","DOI":"10.3390\/v14030611"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"15199","DOI":"10.1128\/JVI.79.24.15199-15208.2005","article-title":"The Papain-Like Protease from the Severe Acute Respiratory Syndrome Coronavirus Is a Deubiquitinating Enzyme","volume":"79","author":"Lindner","year":"2005","journal-title":"J. Virol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/978-1-4939-2438-7_1","article-title":"Coronaviruses: An Overview of Their Replication and Pathogenesis","volume":"1282","author":"Fehr","year":"2015","journal-title":"Coronaviruses"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/j.antiviral.2017.11.001","article-title":"Nsp3 of Coronaviruses: Structures and Functions of a Large Multidomain Protein","volume":"149","author":"Lei","year":"2018","journal-title":"Antiviral. Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1038\/s41392-022-00878-3","article-title":"SARS-CoV-2 NSP5 and N Protein Counteract the RIG-I Signaling Pathway by Suppressing the Formation of Stress Granules","volume":"7","author":"Zheng","year":"2022","journal-title":"Signal Transduct. Target. Ther."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1038\/s41586-020-2601-5","article-title":"Papain-like Protease Regulates SARS-CoV-2 Viral Spread and Innate Immunity","volume":"587","author":"Shin","year":"2020","journal-title":"Nature"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"e1004113","DOI":"10.1371\/journal.ppat.1004113","article-title":"Structural Basis for the Ubiquitin-Linkage Specificity and DeISGylating Activity of SARS-CoV Papain-Like Protease","volume":"10","author":"Ratia","year":"2014","journal-title":"PLoS Pathog."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"15189","DOI":"10.1128\/JVI.79.24.15189-15198.2005","article-title":"The Papain-like Protease of Severe Acute Respiratory Syndrome Coronavirus Has Deubiquitinating Activity","volume":"79","author":"Barretto","year":"2005","journal-title":"J. Virol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1038\/s41467-021-21060-3","article-title":"Structure of Papain-like Protease from SARS-CoV-2 and Its Complexes with Non-Covalent Inhibitors","volume":"12","author":"Osipiuk","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2366","DOI":"10.1038\/s41467-023-38031-5","article-title":"Dual Domain Recognition Determines SARS-CoV-2 PLpro Selectivity for Human ISG15 and K48-Linked Di-Ubiquitin","volume":"14","author":"Wydorski","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/j.virol.2015.06.016","article-title":"A G-Quadruplex-Binding Macrodomain Within the \u201cSARS-Unique Domain\u201d Is Essential for the Activity of the SARS-Coronavirus Replication\u2013Transcription Complex","volume":"484","author":"Kusov","year":"2015","journal-title":"Virology"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1016\/j.bbrc.2007.10.081","article-title":"The \u201cSARS-Unique Domain\u201d (SUD) of SARS Coronavirus Is an Oligo(G)-Binding Protein","volume":"364","author":"Tan","year":"2007","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"e1000428","DOI":"10.1371\/journal.ppat.1000428","article-title":"The SARS-Unique Domain (SUD) of SARS Coronavirus Contains Two Macrodomains That Bind G-Quadruplexes","volume":"5","author":"Tan","year":"2009","journal-title":"PLoS Pathog."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1395","DOI":"10.1126\/science.abd3629","article-title":"A Molecular Pore Spans the Double Membrane of the Coronavirus Replication Organelle","volume":"369","author":"Wolff","year":"2020","journal-title":"Science"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"e1011614","DOI":"10.1371\/journal.ppat.1011614","article-title":"A Single Inactivating Amino Acid Change in the SARS-CoV-2 NSP3 Mac1 Domain Attenuates Viral Replication in Vivo","volume":"19","author":"Taha","year":"2023","journal-title":"PLoS Pathog."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"e2302083120","DOI":"10.1073\/pnas.2302083120","article-title":"SARS-CoV-2 Mac1 Is Required for IFN Antagonism and Efficient Virus Replication in Cell Culture and in Mice","volume":"120","author":"Alhammad","year":"2023","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_41","unstructured":"Emma, B. (2025, February 19). Hodcroft. CoVariants: SARS-CoV-2 Mutations and Variants of Interest. Available online: https:\/\/covariants.org\/."},{"key":"ref_42","unstructured":"(2025, February 19). Tracking SARS-CoV-2 Variants. Available online: https:\/\/www.who.int\/activities\/tracking-SARS-CoV-2-variants."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"4121","DOI":"10.1093\/bioinformatics\/bty407","article-title":"Nextstrain: Real-Time Tracking of Pathogen Evolution","volume":"34","author":"Hadfield","year":"2018","journal-title":"Bioinformatics"},{"key":"ref_44","unstructured":"(2025, February 13). Preliminary Genomic Characterisation of an Emergent SARS-CoV-2 Lineage in the UK Defined by a Novel Set of Spike Mutations-SARS-CoV-2 Coronavirus\/nCoV-2019 Genomic Epidemiology\u2014Virological. Available online: https:\/\/virological.org\/t\/preliminary-genomic-characterisation-of-an-emergent-sars-cov-2-lineage-in-the-uk-defined-by-a-novel-set-of-spike-mutations\/563."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1038\/s41586-021-03402-9","article-title":"Detection of a SARS-CoV-2 Variant of Concern in South Africa","volume":"592","author":"Tegally","year":"2021","journal-title":"Nature"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1261","DOI":"10.1001\/jama.2021.2088","article-title":"SARS-CoV-2 Viral Variants\u2014Tackling a Moving Target","volume":"325","author":"Mascola","year":"2021","journal-title":"JAMA"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e1128","DOI":"10.1093\/cid\/ciab721","article-title":"Clinical and Virological Features of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Variants of Concern: A Retrospective Cohort Study Comparing B.1.1.7 (Alpha), B.1.351 (Beta), and B.1.617.2 (Delta)","volume":"75","author":"Ong","year":"2021","journal-title":"Clin. Infect. Dis."},{"key":"ref_48","unstructured":"(2025, February 13). Classification of Omicron (B.1.1.529): SARS-CoV-2 Variant of Concern. Available online: https:\/\/www.who.int\/news\/item\/26-11-2021-classification-of-omicron-(b.1.1.529)-sars-cov-2-variant-of-concern."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1038\/s41586-022-04442-5","article-title":"Attenuated Replication and Pathogenicity of SARS-CoV-2 B.1.1.529 Omicron","volume":"603","author":"Shuai","year":"2022","journal-title":"Nature"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1038\/s41577-022-00720-5","article-title":"Estimating Disease Severity of Omicron and Delta SARS-CoV-2 Infections","volume":"22","author":"Sigal","year":"2022","journal-title":"Nat. Rev. Immunol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1186\/s13578-021-00644-y","article-title":"Genome-Wide Analysis of Protein\u2013Protein Interactions and Involvement of Viral Proteins in SARS-CoV-2 Replication","volume":"11","author":"Jiang","year":"2021","journal-title":"Cell Biosci"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2697","DOI":"10.1021\/pr300200x","article-title":"Single-Step Inline Hydroxyapatite Enrichment Facilitates Identification and Quantitation of Phosphopeptides from Mass-Limited Proteomes with MudPIT","volume":"11","author":"Fonslow","year":"2012","journal-title":"J. Proteome. Res."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2498","DOI":"10.1101\/gr.1239303","article-title":"Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks","volume":"13","author":"Shannon","year":"2003","journal-title":"Genome Res"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"12049","DOI":"10.1128\/JVI.00969-07","article-title":"Nuclear Magnetic Resonance Structure of the N-Terminal Domain of Nonstructural Protein 3 from the Severe Acute Respiratory Syndrome Coronavirus","volume":"81","author":"Serrano","year":"2007","journal-title":"J. Virol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"10276","DOI":"10.1128\/JVI.01287-10","article-title":"An Interaction between the Nucleocapsid Protein and a Component of the Replicase-Transcriptase Complex Is Crucial for the Infectivity of Coronavirus Genomic RNA","volume":"84","author":"Hurst","year":"2010","journal-title":"J. Virol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"9159","DOI":"10.1128\/JVI.01275-13","article-title":"Characterization of a Critical Interaction between the Coronavirus Nucleocapsid Protein and Nonstructural Protein 3 of the Viral Replicase-Transcriptase Complex","volume":"87","author":"Hurst","year":"2013","journal-title":"J. Virol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"12325","DOI":"10.1128\/JVI.02082-08","article-title":"Mouse Hepatitis Virus Liver Pathology Is Dependent on ADP-Ribose-1\u2033-Phosphatase, a Viral Function Conserved in the Alpha-like Supergroup","volume":"82","author":"Eriksson","year":"2008","journal-title":"J. Virol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1899","DOI":"10.1099\/vir.0.031856-0","article-title":"The ADP-Ribose-1\u2033-Monophosphatase Domains of Severe Acute Respiratory Syndrome Coronavirus and Human Coronavirus 229E Mediate Resistance to Antiviral Interferon Responses","volume":"92","author":"Kuri","year":"2011","journal-title":"J. Gen. Virol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"e01721-16","DOI":"10.1128\/mBio.01721-16","article-title":"The Conserved Coronavirus Macrodomain Promotes Virulence and Suppresses the Innate Immune Response during Severe Acute Respiratory Syndrome Coronavirus Infection","volume":"7","author":"Fehr","year":"2016","journal-title":"MBio"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"e01969-20","DOI":"10.1128\/JVI.01969-20","article-title":"The SARS-CoV-2 Conserved Macrodomain Is a Mono-ADP-Ribosylhydrolase","volume":"95","author":"Alhammad","year":"2021","journal-title":"J. Virol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"e102277","DOI":"10.15252\/embj.2019102277","article-title":"The SARS-unique Domain (SUD) of SARS-CoV and SARS-CoV-2 Interacts with Human Paip1 to Enhance Viral RNA Translation","volume":"40","author":"Lei","year":"2021","journal-title":"EMBO J."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"3999","DOI":"10.1038\/s41467-023-39709-6","article-title":"Identification of the SARS-Unique Domain of SARS-CoV-2 as an Antiviral Target","volume":"14","author":"Qin","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"13600","DOI":"10.1128\/JVI.78.24.13600-13612.2004","article-title":"Identification of Severe Acute Respiratory Syndrome Coronavirus Replicase Products and Characterization of Papain-Like Protease Activity","volume":"78","author":"Harcourt","year":"2004","journal-title":"J. Virol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"4597","DOI":"10.1016\/j.cell.2023.08.026","article-title":"SARS-CoV-2 Variants Evolve Convergent Strategies to Remodel the Host Response","volume":"186","author":"Bouhaddou","year":"2023","journal-title":"Cell"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"W718","DOI":"10.1093\/nar\/gkac336","article-title":"SubcellulaRVis: A Web-Based Tool to Simplify and Visualise Subcellular Compartment Enrichment","volume":"50","author":"Watson","year":"2022","journal-title":"Nucleic. Acids. Res."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"3825","DOI":"10.1128\/MCB.16.7.3825","article-title":"Specific Sequences in the Fragile X Syndrome Protein FMR1 and the FXR Proteins Mediate Their Binding to 60S Ribosomal Subunits and the Interactions among Them","volume":"16","author":"Siomi","year":"1996","journal-title":"Mol. Cell Biol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1038\/s41392-023-01510-8","article-title":"Metabolic Alterations upon SARS-CoV-2 Infection and Potential Therapeutic Targets against Coronavirus Infection","volume":"8","author":"Chen","year":"2023","journal-title":"Signal Transduct. Target. Ther."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1007\/s00011-021-01487-6","article-title":"SARS-CoV-2 and Pathological Matrix Remodeling Mediators","volume":"70","author":"Guizani","year":"2021","journal-title":"Inflamm. Res."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"107384","DOI":"10.1016\/j.isci.2023.107384","article-title":"F-Actin Nanostructures Rearrangements and Regulation Are Essential for SARS-CoV-2 Particle Production in Host Pulmonary Cells","volume":"26","author":"Swain","year":"2023","journal-title":"iScience"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"05032","DOI":"10.7189\/jogh.12.05032","article-title":"COVID-19 Disease Severity in Persons Infected with the Omicron Variant Compared with the Delta Variant in Qatar","volume":"12","author":"Butt","year":"2022","journal-title":"J. Glob. Health"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"e239","DOI":"10.1002\/mco2.239","article-title":"The Rapid Rise of SARS-CoV-2 Omicron Subvariants with Immune Evasion Properties: XBB.1.5 and BQ.1.1 Subvariants","volume":"4","author":"Ao","year":"2023","journal-title":"MedComm"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"e01385-24","DOI":"10.1128\/spectrum.01385-24","article-title":"Prospective Clinical Performance of CoVarScan in Identifying SARS-CoV-2 Omicron Subvariants","volume":"13","author":"Zhu","year":"2025","journal-title":"Microbiol. Spectr."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1414331","DOI":"10.3389\/fmed.2024.1414331","article-title":"SARS-CoV-2 Infectivity and Antigenic Evasion: Spotlight on Isolated Omicron Sub-Lineages","volume":"11","author":"Barrera","year":"2024","journal-title":"Front Med."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1128\/JVI.00766-21","article-title":"Unique Mutations in the Murine Hepatitis Virus Macrodomain Differentially Attenuate Virus Replication, Indicating Multiple Roles for the Macrodomain in Coronavirus Replication","volume":"95","author":"Voth","year":"2021","journal-title":"J. Virol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1038\/s41564-020-00846-z","article-title":"The SARS-CoV-2 RNA\u2013Protein Interactome in Infected Human Cells","volume":"6","author":"Schmidt","year":"2020","journal-title":"Nat. Microbiol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"490","DOI":"10.1016\/j.molcel.2023.11.032","article-title":"SARS-CoV-2 RNA Stabilizes Host MRNAs to Elicit Immunopathogenesis","volume":"84","author":"Zhao","year":"2024","journal-title":"Mol. Cell"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1038\/s41467-017-00102-9","article-title":"Negri Bodies Are Viral Factories with Properties of Liquid Organelles","volume":"8","author":"Nikolic","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"e01771-19","DOI":"10.1128\/JVI.01771-19","article-title":"Phase Separation of Epstein-Barr Virus EBNA2 and Its Coactivator EBNALP Controls Gene Expression","volume":"94","author":"Peng","year":"2020","journal-title":"J. Virol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.cell.2020.11.030","article-title":"RNA-Mediated Feedback Control of Transcriptional Condensates","volume":"184","author":"Henninger","year":"2021","journal-title":"Cell"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"1092","DOI":"10.1016\/j.molcel.2020.11.025","article-title":"Phosphoregulation of Phase Separation by the SARS-CoV-2 N Protein Suggests a Biophysical Basis for Its Dual Functions","volume":"80","author":"Carlson","year":"2020","journal-title":"Mol. Cell"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"107828","DOI":"10.1016\/j.jbc.2024.107828","article-title":"N Terminus of SARS-CoV-2 Nonstructural Protein 3 Interrupts RNA-Driven Phase Separation of N Protein by Displacing RNA","volume":"300","author":"Ke","year":"2024","journal-title":"J. Biol. Chem."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"902","DOI":"10.1038\/s44319-023-00043-z","article-title":"The NSP3 Protein of SARS-CoV-2 Binds Fragile X Mental Retardation Proteins to Disrupt UBAP2L Interactions","volume":"25","author":"Garvanska","year":"2024","journal-title":"EMBO Rep."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1016\/j.ydbio.2010.02.031","article-title":"FMR1\/FXR1 and the MiRNA Pathway Are Required for Eye and Neural Crest Development","volume":"341","author":"Gessert","year":"2010","journal-title":"Dev. Biol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"134411","DOI":"10.1016\/j.ijbiomac.2024.134411","article-title":"PRMT1 and TDRD3 Promote Stress Granule Assembly by Rebuilding the Protein-RNA Interaction Network","volume":"277","author":"Qin","year":"2024","journal-title":"Int. J. Biol. Macromol."},{"key":"ref_85","first-page":"RP100834","article-title":"The Glycoprotein Quality Control Factor Malectin Promotes Coronavirus Replication and Viral Protein Biogenesis","volume":"13","author":"Davies","year":"2024","journal-title":"Elife"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1016\/j.gpb.2021.09.007","article-title":"Integrative Multi-Omics Landscape of Nonstructural Protein 3 of Severe Acute Respiratory Syndrome Coronaviruses","volume":"19","author":"Shi","year":"2021","journal-title":"Genom. Proteom. Bioinform."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1745","DOI":"10.1016\/j.chom.2022.10.012","article-title":"Antigenic Cartography of Well-Characterized Human Sera Shows SARS-CoV-2 Neutralization Differences Based on Infection and Vaccination History","volume":"30","author":"Wang","year":"2022","journal-title":"Cell Host Microbe"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/17\/3\/447\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T16:57:00Z","timestamp":1760029020000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/17\/3\/447"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,3,20]]},"references-count":87,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2025,3]]}},"alternative-id":["v17030447"],"URL":"https:\/\/doi.org\/10.3390\/v17030447","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,3,20]]}}}