{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T00:40:55Z","timestamp":1791852055057,"version":"4.3.4"},"reference-count":78,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2024,5,10]],"date-time":"2024-05-10T00:00:00Z","timestamp":1715299200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"NIH\/NIAID","award":["R37 AI150453"],"award-info":[{"award-number":["R37 AI150453"]}]},{"name":"NIH\/NIAID","award":["R01 AI135806"],"award-info":[{"award-number":["R01 AI135806"]}]},{"name":"NIH\/NIAID","award":["R01AI139238"],"award-info":[{"award-number":["R01AI139238"]}]},{"name":"NIH\/NIAID","award":["1842396"],"award-info":[{"award-number":["1842396"]}]},{"name":"National Science Foundation Graduate Research Fellowship Program","award":["R37 AI150453"],"award-info":[{"award-number":["R37 AI150453"]}]},{"name":"National Science Foundation Graduate Research Fellowship Program","award":["R01 AI135806"],"award-info":[{"award-number":["R01 AI135806"]}]},{"name":"National Science Foundation Graduate Research Fellowship Program","award":["R01AI139238"],"award-info":[{"award-number":["R01AI139238"]}]},{"name":"National Science Foundation Graduate Research Fellowship Program","award":["1842396"],"award-info":[{"award-number":["1842396"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biomolecules"],"abstract":"<jats:p>Host restriction factor SERINC5 (SER5) incorporates into the HIV-1 membrane and inhibits infectivity by a poorly understood mechanism. Recently, SER5 was found to exhibit scramblase-like activity leading to the externalization of phosphatidylserine (PS) on the viral surface, which has been proposed to be responsible for SER5\u2019s antiviral activity. This and other reports that document modulation of HIV-1 infectivity by viral lipid composition prompted us to investigate the role of PS in regulating SER5-mediated HIV-1 restriction. First, we show that the level of SER5 incorporation into virions correlates with an increase in PS levels in the outer leaflet of the viral membrane. We developed an assay to estimate the PS distribution across the viral membrane and found that SER5, but not SER2, which lacks antiviral activity, abrogates PS asymmetry by externalizing this lipid. Second, SER5 incorporation diminished the infectivity of pseudoviruses produced from cells lacking a flippase subunit CDC50a and, therefore, exhibited a higher baseline level of surface-accessible PS. Finally, exogenous manipulation of the viral PS levels utilizing methyl-alpha-cyclodextrin revealed a lack of correlation between external PS and virion infectivity. Taken together, our study implies that the increased PS exposure to SER5-containing virions itself is not directly linked to HIV-1 restriction.<\/jats:p>","DOI":"10.3390\/biom14050570","type":"journal-article","created":{"date-parts":[[2024,5,14]],"date-time":"2024-05-14T08:59:37Z","timestamp":1715677177000},"page":"570","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Disruption of Transmembrane Phosphatidylserine Asymmetry by HIV-1 Incorporated SERINC5 Is Not Responsible for Virus Restriction"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5418-7200","authenticated-orcid":false,"given":"Gokul","family":"Raghunath","sequence":"first","affiliation":[{"name":"Department of Pediatrics, Division of Infectious Diseases, School of Medicine, Emory University, Atlanta, GA 30322, USA"},{"name":"Children\u2019s Healthcare of Atlanta, Atlanta, GA 30322, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth H.","family":"Abbott","sequence":"additional","affiliation":[{"name":"Emory College of Arts and Sciences, Emory University, Atlanta, GA 30322, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mariana","family":"Marin","sequence":"additional","affiliation":[{"name":"Department of Pediatrics, Division of Infectious Diseases, School of Medicine, Emory University, Atlanta, GA 30322, USA"},{"name":"Children\u2019s Healthcare of Atlanta, Atlanta, GA 30322, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hui","family":"Wu","sequence":"additional","affiliation":[{"name":"Department of Pediatrics, Division of Infectious Diseases, School of Medicine, Emory University, Atlanta, GA 30322, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5441-2196","authenticated-orcid":false,"given":"Judith Mary","family":"Reyes Ballista","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, GA 30602, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4929-8085","authenticated-orcid":false,"given":"Melinda A.","family":"Brindley","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, GA 30602, USA"},{"name":"Department of Population Health, College of Veterinary Medicine, University of Georgia, Athens, GA 30602, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5385-3013","authenticated-orcid":false,"given":"Gregory B.","family":"Melikyan","sequence":"additional","affiliation":[{"name":"Department of Pediatrics, Division of Infectious Diseases, School of Medicine, Emory University, Atlanta, GA 30322, USA"},{"name":"Children\u2019s Healthcare of Atlanta, Atlanta, GA 30322, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,5,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"35776","DOI":"10.1074\/jbc.M505712200","article-title":"Serinc, an activity-regulated protein family, incorporates serine into membrane lipid synthesis","volume":"280","author":"Inuzuka","year":"2005","journal-title":"J. Biol. Chem."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1240","DOI":"10.1002\/prot.26145","article-title":"Fungal Ice2p is in the same superfamily as SERINCs, restriction factors for HIV and other viruses","volume":"89","author":"Levine","year":"2021","journal-title":"Proteins"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1038\/nature15400","article-title":"SERINC3 and SERINC5 restrict HIV-1 infectivity and are counteracted by Nef","volume":"526","author":"Usami","year":"2015","journal-title":"Nature"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1038\/nature15399","article-title":"HIV-1 Nef promotes infection by excluding SERINC5 from virion incorporation","volume":"526","author":"Rosa","year":"2015","journal-title":"Nature"},{"key":"ref_5","first-page":"1548905","article-title":"SERINC as a Restriction Factor to Inhibit Viral Infectivity and the Interaction with HIV","volume":"2017","year":"2017","journal-title":"J. Immunol. Res."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1146\/annurev-virology-092917-043308","article-title":"SERINC5 as a New Restriction Factor for Human Immunodeficiency Virus and Murine Leukemia Virus","volume":"5","author":"Firrito","year":"2018","journal-title":"Annu. Rev. Virol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"e00588-20","DOI":"10.1128\/mBio.00588-20","article-title":"SERINC5 Potently Restricts Retrovirus Infection","volume":"11","author":"Timilsina","year":"2020","journal-title":"Mbio"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Xu, S.F., Zheng, Z.C., Pathak, J.L., Cheng, H.Y., Zhou, Z.L., Chen, Y.P., Wu, Q.Y., Wang, L.J., Zeng, M.T., and Wu, L.H. (2022). The Emerging Role of the Serine Incorporator Protein Family in Regulating Viral Infection. Front. Cell Dev. Biol., 10.","DOI":"10.3389\/fcell.2022.856468"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Ahmed, S.S., Bajak, K., and Fackler, O.T. (2024). Beyond Impairment of Virion Infectivity: New Activities of the Anti-HIV Host Cell Factor SERINC5. Viruses, 16.","DOI":"10.3390\/v16020284"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.virol.2017.12.005","article-title":"Localization to detergent-resistant membranes and HIV-1 core entry inhibition correlate with HIV-1 restriction by SERINC5","volume":"515","author":"Schulte","year":"2018","journal-title":"Virology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e02923-22","DOI":"10.1128\/mbio.02923-22","article-title":"Restriction of Influenza A Virus by SERINC5","volume":"13","author":"Lai","year":"2022","journal-title":"Mbio"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Liu, Y., Wang, H., Zhang, J., Yang, J., Bai, L., Zheng, B.S., Zheng, T.H., Wang, Y.C., Li, J.H., and Zhang, W.Y. (2020). SERINC5 Inhibits the Secretion of Complete and Genome-Free Hepatitis B Virions Through Interfering With the Glycosylation of the HBV Envelope. Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.00697"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2935","DOI":"10.1038\/s41467-022-30609-9","article-title":"SARS-CoV-2 ORF7a potently inhibits the antiviral effect of the host factor SERINC5","volume":"13","author":"Timilsina","year":"2022","journal-title":"Nat. Commun."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"e01651-18","DOI":"10.1128\/JVI.01651-18","article-title":"Murine Leukemia Virus Glycosylated Gag Reduces Murine SERINC5 Protein Expression at Steady-State Levels via the Endosome\/Lysosome Pathway to Counteract SERINC5 Antiretroviral Activity","volume":"93","author":"Li","year":"2019","journal-title":"J. Virol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"7013","DOI":"10.1074\/jbc.RA119.007662","article-title":"The retroviral accessory proteins S2, Nef, and glycoMA use similar mechanisms for antagonizing the host restriction factor SERINC5","volume":"294","author":"Ahmad","year":"2019","journal-title":"J. Biol. Chem."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"e01985-16","DOI":"10.1128\/mBio.01985-16","article-title":"Functional Interplay Between Murine Leukemia Virus Glycogag, Serinc5, and Surface Glycoprotein Governs Virus Entry, with Opposite Effects on Gammaretroviral and Ebolavirus Glycoproteins","volume":"7","author":"Ahi","year":"2016","journal-title":"Mbio"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"869","DOI":"10.1016\/j.celrep.2017.12.082","article-title":"A Long Cytoplasmic Loop Governs the Sensitivity of the Anti-viral Host Protein SERINC5 to HIV-1 Nef","volume":"22","author":"Dai","year":"2018","journal-title":"Cell Rep."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"6014","DOI":"10.1074\/jbc.M117.777714","article-title":"SERINC5 protein inhibits HIV-1 fusion pore formation by promoting functional inactivation of envelope glycoproteins","volume":"292","author":"Sood","year":"2017","journal-title":"J. Biol. Chem."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"e2101450118","DOI":"10.1073\/pnas.2101450118","article-title":"HIV envelope tail truncation confers resistance to SERINC5 restriction","volume":"118","author":"Haider","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"e02214-16","DOI":"10.1128\/JVI.02214-16","article-title":"Effect of HIV-1 Env on SERINC5 Antagonism","volume":"91","author":"Beitari","year":"2017","journal-title":"J. Virol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e00594-20","DOI":"10.1128\/JVI.00594-20","article-title":"SERINC5 Inhibits HIV-1 Infectivity by Altering the Conformation of gp120 on HIV-1 Particles","volume":"94","author":"Featherstone","year":"2020","journal-title":"J. Virol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"15183","DOI":"10.1074\/jbc.RA120.014466","article-title":"HIV-cell membrane fusion intermediates are restricted by Serincs as revealed by cryo-electron and TIRF microscopy","volume":"295","author":"Ward","year":"2020","journal-title":"J. Biol. Chem."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e00544-19","DOI":"10.1128\/JVI.00544-19","article-title":"CD4 Expression and Env Conformation Are Critical for HIV-1 Restriction by SERINC5","volume":"93","author":"Zhang","year":"2019","journal-title":"J. Virol."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Chen, Y.C., Sood, C., Marin, M., Aaron, J., Chew, T.L., Salaita, K., and Melikyan, G.B. (2020). 3D Superresolution Studies of the Effect of SERINC5 on Env Glycoprotein Distribution on HIV-1 Particles. Biophys. J., 118.","DOI":"10.1016\/j.bpj.2019.11.944"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"773","DOI":"10.1021\/acsinfecdis.2c00478","article-title":"Serinc5 Restricts HIV Membrane Fusion by Altering Lipid Order and Heterogeneity in the Viral Membrane","volume":"9","author":"Ward","year":"2023","journal-title":"ACS Infect. Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"13702","DOI":"10.1074\/jbc.M117.797332","article-title":"The host-cell restriction factor SERINC5 restricts HIV-1 infectivity without altering the lipid composition and organization of viral particles","volume":"292","author":"Trautz","year":"2017","journal-title":"J. Biol. Chem."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Raghunath, G., Chen, Y.C., Marin, M., Wu, H., and Melikyan, G.B. (2022). SERINC5-Mediated Restriction of HIV-1 Infectivity Correlates with Resistance to Cholesterol Extraction but Not with Lipid Order of Viral Membrane. Viruses, 14.","DOI":"10.3390\/v14081636"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"4368","DOI":"10.1038\/s41467-023-39262-2","article-title":"Antiviral HIV-1 SERINC restriction factors disrupt virus membrane asymmetry","volume":"14","author":"Leonhardt","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"6745","DOI":"10.1021\/jp900913w","article-title":"Flip-Flop of Phospholipids in Vesicles: Kinetic Analysis with Time-Resolved Small-Angle Neutron Scattering","volume":"113","author":"Nakano","year":"2009","journal-title":"J. Phys. Chem. B"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2361","DOI":"10.1021\/bi00656a018","article-title":"Transbilayer Phospholipid Asymmetry and Its Maintenance in Membrane of Influenza-Virus","volume":"15","author":"Rothman","year":"1976","journal-title":"Biochemistry"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1021\/bi00570a024","article-title":"Compositional Asymmetry and Transmembrane Movement of Phosphatidylcholine in Vesicular Stomatitis-Virus Membranes","volume":"18","author":"Shaw","year":"1979","journal-title":"Biochemistry"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1974","DOI":"10.1021\/bi00510a037","article-title":"Phospholipid Asymmetry in Semliki Forest Virus Grown on Baby Hamster-Kidney (Bhk-21) Cells","volume":"20","author":"Simons","year":"1981","journal-title":"Biochemistry"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Urbancic, I., Brun, J., Shrestha, D., Waithe, D., Eggeling, C., and Chojnacki, J. (2018). Lipid Composition but Not Curvature Is the Determinant Factor for the Low Molecular Mobility Observed on the Membrane of Virus-Like Vesicles. Viruses, 10.","DOI":"10.3390\/v10080415"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Bryer, A.J., Reddy, T., Lyman, E., and Perilla, J.R. (2022). Full scale structural, mechanical and dynamical properties of HIV-1 liposomes. PLoS Comput. Biol., 18.","DOI":"10.1371\/journal.pcbi.1009781"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1038\/s41467-017-00515-6","article-title":"Envelope glycoprotein mobility on HIV-1 particles depends on the virus maturation state","volume":"8","author":"Chojnacki","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1038\/nrmicro3469","article-title":"Viral apoptotic mimicry","volume":"13","author":"Amara","year":"2015","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Reyes Ballista, J.M., Miazgowicz, K.L., Acciani, M.D., Jimenez, A.R., Belloli, R.S., Havranek, K.E., and Brindley, M.A. (2023). Chikungunya virus entry and infectivity is primarily facilitated through cell line dependent attachment factors in mammalian and mosquito cells. Front. Cell Dev. Biol., 11.","DOI":"10.3389\/fcell.2023.1085913"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"4840","DOI":"10.4049\/jimmunol.170.9.4840","article-title":"Phosphatidylserine on HIV envelope is a cofactor for infection of monocytic cells","volume":"170","author":"Callahan","year":"2003","journal-title":"J. Immunol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.chom.2017.06.012","article-title":"Fusion Stage of HIV-1 Entry Depends on Virus-Induced Cell Surface Exposure of Phosphatidylserine","volume":"22","author":"Zaitseva","year":"2017","journal-title":"Cell Host Microbe"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"2281","DOI":"10.1038\/nprot.2013.143","article-title":"Genome engineering using the CRISPR-Cas9 system","volume":"8","author":"Ran","year":"2013","journal-title":"Nat. Protoc."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1038\/335181a0","article-title":"Immunodeficiency Virus Rev Trans-Activator Modulates the Expression of the Viral Regulatory Genes","volume":"335","author":"Malim","year":"1988","journal-title":"Nature"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"20196","DOI":"10.1074\/jbc.M117.818088","article-title":"An improved labeling strategy enables automated detection of single-virus fusion and assessment of HIV-1 protease activity in single virions","volume":"292","author":"Sood","year":"2017","journal-title":"J. Biol. Chem."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"834","DOI":"10.1038\/nature09583","article-title":"Calcium-dependent phospholipid scrambling by TMEM16F","volume":"468","author":"Suzuki","year":"2010","journal-title":"Nature"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"6558","DOI":"10.1074\/jbc.M114.623181","article-title":"Distinct Requirements for HIV-Cell Fusion and HIV-mediated Cell-Cell Fusion","volume":"290","author":"Kondo","year":"2015","journal-title":"J. Biol. Chem."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"8036","DOI":"10.1016\/j.vaccine.2007.09.016","article-title":"Advances in methods for the production, purification, and characterization of HIV-1 Gag-Env pseudovirion vaccines","volume":"25","author":"Hammonds","year":"2007","journal-title":"Vaccine"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"5580","DOI":"10.1002\/anie.200351866","article-title":"Self-assembled microarrays of attoliter molecular vessels","volume":"42","author":"Stamou","year":"2003","journal-title":"Angew. Chem. Int. Ed."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"22238","DOI":"10.1074\/jbc.M109.029256","article-title":"Probing HIV-1 Membrane Liquid Order by Laurdan Staining Reveals Producer Cell-dependent Differences","volume":"284","author":"Lorizate","year":"2009","journal-title":"J. Biol. Chem."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"690","DOI":"10.1038\/nmeth.2075","article-title":"Icy: An open bioimage informatics platform for extended reproducible research","volume":"9","author":"Dallongeville","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/0022-1759(95)00072-I","article-title":"A Novel Assay for Apoptosis\u2014Flow Cytometric Detection of Phosphatidylserine Expression on Early Apoptotic Cells Using Fluorescein-Labeled Annexin-V","volume":"184","author":"Vermes","year":"1995","journal-title":"J. Immunol. Methods"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/(SICI)1097-0320(19980101)31:1<1::AID-CYTO1>3.0.CO;2-R","article-title":"Annexin V-affinity assay: A review on an apoptosis detection system based on phosphatidylserine exposure","volume":"31","author":"Nieland","year":"1998","journal-title":"Cytometry"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1038\/s41467-018-07962-9","article-title":"Molecular recognition of the native HIV-1 MPER revealed by STED microscopy of single virions","volume":"10","author":"Carravilla","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"11288","DOI":"10.1074\/jbc.272.17.11288","article-title":"Interaction of biotin with streptavidin\u2014Thermostability and conformational changes upon binding","volume":"272","author":"Gonzalez","year":"1997","journal-title":"J. Biol. Chem."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Kirschman, J., Marin, M., Chen, Y.C., Chen, J.H., Herschhorn, A., Smith, A.B., and Melikyan, G.B. (2022). SERINC5 Restricts HIV-1 Infectivity by Promoting Conformational Changes and Accelerating Functional Inactivation of Env. Viruses, 14.","DOI":"10.3390\/v14071388"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"C723","DOI":"10.1152\/ajpcell.00462.2010","article-title":"A practical guide to evaluating colocalization in biological microscopy","volume":"300","author":"Dunn","year":"2011","journal-title":"Am. J. Physiol. Cell Physiol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1188","DOI":"10.1128\/iai.63.4.1188-1194.1995","article-title":"Binding, Oligomerization, and Pore Formation by Streptolysin-O in Erythrocytes and Fibroblast Membranes\u2014Detection of Nonlytic Polymers","volume":"63","author":"Walev","year":"1995","journal-title":"Infect. Immun."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"5953","DOI":"10.1128\/jb.175.18.5953-5961.1993","article-title":"A Ring-Shaped Structure with a Crown Formed by Streptolysin-O on the Erythrocyte-Membrane","volume":"175","author":"Sekiya","year":"1993","journal-title":"J. Bacteriol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"3867","DOI":"10.1002\/j.1460-2075.1990.tb07605.x","article-title":"The Crystal and Molecular-Structure of Human Annexin-V, an Anticoagulant Protein That Binds to Calcium and Membranes","volume":"9","author":"Huber","year":"1990","journal-title":"EMBO J."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Pennington, H.N., and Lee, J. (2022). Lassa virus glycoprotein complex review: Insights into its unique fusion machinery. Biosci. Rep., 42.","DOI":"10.1042\/BSR20211930"},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Suddala, K.C., Lee, C.C., Meraner, P., Marin, M., Markosyan, R.M., Desai, T.M., Cohen, F.S., Brass, A.L., and Melikyan, G.B. (2019). Interferon-induced transmembrane protein 3 blocks fusion of sensitive but not resistant viruses by partitioning into virus-carrying endosomes. PLoS Pathog., 15.","DOI":"10.1371\/journal.ppat.1007532"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"19246","DOI":"10.1073\/pnas.1114799108","article-title":"Constitutive exposure of phosphatidylserine on viable cells","volume":"108","author":"Segawa","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_61","first-page":"S335","article-title":"Role of Transmembrane Protein 16F in the Incorporation of Phosphatidylserine Into Budding Ebola Virus Virions","volume":"218","author":"Younan","year":"2018","journal-title":"J. Infect. Dis."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1006\/viro.1998.9398","article-title":"HIV-1 Gag proteins: Diverse functions in the virus life cycle","volume":"251","author":"Freed","year":"1998","journal-title":"Virology"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"700","DOI":"10.1126\/science.abe6821","article-title":"Maturation of the matrix and viral membrane of HIV-1","volume":"373","author":"Qu","year":"2021","journal-title":"Science"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/1742-4690-10-4","article-title":"Virion stiffness regulates immature HIV-1 entry","volume":"10","author":"Pang","year":"2013","journal-title":"Retrovirology"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"3620","DOI":"10.1128\/AAC.00055-12","article-title":"Activity of Human Immunodeficiency Virus Type 1 Protease Inhibitors against the Initial Autocleavage in Gag-Pol Polyprotein Processing","volume":"56","author":"Davis","year":"2012","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1089\/aid.2011.0230","article-title":"HIV Type 1 Gag as a Target for Antiviral Therapy","volume":"28","author":"Waheed","year":"2012","journal-title":"AIDS Res. Hum. Retroviruses"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"e0116521","DOI":"10.1128\/JVI.01165-21","article-title":"Ebola Virus Requires Phosphatidylserine Scrambling Activity for Efficient Budding and Optimal Infectivity","volume":"95","author":"Acciani","year":"2021","journal-title":"J. Virol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1164","DOI":"10.1126\/science.1252809","article-title":"Caspase-mediated cleavage of phospholipid flippase for apoptotic phosphatidylserine exposure","volume":"344","author":"Segawa","year":"2014","journal-title":"Science"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1508","DOI":"10.1021\/acsinfecdis.3c00063","article-title":"Peptidomimetic Oligomers Targeting Membrane Phosphatidylserine Exhibit Broad Antiviral Activity","volume":"9","author":"Tate","year":"2023","journal-title":"ACS Infect. Dis."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"2253","DOI":"10.1097\/00002030-200211220-00004","article-title":"Virion-associated cholesterol is critical for the maintenance of HIV-1 structure and infectivity","volume":"16","author":"Campbell","year":"2002","journal-title":"AIDS"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"14025","DOI":"10.1073\/pnas.1610705113","article-title":"Efficient replacement of plasma membrane outer leaflet phospholipids and sphingolipids in cells with exogenous lipids","volume":"113","author":"Li","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"14631","DOI":"10.1021\/la4031427","article-title":"Effect of Cyclodextrin and Membrane Lipid Structure upon Cyclodextrin-Lipid Interaction","volume":"29","author":"Huang","year":"2013","journal-title":"Langmuir"},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Suresh, P., and London, E. (2022). Using cyclodextrin-induced lipid substitution to study membrane lipid and ordered membrane domain (raft) function in cells. BBA-Biomembranes, 1864.","DOI":"10.1016\/j.bbamem.2021.183774"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1038\/s41467-019-14045-w","article-title":"Annexin-V stabilizes membrane defects by inducing lipid phase transition","volume":"11","author":"Lin","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1038\/s41594-019-0357-0","article-title":"A bipartite structural organization defines the SERINC family of HIV-1 restriction factors","volume":"27","author":"Pye","year":"2020","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_76","first-page":"122a","article-title":"Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 gag targeting to the plasma membrane","volume":"15","author":"Ono","year":"2004","journal-title":"Mol. Biol. Cell"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"e2219475120","DOI":"10.1073\/pnas.2219475120","article-title":"Neutral sphingomyelinase 2 is required for HIV-1 maturation","volume":"120","author":"Waheed","year":"2023","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1906","DOI":"10.1126\/science.1111781","article-title":"Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies","volume":"308","author":"Haynes","year":"2005","journal-title":"Science"}],"container-title":["Biomolecules"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2218-273X\/14\/5\/570\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:43:58Z","timestamp":1760107438000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2218-273X\/14\/5\/570"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,5,10]]},"references-count":78,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2024,5]]}},"alternative-id":["biom14050570"],"URL":"https:\/\/doi.org\/10.3390\/biom14050570","relation":{},"ISSN":["2218-273X"],"issn-type":[{"value":"2218-273X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,5,10]]}}}