{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,27]],"date-time":"2026-08-27T23:12:19Z","timestamp":1787872339378,"version":"build-2784847793"},"reference-count":72,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2024,2,15]],"date-time":"2024-02-15T00:00:00Z","timestamp":1707955200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"BBSRC","award":["BB\/P003966\/1"],"award-info":[{"award-number":["BB\/P003966\/1"]}]},{"name":"BBSRC","award":["BB\/P013740\/1"],"award-info":[{"award-number":["BB\/P013740\/1"]}]},{"name":"BBSRC","award":["BB\/P013759\/1"],"award-info":[{"award-number":["BB\/P013759\/1"]}]},{"name":"BBSRC strategic","award":["BB\/P003966\/1"],"award-info":[{"award-number":["BB\/P003966\/1"]}]},{"name":"BBSRC strategic","award":["BB\/P013740\/1"],"award-info":[{"award-number":["BB\/P013740\/1"]}]},{"name":"BBSRC strategic","award":["BB\/P013759\/1"],"award-info":[{"award-number":["BB\/P013759\/1"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>To identify host factors that affect Bovine Herpes Virus Type 1 (BoHV-1) infection we previously applied a genome wide CRISPR knockout screen targeting all bovine protein coding genes. By doing so we compiled a list of both pro-viral and anti-viral proteins involved in BoHV-1 replication. Here we provide further analysis of those that are potentially involved in viral entry into the host cell. We first generated single cell knockout clones deficient in some of the candidate genes for validation. We provide evidence that Polio Virus Receptor-related protein (PVRL2) serves as a receptor for BoHV-1, mediating more efficient entry than the previously identified Polio Virus Receptor (PVR). By knocking out two enzymes that catalyze HSPG chain elongation, HST2ST1 and GLCE, we further demonstrate the significance of HSPG in BoHV-1 entry. Another intriguing cluster of candidate genes, COG1, COG2 and COG4-7 encode six subunits of the Conserved Oligomeric Golgi (COG) complex. MDBK cells lacking COG6 produced fewer but bigger plaques compared to control cells, suggesting more efficient release of newly produced virions from these COG6 knockout cells, due to impaired HSPG biosynthesis. We further observed that viruses produced by the COG6 knockout cells consist of protein(s) with reduced N-glycosylation, potentially explaining their lower infectivity. To facilitate candidate validation, we also detailed a one-step multiplex CRISPR interference (CRISPRi) system, an orthogonal method to KO that enables quick and simultaneous deployment of three CRISPRs for efficient gene inactivation. Using CRISPR3i, we verified eight candidates that have been implicated in the synthesis of surface heparan sulfate proteoglycans (HSPGs). In summary, our experiments confirmed the two receptors PVR and PVRL2 for BoHV-1 entry into the host cell and other factors that affect this process, likely through the direct or indirect roles they play during HSPG synthesis and glycosylation of viral proteins.<\/jats:p>","DOI":"10.3390\/v16020297","type":"journal-article","created":{"date-parts":[[2024,2,15]],"date-time":"2024-02-15T05:55:59Z","timestamp":1707976559000},"page":"297","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Validation of Candidate Host Cell Entry Factors for Bovine Herpes Virus Type-1 Based on a Genome-Wide CRISPR Knockout Screen"],"prefix":"10.3390","volume":"16","author":[{"given":"Wenfang Spring","family":"Tan","sequence":"first","affiliation":[{"name":"Division of Infection and Immunity, the Roslin Institute, Easter Bush Campus, University of Edinburgh, Edinburgh EH259RG, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Enguang","family":"Rong","sequence":"additional","affiliation":[{"name":"Division of Infection and Immunity, the Roslin Institute, Easter Bush Campus, University of Edinburgh, Edinburgh EH259RG, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Inga","family":"Dry","sequence":"additional","affiliation":[{"name":"Division of Infection and Immunity, the Roslin Institute, Easter Bush Campus, University of Edinburgh, Edinburgh EH259RG, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Simon","family":"Lillico","sequence":"additional","affiliation":[{"name":"Division of Functional Genetics and Development, the Roslin Institute, Easter Bush Campus, University of Edinburgh, Edinburgh EH259RG, UK"},{"name":"Centre for Tropical Livestock Genetics and Health, the Roslin Institute, Easter Bush Campus, University of Edinburgh, Edinburgh EH259RG, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1868-2364","authenticated-orcid":false,"given":"Andy","family":"Law","sequence":"additional","affiliation":[{"name":"Division of Genetics and Genomics, the Roslin Institute, Easter Bush Campus, University of Edinburgh, Edinburgh EH259RG, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0872-9440","authenticated-orcid":false,"given":"Paul","family":"Digard","sequence":"additional","affiliation":[{"name":"Division of Infection and Immunity, the Roslin Institute, Easter Bush Campus, University of Edinburgh, Edinburgh EH259RG, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bruce","family":"Whitelaw","sequence":"additional","affiliation":[{"name":"Division of Functional Genetics and Development, the Roslin Institute, Easter Bush Campus, University of Edinburgh, Edinburgh EH259RG, UK"},{"name":"Division of Genetics and Genomics, the Roslin Institute, Easter Bush Campus, University of Edinburgh, Edinburgh EH259RG, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert G.","family":"Dalziel","sequence":"additional","affiliation":[{"name":"Division of Infection and Immunity, the Roslin Institute, Easter Bush Campus, University of Edinburgh, Edinburgh EH259RG, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,2,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1017\/S146625230700134X","article-title":"A review of the biology of bovine herpesvirus type 1 (BHV-1), its role as a cofactor in the bovine respiratory disease complex and development of improved vaccines","volume":"8","author":"Jones","year":"1996","journal-title":"Anim. Health Res. Rev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/S0378-1135(96)01232-1","article-title":"Immunology of bovine herpesvirus 1 infection","volume":"53","author":"Babiuk","year":"1996","journal-title":"Veter. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1017\/S1466252307001326","article-title":"Immune evasion by pathogens of bovine respiratory disease complex","volume":"8","author":"Srikumaran","year":"1996","journal-title":"Anim. Health Res. Rev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"e00839-18","DOI":"10.1128\/JVI.00839-18","article-title":"Bovine Herpesvirus 1 Entry by a Low-pH Endosomal Pathway","volume":"92","author":"Pastenkos","year":"2018","journal-title":"J. Virol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1124","DOI":"10.1128\/jvi.65.3.1124-1132.1991","article-title":"Bovine herpesvirus 1 attachment to permissive cells is mediated by its major glycoproteins gI, gIII, and gIV","volume":"65","author":"Liang","year":"1991","journal-title":"J. Virol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"4758","DOI":"10.1128\/jvi.69.8.4758-4768.1995","article-title":"Characterization of cell-binding properties of bovine herpesvirus 1 glycoproteins B, C, and D: Identification of a dual cell-binding function of gB","volume":"69","author":"Li","year":"1995","journal-title":"J. Virol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1016\/0042-6822(92)90586-E","article-title":"An in vivo study of a glycoprotein gIII-negative bovine herpesvirus 1 (BHV-1) mutant expressing \u03b2-galactosidase: Evaluation of the role of gIII in virus infectivity and its use as a vector for mucosal immunization","volume":"189","author":"Liang","year":"1992","journal-title":"Virology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"666","DOI":"10.1016\/0042-6822(91)90900-V","article-title":"BHV-1 Adsorption is mediated by the interaction of glycoprotein gIII with heparinlike moiety on the cell surface","volume":"181","author":"Okazaki","year":"1991","journal-title":"Virology"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1128\/JVI.79.2.791-799.2005","article-title":"Engineering Glycoprotein B of Bovine Herpesvirus 1 To Function as Transporter for Secreted Proteins: A New Protein Expression Approach","volume":"79","author":"Keil","year":"2005","journal-title":"J. Virol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1006\/viro.1996.8372","article-title":"Functional analysis of the transmembrane anchor region of bovine herpesvirus 1 glycoprotein gB","volume":"228","author":"Li","year":"1997","journal-title":"Virology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1186\/s13567-014-0111-x","article-title":"Bovine herpesvirus glycoprotein D: A review of its structural characteristics and applications in vaccinology","volume":"45","year":"2014","journal-title":"Vet. Res."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"4866","DOI":"10.1128\/jvi.64.10.4866-4872.1990","article-title":"Bovine cells expressing bovine herpesvirus 1 (BHV-1) glycoprotein IV resist infection by BHV-1, herpes simplex virus, and pseudorabies virus","volume":"64","author":"Chase","year":"1990","journal-title":"J. Virol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1623","DOI":"10.1099\/0022-1317-76-7-1623","article-title":"Unidirectional complementation, between glycoprotein B homologues of pseudorabies virus and bovine herpesvirus 1 is determined by the carboxy-terminal part of the molecule","volume":"76","author":"Miethke","year":"1995","journal-title":"J. Gen. Virol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1002\/1099-1654(200009\/10)10:5<305::AID-RMV286>3.0.CO;2-T","article-title":"The novel receptors that mediate the entry of herpes simplex viruses and animal alphaherpesviruses into cells","volume":"10","author":"Cocchi","year":"2000","journal-title":"Rev. Med. Virol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1006\/viro.2000.0529","article-title":"Three classes of cell surface receptors for alphaherpesvirus entry","volume":"275","author":"Spear","year":"2000","journal-title":"Virology"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1618","DOI":"10.1126\/science.280.5369.1618","article-title":"Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor","volume":"280","author":"Geraghty","year":"1998","journal-title":"Science"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4520","DOI":"10.1128\/JVI.02601-08","article-title":"Entry of Herpes Simplex Virus 1 and Other Alphaherpesviruses via the Paired Immunoglobulin-Like Type 2 Receptor \u03b1","volume":"83","author":"Arii","year":"2009","journal-title":"J. Virol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1515","DOI":"10.1099\/0022-1317-77-7-1515","article-title":"Glycoprotein H (gII\/gp108) and glycoprotein L form a functional complex which plays a role in penetration, but not in attachment, of bovine herpesvirus 1","volume":"77","author":"Khattar","year":"1996","journal-title":"J. Gen. Virol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3435","DOI":"10.1128\/jvi.63.8.3435-3443.1989","article-title":"Neutralizing antibodies specific for glycoprotein H of herpes simplex virus permit viral attachment to cells but prevent penetration","volume":"63","author":"Fuller","year":"1989","journal-title":"J. Virol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1983","DOI":"10.1099\/0022-1317-79-8-1983","article-title":"Bovine herpesvirus type 1 glycoprotein H is essential for penetration and propagation in cell culture","volume":"79","author":"Meyer","year":"1998","journal-title":"J. Gen. Virol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1006\/viro.1996.0223","article-title":"Identification and characterization of a bovine herpesvirus-1 (BHV-1) glycoprotein gL which is required for proper antigenicity, processing, and transport of BHV-1 glycoprotein gH","volume":"219","author":"Khattar","year":"1996","journal-title":"Virology"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1099\/0022-1317-80-1-57","article-title":"Bovine herpesvirus 1 requires glycoprotein H for infectivity and direct spreading and glycoproteins gHW450 and gB for glycoprotein D-independent cell-to-cell spread","volume":"80","author":"Keil","year":"1999","journal-title":"J. Gen. Virol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1006\/viro.1998.9218","article-title":"A cell surface protein with herpesvirus entry activity (Hveb) confers susceptibility to infection by mutants of herpes simplex virus type 1, herpes simplex virus type 2, and pseudorabies virus","volume":"246","author":"Warner","year":"1998","journal-title":"Virology"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"12940","DOI":"10.1128\/JVI.76.24.12940-12950.2002","article-title":"Mutations in the N-Terminal Domains of Nectin-1 and Nectin-2 Reveal Differences in Requirements for Entry of Various Alphaherpesviruses and for Nectin-Nectin Interactions","volume":"76","author":"Struyf","year":"2002","journal-title":"J. Virol."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Sarrazin, S., Lamanna, W.C., and Esko, J.D. (2011). Heparan sulfate proteoglycans. Cold Spring Harb. Perspect. Biol., 3.","DOI":"10.1101\/cshperspect.a004952"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"8193","DOI":"10.1021\/acs.chemrev.6b00010","article-title":"Chemical Synthesis of Glycosaminoglycans","volume":"116","author":"Mende","year":"2016","journal-title":"Chem. Rev."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Cagno, V., Tseligka, E.D., Jones, S.T., and Tapparel, C. (2019). Heparan sulfate proteoglycans and viral attachment: True receptors or adaptation bias?. Viruses, 11.","DOI":"10.3390\/v11070596"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"10508","DOI":"10.1128\/JVI.74.22.10508-10513.2000","article-title":"Glycosaminoglycan Sulfation Requirements for Respiratory Syncytial Virus Infection","volume":"74","author":"Hallak","year":"2000","journal-title":"J. Virol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"12714","DOI":"10.1128\/JVI.00717-09","article-title":"Heparan Sulfate Proteoglycans Are Required for Cellular Binding of the Hepatitis E Virus ORF2 Capsid Protein and for Viral Infection","volume":"83","author":"Kalia","year":"2009","journal-title":"J. Virol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/S0092-8674(00)80058-6","article-title":"A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry","volume":"99","author":"Shukla","year":"1999","journal-title":"Cell"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1007\/978-1-4939-1714-3_45","article-title":"Role of glycosaminoglycans in infectious disease","volume":"Volume 1229","author":"Jinno","year":"2015","journal-title":"Glycosaminoglycans"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1006\/viro.1995.1184","article-title":"Evidence for an Interaction of Herpes Simplex Virus with Chondroitin Sulfate Proteoglycans during Infection","volume":"208","author":"Banfield","year":"1995","journal-title":"Virology"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"38668","DOI":"10.1074\/jbc.M609320200","article-title":"Chondroitin 4-O-sulfotransferase-1 regulates E disaccharide expression of chondroitin sulfate required for herpes simplex virus infectivity","volume":"281","author":"Uyama","year":"2006","journal-title":"J. Biol. Chem."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.csbj.2014.05.003","article-title":"Structure and function of nucleotide sugar transporters: Current progress","volume":"10","author":"Hadley","year":"2014","journal-title":"Comput. Struct. Biotechnol. J."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"26265","DOI":"10.1074\/jbc.273.41.26265","article-title":"The putative tumor suppressors EXT1 and EXT2 are glycosyltransferases required for the biosynthesis of heparan sulfate","volume":"273","author":"Lind","year":"1998","journal-title":"J. Biol. Chem."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Fisher, P., and Ungar, D. (2016). Bridging the gap between glycosylation and vesicle traffic. Front. Cell Develop. Biol., 4.","DOI":"10.3389\/fcell.2016.00015"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2466","DOI":"10.1002\/1873-3468.13570","article-title":"Maintaining order: COG complex controls Golgi trafficking, processing, and sorting","volume":"593","author":"Blackburn","year":"2019","journal-title":"FEBS Lett."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.ymgme.2007.08.118","article-title":"Deficiencies in subunits of the Conserved Oligomeric Golgi (COG) complex define a novel group of Congenital Disorders of Glycosylation","volume":"93","author":"Zeevaert","year":"2008","journal-title":"Mol. Genet. Metab."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1038\/nm1041","article-title":"Mutation of the COG complex subunit gene COG7 causes a lethal congenital disorder","volume":"10","author":"Wu","year":"2004","journal-title":"Nat. Med."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1083\/jcb.200202016","article-title":"Characterization of a mammalian Golgi-localized protein complex, COG, that is required for normal Golgi morphology and function","volume":"157","author":"Ungar","year":"2002","journal-title":"J. Cell Biol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1576","DOI":"10.1083\/jcb.102.5.1576","article-title":"Three types of low density lipoprotein receptor-deficient mutant have pleiotropic defects in the synthesis of N-linked, O-linked, and lipid-linked carbohydrate chains","volume":"102","author":"Kingsley","year":"1986","journal-title":"J. Cell Biol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"16526","DOI":"10.1073\/pnas.1310478110","article-title":"Efficient nonmeiotic allele introgression in livestock using custom endonucleases","volume":"110","author":"Tan","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"e82","DOI":"10.1093\/nar\/gkr218","article-title":"Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting","volume":"39","author":"Cermak","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1126\/science.1231143","article-title":"Multiplex genome engineering using CRISPR\/Cas systems","volume":"339","author":"Cong","year":"2013","journal-title":"Science"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"957","DOI":"10.1038\/nmeth.2649","article-title":"Cas9 as a versatile tool for engineering biology","volume":"10","author":"Mali","year":"2013","journal-title":"Nat. Methods"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"e00471","DOI":"10.7554\/eLife.00471","article-title":"RNA-programmed genome editing in human cells","volume":"2013","author":"Jinek","year":"2013","journal-title":"eLife"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1038\/ng.3741","article-title":"A genome-wide CRISPR screen identifies a restricted set of HIV host dependency factors","volume":"49","author":"Park","year":"2017","journal-title":"Nat. Genet."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"9527","DOI":"10.1073\/pnas.1900867116","article-title":"Genome-wide CRISPR screen for Zika virus resistance in human neural cells","volume":"116","author":"Li","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Tan, W.S., Rong, E., Dry, I., Lillico, S.G., Law, A., Digard, P., Whitelaw, B., and Dalziel, R.G. (2023). GARP and EARP are required for efficient BoHV-1 replication as identified by a genome wide CRISPR knockout screen. PLOS Pathog., 19.","DOI":"10.1371\/journal.ppat.1011822"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1038\/s41467-019-13965-x","article-title":"Genome-wide CRISPR screen identifies host dependency factors for influenza A virus infection","volume":"11","author":"Li","year":"2020","journal-title":"Nat Commun"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1038\/nature14136","article-title":"Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex","volume":"517","author":"Konermann","year":"2015","journal-title":"Nature"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1038\/s41592-018-0048-5","article-title":"An enhanced CRISPR repressor for targeted mammalian gene regulation","volume":"15","author":"Yeo","year":"2018","journal-title":"Nat. Methods"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1128\/JVI.79.2.1071-1083.2005","article-title":"Impairment of nuclear pores in bovine herpesvirus 1-infected MDBK cells","volume":"79","author":"Wild","year":"2005","journal-title":"J. Virol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1093\/nar\/gku936","article-title":"Easy quantitative assessment of genome editing by sequence trace decomposition","volume":"42","author":"Brinkman","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1038\/s41592-018-0086-z","article-title":"The GAGOme: A cell-based library of displayed glycosaminoglycans","volume":"15","author":"Chen","year":"2018","journal-title":"Nat. Methods"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"e00432-17","DOI":"10.1128\/JVI.00432-17","article-title":"Genome-Wide Screening Uncovers the Significance of N-Sulfation of Heparan Sulfate as a Host Cell Factor for Chikungunya Virus Infection","volume":"91","author":"Tanaka","year":"2017","journal-title":"J. Virol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1126\/science.1233675","article-title":"Deciphering the glycosylome of dystroglycanopathies using haploid screens for Lassa virus entry","volume":"340","author":"Jae","year":"2013","journal-title":"Science"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1414","DOI":"10.1128\/JVI.02055-15","article-title":"A Haploid Genetic Screen Identifies Heparan Sulfate Proteoglycans Supporting Rift Valley Fever Virus Infection","volume":"90","author":"Riblett","year":"2016","journal-title":"J. Virol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"e02160-18","DOI":"10.1128\/JVI.02160-18","article-title":"A Genome-Wide Haploid Genetic Screen Identifies Heparan Sulfate-Associated Genes and the Macropinocytosis Modulator TMED10 as Factors Supporting Vaccinia Virus Infection","volume":"93","author":"Luteijn","year":"2019","journal-title":"J. Virol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"3218","DOI":"10.1038\/s41467-019-11056-5","article-title":"Dopey1-Mon2 complex binds to dual-lipids and recruits kinesin-1 for membrane trafficking","volume":"10","author":"Mahajan","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"7176","DOI":"10.1073\/pnas.131188498","article-title":"Human tumor suppressor EXT gene family members EXTL1 and EXTL3 encode \u03b11,4-N-acetylglucosaminyltransferases that likely are involved in heparan sulfate\/heparin biosynthesis","volume":"98","author":"Kim","year":"2001","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"12984","DOI":"10.1073\/pnas.241175798","article-title":"Enzyme interactions in heparan sulfate biosynthesis: Uronosyl 5-epimerase and 2-O-sulfotransferase interact in vivo","volume":"98","author":"Pinhal","year":"2001","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1099\/0022-1317-83-2-291","article-title":"Herpes simplex virus type 1 glycoprotein C is necessary for efficient infection of chondroitin sulfate-expressing gro2C cells","volume":"83","author":"Trybala","year":"2002","journal-title":"J. Gen. Virol."},{"key":"ref_64","first-page":"324","article-title":"Malignant catarrhal fever: A review","volume":"179","author":"Russell","year":"2009","journal-title":"Veter. J."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1554","DOI":"10.1093\/glycob\/cwr028","article-title":"Conserved oligomeric Golgi complex specifically regulates the maintenance of Golgi glycosylation machinery","volume":"21","author":"Pokrovskaya","year":"2011","journal-title":"Glycobiology"},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Burkard, C., Lillico, S.G., Reid, E., Jackson, B., Mileham, A.J., Ait-Ali, T., Whitelaw, C.B.A., and Archibald, A.L. (2017). Precision engineering for PRRSV resistance in pigs: Macrophages from genome edited pigs lacking CD163 SRCR5 domain are fully resistant to both PRRSV genotypes while maintaining biological function. PLOS Pathog., 13.","DOI":"10.1371\/journal.ppat.1006206"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1038\/nbt.3434","article-title":"Gene-edited pigs are protected from porcine reproductive and respiratory syndrome virus","volume":"34","author":"Whitworth","year":"2016","journal-title":"Nat. Biotechnol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1007\/s11248-018-0100-3","article-title":"Resistance to coronavirus infection in amino peptidase N-deficient pigs","volume":"28","author":"Whitworth","year":"2019","journal-title":"Transgenic Res."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"6985","DOI":"10.1038\/ncomms7985","article-title":"Heparanase is a host enzyme required for herpes simplex virus-1 release from cells","volume":"6","author":"Hadigal","year":"2015","journal-title":"Nat. Commun."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"e01179-18","DOI":"10.1128\/JVI.01179-18","article-title":"Host Enzymes Heparanase and Cathepsin L Promote Herpes Simplex Virus 2 Release from Cells","volume":"92","author":"Hopkins","year":"2018","journal-title":"J. Virol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1111\/tra.12564","article-title":"More than just sugars: Conserved oligomeric Golgi complex deficiency causes glycosylation-independent cellular defects","volume":"19","author":"Blackburn","year":"2018","journal-title":"Traffic"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"668","DOI":"10.3389\/fgene.2019.00668","article-title":"A Gene Expression Atlas of the Domestic Water Buffalo (Bubalus bubalis)","volume":"10","author":"Young","year":"2019","journal-title":"Front. Genet."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/16\/2\/297\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:00:09Z","timestamp":1760104809000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/16\/2\/297"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,2,15]]},"references-count":72,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2024,2]]}},"alternative-id":["v16020297"],"URL":"https:\/\/doi.org\/10.3390\/v16020297","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,2,15]]}}}