{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T00:21:06Z","timestamp":1789172466193,"version":"build-2803163510"},"update-to":[{"DOI":"10.1371\/journal.ppat.1011204","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2023,6,21]],"date-time":"2023-06-21T00:00:00Z","timestamp":1687305600000}}],"reference-count":101,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2023,6,8]],"date-time":"2023-06-08T00:00:00Z","timestamp":1686182400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/publicdomain\/zero\/1.0\/"}],"funder":[{"DOI":"10.13039\/100005825","name":"National Institute of Food and Agriculture","doi-asserted-by":"publisher","award":["2013-67015-26787"],"award-info":[{"award-number":["2013-67015-26787"]}],"id":[{"id":"10.13039\/100005825","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100005825","name":"National Institute of Food and Agriculture","doi-asserted-by":"publisher","award":["2016-67015-26777"],"award-info":[{"award-number":["2016-67015-26777"]}],"id":[{"id":"10.13039\/100005825","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100005825","name":"National Institute of Food and Agriculture","doi-asserted-by":"publisher","award":["2020-67015-21399"],"award-info":[{"award-number":["2020-67015-21399"]}],"id":[{"id":"10.13039\/100005825","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100005825","name":"National Institute of Food and Agriculture","doi-asserted-by":"publisher","award":["58-6040-8-037"],"award-info":[{"award-number":["58-6040-8-037"]}],"id":[{"id":"10.13039\/100005825","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100005825","name":"National Institute of Food and Agriculture","doi-asserted-by":"publisher","award":["58-6040-0-015"],"award-info":[{"award-number":["58-6040-0-015"]}],"id":[{"id":"10.13039\/100005825","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p>Efficient transmission of herpesviruses is essential for dissemination in host populations; however, little is known about the viral genes that mediate transmission, mostly due to a lack of natural virus-host model systems. Marek\u2019s disease is a devastating herpesviral disease of chickens caused by Marek\u2019s disease virus (MDV) and an excellent natural model to study skin-tropic herpesviruses and transmission. Like varicella zoster virus that causes chicken pox in humans, the only site where infectious cell-free MD virions are efficiently produced is in epithelial skin cells, a requirement for host-to-host transmission. Here, we enriched for heavily infected feather follicle epithelial skin cells of live chickens to measure both viral transcription and protein expression using combined short- and long-read RNA sequencing and LC\/MS-MS bottom-up proteomics. Enrichment produced a previously unseen breadth and depth of viral peptide sequencing. We confirmed protein translation for 84 viral genes at high confidence (1% FDR) and correlated relative protein abundance with RNA expression levels. Using a proteogenomic approach, we confirmed translation of most well-characterized spliced viral transcripts and identified a novel, abundant isoform of the 14 kDa transcript family via IsoSeq transcripts, short-read intron-spanning sequencing reads, and a high-quality junction-spanning peptide identification. We identified peptides representing alternative start codon usage in several genes and putative novel microORFs at the 5\u2019 ends of two core herpesviral genes, pUL47 and ICP4, along with strong evidence of independent transcription and translation of the capsid scaffold protein pUL26.5. Using a natural animal host model system to examine viral gene expression provides a robust, efficient, and meaningful way of validating results gathered from cell culture systems.<\/jats:p>","DOI":"10.1371\/journal.ppat.1011204","type":"journal-article","created":{"date-parts":[[2023,6,8]],"date-time":"2023-06-08T13:51:57Z","timestamp":1686232317000},"page":"e1011204","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":21,"title":["Viral proteogenomic and expression profiling during productive replication of a skin-tropic herpesvirus in the natural host"],"prefix":"10.1371","volume":"19","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8892-7155","authenticated-orcid":true,"given":"Jeremy D.","family":"Volkening","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1545-5855","authenticated-orcid":true,"given":"Stephen J.","family":"Spatz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4697-1502","authenticated-orcid":true,"given":"Nagendraprabhu","family":"Ponnuraj","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4379-7091","authenticated-orcid":true,"given":"Haji","family":"Akbar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1511-8805","authenticated-orcid":true,"given":"Justine V.","family":"Arrington","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7589-2328","authenticated-orcid":true,"given":"Widaliz","family":"Vega-Rodriguez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0391-9018","authenticated-orcid":true,"given":"Keith W.","family":"Jarosinski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2023,6,8]]},"reference":[{"key":"ppat.1011204.ref001","first-page":"2501","volume-title":"Fields Virology","author":"B Roizman","year":"2007","edition":"5"},{"issue":"3","key":"ppat.1011204.ref002","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1637\/aviandiseases-D-21-00022","article-title":"Cell-to-Cell Transmission of Turkey Herpesvirus in Chicken Embryo Cells via Tunneling Nanotubes","volume":"65","author":"T Okura","year":"2021","journal-title":"Avian Dis"},{"issue":"12","key":"ppat.1011204.ref003","article-title":"Release of HSV-1 Cell-Free Virions: Mechanisms, Regulation, and Likely Role in Human-Human Transmission","volume":"13","author":"SA Rice","year":"2021","journal-title":"Viruses"},{"issue":"1\u20132","key":"ppat.1011204.ref004","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/S0378-1135(01)00492-8","article-title":"Evolution of the herpesviruses","volume":"86","author":"AJ Davison","year":"2002","journal-title":"Vet Microbiol"},{"issue":"1","key":"ppat.1011204.ref005","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0166-3542(02)00107-9","article-title":"Fundamental and accessory systems in herpesviruses","volume":"56","author":"AJ Davison","year":"2002","journal-title":"Antiviral Res"},{"issue":"1","key":"ppat.1011204.ref006","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1186\/s12985-015-0458-2","article-title":"Keratinocytes derived from chicken embryonic stem cells support Marek\u2019s disease virus infection: a highly differentiated cell model to study viral replication and morphogenesis","volume":"13","author":"M Couteaudier","year":"2016","journal-title":"Virol J"},{"issue":"3","key":"ppat.1011204.ref007","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1080\/03079457.2018.1556385","article-title":"Suspension culture of Marek\u2019s disease virus and evaluation of its immunological effects","volume":"48","author":"L Wen","year":"2019","journal-title":"Avian pathology: journal of the WVPA"},{"issue":"4","key":"ppat.1011204.ref008","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1637\/7182-032604R","article-title":"Quail cell lines supporting replication of Marek\u2019s disease virus serotype 1 and 2 and herpesvirus of turkeys","volume":"48","author":"X Li","year":"2004","journal-title":"Avian Dis"},{"issue":"2 Suppl","key":"ppat.1011204.ref009","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1637\/10344-090312-Reg.1","article-title":"Efficacy and safety of cell-associated vaccines against Marek\u2019s disease virus grown in QT35 cells or JBJ-1 cells","volume":"57","author":"H Geerligs","year":"2013","journal-title":"Avian Dis"},{"issue":"44","key":"ppat.1011204.ref010","doi-asserted-by":"crossref","first-page":"5595","DOI":"10.1016\/j.vaccine.2008.07.080","article-title":"Efficacy and safety of cell associated vaccines against Marek\u2019s disease virus grown in a continuous cell line from chickens","volume":"26","author":"H Geerligs","year":"2008","journal-title":"Vaccine"},{"issue":"2","key":"ppat.1011204.ref011","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1006\/viro.1995.0065","article-title":"Development of a sustainable chick cell line infected with Marek\u2019s disease virus","volume":"214","author":"A Abujoub","year":"1995","journal-title":"Virology"},{"issue":"2","key":"ppat.1011204.ref012","doi-asserted-by":"crossref","first-page":"219","DOI":"10.2307\/1588466","article-title":"Feather follicle epithelium: a source of enveloped and infectious cell-free herpesvirus from Marek\u2019s disease","volume":"14","author":"BW Calnek","year":"1970","journal-title":"Avian Dis"},{"issue":"19","key":"ppat.1011204.ref013","doi-asserted-by":"crossref","first-page":"10575","DOI":"10.1128\/JVI.01065-07","article-title":"Horizontal transmission of Marek\u2019s disease virus requires US2, the UL13 protein kinase, and gC","volume":"81","author":"KW Jarosinski","year":"2007","journal-title":"J Virol"},{"key":"ppat.1011204.ref014","volume-title":"Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis","author":"J Moffat","year":"2007"},{"issue":"10","key":"ppat.1011204.ref015","doi-asserted-by":"crossref","first-page":"1145","DOI":"10.2217\/fvl.15.85","article-title":"Cell entry mechanisms of HSV: what we have learned in recent years","volume":"10","author":"AM Agelidis","year":"2015","journal-title":"Future Virol"},{"issue":"17","key":"ppat.1011204.ref016","doi-asserted-by":"crossref","first-page":"7980","DOI":"10.1128\/JVI.74.17.7980-7988.2000","article-title":"The genome of a very virulent Marek\u2019s disease virus","volume":"74","author":"ER Tulman","year":"2000","journal-title":"J Virol"},{"issue":"11","key":"ppat.1011204.ref017","doi-asserted-by":"crossref","first-page":"6091","DOI":"10.1073\/pnas.97.11.6091","article-title":"The complete unique long sequence and the overall genomic organization of the GA strain of Marek\u2019s disease virus","volume":"97","author":"LF Lee","year":"2000","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ppat.1011204.ref018","first-page":"17","volume-title":"Marek\u2019s disease. Biology of Animal Infection","author":"N Osterrieder","year":"2004"},{"issue":"3","key":"ppat.1011204.ref019","doi-asserted-by":"crossref","DOI":"10.3390\/v12030329","article-title":"Pervasive Differential Splicing in Marek\u2019s Disease Virus can Discriminate CVI-988 Vaccine Strain from RB-1B Very Virulent Strain in Chicken Embryonic Fibroblasts","volume":"12","author":"Y Sadigh","year":"2020","journal-title":"Viruses"},{"issue":"3","key":"ppat.1011204.ref020","doi-asserted-by":"crossref","DOI":"10.3390\/v11030264","article-title":"The Transcriptional Landscape of Marek\u2019s Disease Virus in Primary Chicken B Cells Reveals Novel Splice Variants and Genes","volume":"11","author":"LD Bertzbach","year":"2019","journal-title":"Viruses"},{"key":"ppat.1011204.ref021","doi-asserted-by":"crossref","first-page":"109882","DOI":"10.1016\/j.vetimm.2019.109882","article-title":"RNA-seq analysis of viral gene expression in the skin of Marek\u2019s disease virus infected chickens","volume":"213","author":"L Sunkaraa","year":"2019","journal-title":"Vet Immunol Immunopathol"},{"issue":"8","key":"ppat.1011204.ref022","doi-asserted-by":"crossref","first-page":"1316","DOI":"10.1002\/pmic.200600946","article-title":"Modeling the proteome of a Marek\u2019s disease transformed cell line: a natural animal model for CD30 overexpressing lymphomas","volume":"7","author":"JJ Buza","year":"2007","journal-title":"Proteomics"},{"issue":"1","key":"ppat.1011204.ref023","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/j.jviromet.2006.02.001","article-title":"A mass spectrometry-based proteomic approach to study Marek\u2019s Disease Virus gene expression","volume":"135","author":"HC Liu","year":"2006","journal-title":"J Virol Methods"},{"issue":"5","key":"ppat.1011204.ref024","doi-asserted-by":"crossref","first-page":"2428","DOI":"10.1128\/JVI.06719-11","article-title":"Fluorescently tagged pUL47 of Marek\u2019s disease virus reveals differential tissue expression of the tegument protein in vivo","volume":"86","author":"KW Jarosinski","year":"2012","journal-title":"J Virol"},{"issue":"15","key":"ppat.1011204.ref025","doi-asserted-by":"crossref","first-page":"7896","DOI":"10.1128\/JVI.00908-12","article-title":"Marek\u2019s disease virus expresses multiple UL44 (gC) variants through mRNA splicing that are all required for efficient horizontal transmission","volume":"86","author":"KW Jarosinski","year":"2012","journal-title":"J Virol"},{"issue":"4","key":"ppat.1011204.ref026","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1637\/10252-052212-Reg.1","article-title":"Marek\u2019s disease virus late protein expression in feather follicle epithelial cells as early as 8 days postinfection","volume":"56","author":"KW Jarosinski","year":"2012","journal-title":"Avian Dis"},{"issue":"4","key":"ppat.1011204.ref027","doi-asserted-by":"crossref","first-page":"1820","DOI":"10.1021\/pr301157j","article-title":"Proteomics analysis of herpes simplex virus type 1-infected cells reveals dynamic changes of viral protein expression, ubiquitylation, and phosphorylation","volume":"12","author":"C Bell","year":"2013","journal-title":"J Proteome Res"},{"key":"ppat.1011204.ref028","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.3389\/fmicb.2020.01179","article-title":"Analysis of Virus and Host Proteomes During Productive HSV-1 and VZV Infection in Human Epithelial Cells","volume":"11","author":"WJD Ouwendijk","year":"2020","journal-title":"Front Microbiol"},{"issue":"W1","key":"ppat.1011204.ref029","doi-asserted-by":"crossref","first-page":"W12","DOI":"10.1093\/nar\/gkx428","article-title":"CPC2: a fast and accurate coding potential calculator based on sequence intrinsic features","volume":"45","author":"YJ Kang","year":"2017","journal-title":"Nucleic Acids Res"},{"issue":"15","key":"ppat.1011204.ref030","doi-asserted-by":"crossref","first-page":"e0013121","DOI":"10.1128\/JVI.00131-21","article-title":"The Marek\u2019s Disease Virus Unique Gene MDV082 Is Dispensable for Virus Replication but Contributes to a Rapid Disease Onset","volume":"95","author":"Y You","year":"2021","journal-title":"J Virol"},{"issue":"3","key":"ppat.1011204.ref031","doi-asserted-by":"crossref","first-page":"690","DOI":"10.1128\/jvi.54.3.690-696.1985","article-title":"Genomic expansion of Marek\u2019s disease virus DNA is associated with serial in vitro passage","volume":"54","author":"RF Silva","year":"1985","journal-title":"J Virol"},{"issue":"1","key":"ppat.1011204.ref032","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1128\/JVI.78.1.424-440.2004","article-title":"Complete, annotated sequence of the pseudorabies virus genome","volume":"78","author":"BG Klupp","year":"2004","journal-title":"J Virol"},{"key":"ppat.1011204.ref033","article-title":"Identifying and quantifying isoforms from accurate full-length transcriptome sequencing reads with Mandalorion","author":"R Volden","year":"2022","journal-title":"BioRxiv"},{"issue":"10","key":"ppat.1011204.ref034","doi-asserted-by":"crossref","first-page":"1555","DOI":"10.1093\/bioinformatics\/btw024","article-title":"TFBSTools: an R\/bioconductor package for transcription factor binding site analysis","volume":"32","author":"G Tan","year":"2016","journal-title":"Bioinformatics"},{"issue":"8","key":"ppat.1011204.ref035","doi-asserted-by":"crossref","first-page":"R78","DOI":"10.1186\/gb-2006-7-8-r78","article-title":"Transcriptional and structural impact of TATA-initiation site spacing in mammalian core promoters","volume":"7","author":"J Ponjavic","year":"2006","journal-title":"Genome biology"},{"issue":"6","key":"ppat.1011204.ref036","doi-asserted-by":"crossref","first-page":"626","DOI":"10.1038\/ng1789","article-title":"Genome-wide analysis of mammalian promoter architecture and evolution","volume":"38","author":"P Carninci","year":"2006","journal-title":"Nature genetics"},{"issue":"21","key":"ppat.1011204.ref037","doi-asserted-by":"crossref","first-page":"2755","DOI":"10.1101\/gad.11.21.2755","article-title":"Mechanism and regulation of mRNA polyadenylation","volume":"11","author":"DF Colgan","year":"1997","journal-title":"Genes & development"},{"issue":"7","key":"ppat.1011204.ref038","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1080\/15476286.2017.1306171","article-title":"Cleavage and polyadenylation: Ending the message expands gene regulation","volume":"14","author":"J Neve","year":"2017","journal-title":"RNA Biol"},{"issue":"11","key":"ppat.1011204.ref039","doi-asserted-by":"crossref","first-page":"e79511","DOI":"10.1371\/journal.pone.0079511","article-title":"RNA polyadenylation sites on the genomes of microorganisms, animals, and plants","volume":"8","author":"XQ Li","year":"2013","journal-title":"PLoS One"},{"issue":"2\u20134","key":"ppat.1011204.ref040","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1016\/j.vetmic.2006.06.019","article-title":"Expression of Marek\u2019s disease virus phosphorylated polypeptide pp38 produces splice variants and enhances metabolic activity","volume":"117","author":"X Li","year":"2006","journal-title":"Vet Microbiol"},{"issue":"1","key":"ppat.1011204.ref041","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1007\/s11262-006-0004-9","article-title":"Multiple alternative splicing to exons II and III of viral interleukin-8 (vIL-8) in the Marek\u2019s disease virus genome: the importance of vIL-8 exon I","volume":"34","author":"KW Jarosinski","year":"2007","journal-title":"Virus Genes"},{"issue":"11","key":"ppat.1011204.ref042","doi-asserted-by":"crossref","first-page":"5159","DOI":"10.1128\/JVI.75.11.5159-5173.2001","article-title":"Marek\u2019s disease virus (MDV) encodes an interleukin-8 homolog (vIL-8): characterization of the vIL-8 protein and a vIL-8 deletion mutant MDV","volume":"75","author":"MS Parcells","year":"2001","journal-title":"J Virol"},{"issue":"2","key":"ppat.1011204.ref043","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1006\/viro.1996.0388","article-title":"Isolation and characterization of Marek\u2019s disease virus (MDV) cDNAs from a MDV-transformed lymphoblastoid cell line: identification of an open reading frame antisense to the MDV Eco-Q protein (Meq)","volume":"221","author":"Q Peng","year":"1996","journal-title":"Virology"},{"issue":"2","key":"ppat.1011204.ref044","doi-asserted-by":"crossref","first-page":"1353","DOI":"10.1128\/jvi.71.2.1353-1361.1997","article-title":"Marek\u2019s disease virus latency-associated transcripts belong to a family of spliced RNAs that are antisense to the ICP4 homolog gene","volume":"71","author":"JL Cantello","year":"1997","journal-title":"J Virol"},{"issue":"2","key":"ppat.1011204.ref045","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1006\/viro.1995.0031","article-title":"Isolation and characterization of Marek\u2019s disease virus (MDV) cDNAs mapping to the BamHI-I2, BamHI-Q2, and BamHI-L fragments of the MDV genome from lymphoblastoid cells transformed and persistently infected with MDV","volume":"213","author":"Q Peng","year":"1995","journal-title":"Virology"},{"issue":"6","key":"ppat.1011204.ref046","doi-asserted-by":"crossref","first-page":"3593","DOI":"10.1128\/jvi.68.6.3593-3603.1994","article-title":"Identification of an immediate-early gene in the Marek\u2019s disease virus long internal repeat region which encodes a unique 14-kilodalton polypeptide","volume":"68","author":"Y Hong","year":"1994","journal-title":"J Virol"},{"issue":"9","key":"ppat.1011204.ref047","doi-asserted-by":"crossref","first-page":"e108475","DOI":"10.1371\/journal.pone.0108475","article-title":"Natural variability of Kozak sequences correlates with function in a zebrafish model","volume":"9","author":"SJ Grzegorski","year":"2014","journal-title":"PLoS One"},{"key":"ppat.1011204.ref048","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1002\/cpps.29","article-title":"N-Terminal Methionine Processing","volume":"88","author":"PT Wingfield","year":"2017","journal-title":"Curr Protoc Protein Sci"},{"issue":"15","key":"ppat.1011204.ref049","doi-asserted-by":"crossref","first-page":"7443","DOI":"10.1128\/JVI.00388-08","article-title":"Herpes simplex virus type 1 ICP27 regulates expression of a variant, secreted form of glycoprotein C by an intron retention mechanism","volume":"82","author":"L Sedlackova","year":"2008","journal-title":"J Virol"},{"issue":"2 Suppl","key":"ppat.1011204.ref050","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1637\/10414-100612-Reg.1","article-title":"Importance of differential expression of Marek\u2019s disease virus gene pp38 for the pathogenesis of Marek\u2019s disease","volume":"57","author":"KA Schat","year":"2013","journal-title":"Avian Dis"},{"issue":"12","key":"ppat.1011204.ref051","doi-asserted-by":"crossref","first-page":"7362","DOI":"10.1128\/jvi.66.12.7362-7367.1992","article-title":"3rd. Herpes simplex virus type 1 protease expressed in Escherichia coli exhibits autoprocessing and specific cleavage of the ICP35 assembly protein","volume":"66","author":"IC Deckman","year":"1992","journal-title":"J Virol"},{"issue":"3","key":"ppat.1011204.ref052","doi-asserted-by":"crossref","first-page":"1300","DOI":"10.1128\/jvi.67.3.1300-1309.1993","article-title":"Characterization of the protease and other products of amino-terminus-proximal cleavage of the herpes simplex virus 1 UL26 protein","volume":"67","author":"F Liu","year":"1993","journal-title":"J Virol"},{"issue":"10","key":"ppat.1011204.ref053","doi-asserted-by":"crossref","first-page":"5813","DOI":"10.1128\/jvi.67.10.5813-5822.1993","article-title":"Autoproteolysis of herpes simplex virus type 1 protease releases an active catalytic domain found in intermediate capsid particles","volume":"67","author":"SP Weinheimer","year":"1993","journal-title":"J Virol"},{"issue":"3","key":"ppat.1011204.ref054","doi-asserted-by":"crossref","first-page":"2048","DOI":"10.1016\/S0021-9258(18)53960-0","article-title":"Identification of the herpes simplex virus-1 protease cleavage sites by direct sequence analysis of autoproteolytic cleavage products","volume":"268","author":"CL DiIanni","year":"1993","journal-title":"The Journal of biological chemistry"},{"issue":"6","key":"ppat.1011204.ref055","doi-asserted-by":"crossref","first-page":"3702","DOI":"10.1128\/jvi.68.6.3702-3712.1994","article-title":"The protease of herpes simplex virus type 1 is essential for functional capsid formation and viral growth","volume":"68","author":"M Gao","year":"1994","journal-title":"J Virol"},{"issue":"Pt 10","key":"ppat.1011204.ref056","doi-asserted-by":"crossref","first-page":"2709","DOI":"10.1099\/0022-1317-73-10-2709","article-title":"Identification of genes encoding two capsid proteins (VP24 and VP26) of herpes simplex virus type 1","volume":"73","author":"MD Davison","year":"1992","journal-title":"J Gen Virol"},{"issue":"1","key":"ppat.1011204.ref057","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/S0378-1119(99)00368-6","article-title":"The molecular biology of the CCAAT-binding factor NF-Y","volume":"239","author":"R. Mantovani","year":"1999","journal-title":"Gene"},{"issue":"10","key":"ppat.1011204.ref058","doi-asserted-by":"crossref","first-page":"5149","DOI":"10.1128\/jvi.65.10.5149-5156.1991","article-title":"The herpes simplex virus 1 gene encoding a protease also contains within its coding domain the gene encoding the more abundant substrate","volume":"65","author":"FY Liu","year":"1991","journal-title":"J Virol"},{"issue":"2","key":"ppat.1011204.ref059","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1128\/jvi.58.2.657-660.1986","article-title":"Amplification of a tandem direct repeat within inverted repeats of Marek\u2019s disease virus DNA during serial in vitro passage","volume":"58","author":"K Maotani","year":"1986","journal-title":"J Virol"},{"issue":"12","key":"ppat.1011204.ref060","doi-asserted-by":"crossref","first-page":"7389","DOI":"10.1128\/jvi.66.12.7389-7396.1992","article-title":"Isolation and characterization of cDNAs from BamHI-H gene family RNAs associated with the tumorigenicity of Marek\u2019s disease virus","volume":"66","author":"F Peng","year":"1992","journal-title":"J Virol"},{"issue":"2","key":"ppat.1011204.ref061","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1128\/JVI.78.2.733-740.2004","article-title":"Expansion of a unique region in the Marek\u2019s disease virus genome occurs concomitantly with attenuation but is not sufficient to cause attenuation","volume":"78","author":"RF Silva","year":"2004","journal-title":"J Virol"},{"issue":"9","key":"ppat.1011204.ref062","doi-asserted-by":"crossref","first-page":"1963","DOI":"10.1021\/ac026359i","article-title":"Cleavage N-terminal to proline: analysis of a database of peptide tandem mass spectra","volume":"75","author":"LA Breci","year":"2003","journal-title":"Analytical chemistry"},{"issue":"17","key":"ppat.1011204.ref063","doi-asserted-by":"crossref","first-page":"8778","DOI":"10.1128\/JVI.00831-06","article-title":"Marek\u2019s disease virus encodes MicroRNAs that map to meq and the latency-associated transcript","volume":"80","author":"J Burnside","year":"2006","journal-title":"J Virol"},{"issue":"13","key":"ppat.1011204.ref064","doi-asserted-by":"crossref","first-page":"7164","DOI":"10.1128\/JVI.00112-07","article-title":"Marek\u2019s disease virus type 2 (MDV-2)-encoded microRNAs show no sequence conservation with those encoded by MDV-1","volume":"81","author":"Y Yao","year":"2007","journal-title":"J Virol"},{"issue":"24","key":"ppat.1011204.ref065","doi-asserted-by":"crossref","first-page":"12769","DOI":"10.1128\/JVI.01010-09","article-title":"The 5\u2019 leader of the mRNA encoding the marek\u2019s disease virus serotype 1 pp14 protein contains an intronic internal ribosome entry site with allosteric properties","volume":"83","author":"A Tahiri-Alaoui","year":"2009","journal-title":"J Virol"},{"key":"ppat.1011204.ref066","article-title":"Marek\u2019s Disease Virus Virulence Genes Encode Circular RNAs","author":"AS Chasseur","year":"2022","journal-title":"J Virol"},{"issue":"Pt 7","key":"ppat.1011204.ref067","doi-asserted-by":"crossref","first-page":"1581","DOI":"10.1099\/vir.0.000128","article-title":"A comparison of herpes simplex virus type 1 and varicella-zoster virus latency and reactivation","volume":"96","author":"PG Kennedy","year":"2015","journal-title":"J Gen Virol"},{"issue":"46","key":"ppat.1011204.ref068","doi-asserted-by":"crossref","first-page":"16286","DOI":"10.1073\/pnas.0407320101","article-title":"Proteins of purified Epstein-Barr virus","volume":"101","author":"E Johannsen","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"17","key":"ppat.1011204.ref069","doi-asserted-by":"crossref","first-page":"8605","DOI":"10.1128\/JVI.00904-08","article-title":"Comprehensive characterization of extracellular herpes simplex virus type 1 virions","volume":"82","author":"S Loret","year":"2008","journal-title":"J Virol"},{"key":"ppat.1011204.ref070","unstructured":"Technical Overview: Iso-Seq Express Library Preparation Using SMRTbell Express Template Prep Kit 2.0 (white paper). 2021."},{"key":"ppat.1011204.ref071","unstructured":"Tseng E. Discover Full-Length RNA Sequencing\u2013No Assembly Required [Video]. 2019 [updated Nov. 7, 2019]. 1:00:16]. Available from: https:\/\/www.youtube.com\/watch?v=qz0tR7TFfcc&t=163s."},{"issue":"2","key":"ppat.1011204.ref072","doi-asserted-by":"crossref","first-page":"e1010959","DOI":"10.1371\/journal.ppat.1010959","article-title":"The alphaherpesvirus conserved pUS10 is important for natural infection and its expression is regulated by the conserved Herpesviridae protein kinase (CHPK)","volume":"19","author":"N Ponnuraj","year":"2023","journal-title":"PLoS Pathog"},{"issue":"4","key":"ppat.1011204.ref073","doi-asserted-by":"crossref","first-page":"e01903","DOI":"10.1128\/JVI.01903-18","article-title":"The Herpesviridae Conserved Multifunctional Infected-Cell Protein 27 (ICP27) Is Important but Not Required for Replication and Oncogenicity of Marek\u2019s Disease Alphaherpesvirus","volume":"93","author":"N Ponnuraj","year":"2019","journal-title":"J Virol"},{"issue":"4","key":"ppat.1011204.ref074","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1080\/03079458208436134","article-title":"Characterisation of two highly oncogenic strains of Marek\u2019s disease virus","volume":"11","author":"KA Schat","year":"1982","journal-title":"Avian pathology : journal of the WVPA"},{"key":"ppat.1011204.ref075","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.virol.2019.06.008","article-title":"Marek\u2019s disease alphaherpesvirus (MDV) RLORF4 is not required for expression of glycoprotein C and interindividual spread","volume":"534","author":"W Vega-Rodriguez","year":"2019","journal-title":"Virology"},{"issue":"5","key":"ppat.1011204.ref076","doi-asserted-by":"crossref","first-page":"e01522","DOI":"10.1128\/JVI.01522-19","article-title":"Expression of the Conserved Herpesvirus Protein Kinase (CHPK) of Marek\u2019s Disease Alphaherpesvirus in the Skin Reveals a Mechanistic Importance for CHPK during Interindividual Spread in Chickens","volume":"94","author":"A Krieter","year":"2020","journal-title":"J Virol"},{"issue":"1","key":"ppat.1011204.ref077","doi-asserted-by":"crossref","first-page":"7753","DOI":"10.1038\/s41598-021-87400-x","article-title":"The requirement of glycoprotein C (gC) for interindividual spread is a conserved function of gC for avian herpesviruses","volume":"11","author":"W Vega-Rodriguez","year":"2021","journal-title":"Scientific reports"},{"issue":"8","key":"ppat.1011204.ref078","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1038\/s41587-019-0201-4","article-title":"Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype","volume":"37","author":"D Kim","year":"2019","journal-title":"Nat Biotechnol"},{"issue":"16","key":"ppat.1011204.ref079","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","article-title":"The Sequence Alignment\/Map format and SAMtools","volume":"25","author":"H Li","year":"2009","journal-title":"Bioinformatics"},{"key":"ppat.1011204.ref080","article-title":"RegTools: Integrated analysis of genomic and transcriptomic data for the discovery of splicing variants in cancer","author":"KC Cotto","journal-title":"BioRxiv"},{"issue":"16","key":"ppat.1011204.ref081","doi-asserted-by":"crossref","first-page":"2184","DOI":"10.1093\/bioinformatics\/bts356","article-title":"RSeQC: quality control of RNA-seq experiments","volume":"28","author":"L Wang","year":"2012","journal-title":"Bioinformatics"},{"issue":"6","key":"ppat.1011204.ref082","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1093\/bioinformatics\/btq033","article-title":"BEDTools: a flexible suite of utilities for comparing genomic features","volume":"26","author":"AR Quinlan","year":"2010","journal-title":"Bioinformatics"},{"issue":"6","key":"ppat.1011204.ref083","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v032.i06","article-title":"mixtools: An R Package for Analyzing Mixture Models","volume":"32","author":"T Benaglia","year":"2009","journal-title":"Journal of Statistical Software"},{"issue":"7","key":"ppat.1011204.ref084","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1038\/s41592-018-0046-7","article-title":"Bioconda: sustainable and comprehensive software distribution for the life sciences","volume":"15","author":"B Gruning","year":"2018","journal-title":"Nature methods"},{"issue":"3","key":"ppat.1011204.ref085","doi-asserted-by":"crossref","first-page":"396","DOI":"10.1101\/gr.222976.117","article-title":"SQANTI: extensive characterization of long-read transcript sequences for quality control in full-length transcriptome identification and quantification","volume":"28","author":"M Tardaguila","year":"2018","journal-title":"Genome research"},{"key":"ppat.1011204.ref086","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-319-24277-4","volume-title":"ggplot2 : Elegant Graphics for Data Analysis","author":"H. Wickham","year":"2016"},{"issue":"1","key":"ppat.1011204.ref087","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1101\/gad.293837.116","article-title":"The human initiator is a distinct and abundant element that is precisely positioned in focused core promoters","volume":"31","author":"L Vo Ngoc","year":"2017","journal-title":"Genes & development"},{"issue":"3","key":"ppat.1011204.ref088","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1038\/nmeth.2834","article-title":"Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells","volume":"11","author":"NA Kulak","year":"2014","journal-title":"Nature methods"},{"issue":"8","key":"ppat.1011204.ref089","doi-asserted-by":"crossref","first-page":"1896","DOI":"10.1038\/nprot.2007.261","article-title":"Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips","volume":"2","author":"J Rappsilber","year":"2007","journal-title":"Nature protocols"},{"issue":"1","key":"ppat.1011204.ref090","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1002\/pmic.201200439","article-title":"Comet: an open-source MS\/MS sequence database search tool","volume":"13","author":"JK Eng","year":"2013","journal-title":"Proteomics"},{"key":"ppat.1011204.ref091","doi-asserted-by":"crossref","first-page":"5277","DOI":"10.1038\/ncomms6277","article-title":"MS-GF+ makes progress towards a universal database search tool for proteomics","volume":"5","author":"S Kim","year":"2014","journal-title":"Nat Commun"},{"issue":"11","key":"ppat.1011204.ref092","doi-asserted-by":"crossref","first-page":"1719","DOI":"10.1007\/s13361-016-1460-7","article-title":"Fast and Accurate Protein False Discovery Rates on Large-Scale Proteomics Data Sets with Percolator 3.0","volume":"27","author":"M The","year":"2016","journal-title":"Journal of the American Society for Mass Spectrometry"},{"issue":"10","key":"ppat.1011204.ref093","doi-asserted-by":"crossref","first-page":"4488","DOI":"10.1021\/pr500741y","article-title":"Crux: rapid open source protein tandem mass spectrometry analysis","volume":"13","author":"S McIlwain","year":"2014","journal-title":"J Proteome Res"},{"issue":"2","key":"ppat.1011204.ref094","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1093\/bib\/bbs017","article-title":"Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration","volume":"14","author":"H Thorvaldsdottir","year":"2013","journal-title":"Brief Bioinform"},{"issue":"1","key":"ppat.1011204.ref095","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1021\/acs.jproteome.7b00608","article-title":"Ultrafast Peptide Label-Free Quantification with FlashLFQ","volume":"17","author":"RJ Millikin","year":"2018","journal-title":"J Proteome Res"},{"issue":"1","key":"ppat.1011204.ref096","doi-asserted-by":"crossref","DOI":"10.1093\/bioinformatics\/btac830","article-title":"igv.js: an embeddable JavaScript implementation of the Integrative Genomics Viewer (IGV)","volume":"39","author":"JT Robinson","year":"2023","journal-title":"Bioinformatics"},{"issue":"6","key":"ppat.1011204.ref097","doi-asserted-by":"crossref","first-page":"1188","DOI":"10.1101\/gr.849004","article-title":"WebLogo: a sequence logo generator","volume":"14","author":"GE Crooks","year":"2004","journal-title":"Genome research"},{"key":"ppat.1011204.ref098","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1007\/978-1-4939-3578-9_16","article-title":"Visualizing Genomic Data Using Gviz and Bioconductor","volume":"1418","author":"F Hahne","year":"2016","journal-title":"Methods in molecular biology"},{"key":"ppat.1011204.ref099","author":"Team RC","year":"2022","journal-title":"R: A language and environment for statistical computing Vienna, Austria: R Foundation for Statistical Computing"},{"issue":"2","key":"ppat.1011204.ref100","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1093\/bioinformatics\/btr645","article-title":"MSnbase-an R\/Bioconductor package for isobaric tagged mass spectrometry data visualization, processing and quantitation","volume":"28","author":"L Gatto","year":"2012","journal-title":"Bioinformatics"},{"issue":"9","key":"ppat.1011204.ref101","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1038\/nmeth.3959","article-title":"OpenMS: a flexible open-source software platform for mass spectrometry data analysis","volume":"13","author":"HL Rost","year":"2016","journal-title":"Nature methods"}],"updated-by":[{"DOI":"10.1371\/journal.ppat.1011204","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2023,6,21]],"date-time":"2023-06-21T00:00:00Z","timestamp":1687305600000}}],"container-title":["PLOS Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1011204","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,6,21]],"date-time":"2023-06-21T20:13:19Z","timestamp":1687378399000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1011204"}},"subtitle":[],"editor":[{"given":"Donna M.","family":"Neumann","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2023,6,8]]},"references-count":101,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2023,6,8]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.ppat.1011204","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2023.02.13.528429","asserted-by":"object"}]},"ISSN":["1553-7374"],"issn-type":[{"value":"1553-7374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,8]]}}}