The genome of human papillomavirus type 23 (HPV-23; family Papillomaviridae, genus Betapapillomavirus, species Betapapillomavirus 2, type 23) was assembled by deep sequencing from nasopharyngeal swabs. The assembled genome

is 2.7% divergent over its full length from the single complete genome of HPV-23 in GenBank (accession no. U31781). We named the strain HPV-23/Lancaster/201

Atkinson, Kate V.

Bishop, Lisa A.

Gatherer, Derek

Harding, Nicola

Hegarty, Matthew

Lauder, Robert M.

McEwan, Neil

Pickup, Roger W.

Rhodes, Glenn

Robey, Julie

Salez, Nicolas

Wetherell, Simon

Wilkinson, Mark

English

ABSTRACT
          
            The genome of human papillomavirus type 23 (HPV-23; family
            Papillomaviridae
            , genus
            Betapapillomavirus
            , species
            Betapapillomavirus 2
            , type 23) was assembled by deep sequencing from nasopharyngeal swabs. The assembled genome is 2.7% divergent over its full length from the single complete genome of HPV-23 in GenBank (accession no. U31781). We named the strain HPV-23/Lancaster/2015.
          </jats:p

Kate V. Atkinson

Lisa A. Bishop

Glenn Rhodes

Nicolas Salez

Neil R. McEwan

Matthew J. Hegarty

Julie Robey

Nicola Harding

Simon Wetherell

Robert M. Lauder

Roger W. Pickup

Mark Wilkinson

Derek Gatherer

Crossref

Genome Announcements

Genome Sequence of Human Papillomavirus 23 Strain HPV-23/Lancaster/2015

The genome of human papillomavirus type 23 (HPV-23; family Papillomaviridae, genus Betapapillomavirus, species Betapapillomavirus 2, type 23) was assembled by deep sequencing from nasopharyngeal swabs. The assembled genome is 2.7% divergent over its full length from the single complete genome of HPV-23 in GenBank (accession no. U31781). We named the strain HPV-23/Lancaster/201

Aberystwyth Research Portal

Aberystwyth UniversityGenome Sequence of Human Papillomavirus 23 Strain HPV-23/Lancaster/2015Atkinson, Kate V.; Bishop, Lisa A.; Rhodes, Glenn; Salez, Nicolas; McEwan, Neil; Hegarty, Matthew; Robey,Julie; Harding, Nicola; Wetherell, Simon; Lauder, Robert M.; Pickup, Roger W.; Wilkinson, Mark; Gatherer,DerekPublished in:Genome AnnouncementsDOI:10.1128/genomeA.00257-17Publication date:2017Citation for published version (APA):Atkinson, K. V., Bishop, L. A., Rhodes, G., Salez, N., McEwan, N., Hegarty, M., ... Gatherer, D. (2017). GenomeSequence of Human Papillomavirus 23 Strain HPV-23/Lancaster/2015. Genome Announcements, 5(20),[e00257-17]. https://doi.org/10.1128/genomeA.00257-17Document LicenseCC BYGeneral rightsCopyright and moral rights for the publications made accessible in the Aberystwyth Research Portal (the Institutional Repository) areretained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by thelegal requirements associated with these rights.            • Users may download and print one copy of any publication from the Aberystwyth Research Portal for the purpose of private study orresearch.            • You may not further distribute the material or use it for any profit-making activity or commercial gain            • You may freely distribute the URL identifying the publication in the Aberystwyth Research PortalTake down policyIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediatelyand investigate your claim.tel: +44 1970 62 2400email: is@aber.ac.ukDownload date: 03. Oct. 2019Genome Sequence of HumanPapillomavirus 23 StrainHPV-23/Lancaster/2015Kate V. Atkinson,a* Lisa A. Bishop,a,b Glenn Rhodes,c Nicolas Salez,dNeil R. McEwan,e Matthew J. Hegarty,e Julie Robey,f Nicola Harding,fSimon Wetherell,f Robert M. Lauder,a Roger W. Pickup,a,c Mark Wilkinson,bDerek GathereraDivision of Biomedical & Life Sciences, Faculty of Health & Medicine, Lancaster University, Lancaster, UnitedKingdoma; Royal Lancaster Inﬁrmary, Lancaster, United Kingdomb; Centre for Ecology & Hydrology, LakeEcosystems Group, Lancaster Environment Centre, Lancaster University, Lancaster, United Kingdomc; UMR_D190, Emergence des Pathologies Virales, Aix-Marseille University, Marseille, Franced; Institute of Biological,Environmental & Rural Sciences, Aberystwyth University, Aberystwyth, United Kingdome; Queen SquareMedical Practice, Lancaster, United KingdomfABSTRACT The genome of human papillomavirus type 23 (HPV-23; family Papillo-maviridae, genus Betapapillomavirus, species Betapapillomavirus 2, type 23) was as-sembled by deep sequencing from nasopharyngeal swabs. The assembled genomeis 2.7% divergent over its full length from the single complete genome of HPV-23 inGenBank (accession no. U31781). We named the strain HPV-23/Lancaster/2015.The family Papillomaviridae consists of more than 120 viral types divided into 49genera (1). Within the genus Betapapillomavirus, type 23 of species Betapapilloma-virus 2 (HPV-23) is represented in GenBank by a single complete genome (2) composedof a circular double-stranded DNA of 7.3 kb (accession no. U31781), as well as twoshorter fragments (3, 4). HPV-23 is a clinically signiﬁcant papillomavirus, having beenimplicated in epidermodysplasia verruciformis (2), skin cancer (5), ocular syringoma (6),nongenital seborrhoeic keratosis (7), breast cancer (8), and toenail onycholysis (9).Volunteers were recruited from a general practice surgery and a general hospital inLancaster, UK (54.05°N, 2.80°W). Nasopharyngeal swabs were taken between 16 De-cember 2014 and 25 February 2015. Ethical approval was granted by the UK NationalResearch Ethics Service, reference 14/LO/1634, NIHR Clinical Research Network (UKCRN)portfolio, ID 17799. All methods were carried out in accordance with the relevantguidelines and regulations.Pooled RNA from 51 swabs was deep sequenced using an Illumina Nextera XT libraryand HiSeq 2500 system (SRA GenBank accession no. SRP092324). An HPV-23 genomewas assembled using Bowtie 1.1.1 (10) and BWA 0.7.12-r1039 (11), with U31781 as thetemplate. The assembled genome is 7,317 bases in length, differing from U31781 by188 substitutions (2.7%). A 6-base deletion in the new genome starts at position 5418,within the L2 gene. A further single-base deletion occurs at position 7193, in the 3=direction from the L1 gene. The predicted protein sequences are derived by referenceto U31781 and differ at 62 amino acid residues (2.4%), without nonsense substitutions.de Villiers et al. (12) recommend that a nucleotide divergence of 15% be used as thethreshold for designation of a new type of human papillomavirus. The new strain istherefore well within the range of diversity expected within type 23 and has beendesignated HPV-23/Lancaster/2015. It is only the second full-length genome of HPV-23to be described.Forslund et al. (13) found HPV types of the Betapapillomavirus 2 species in 9% ofnasal swabs in a study of 312 Danish health care staff, but they detected HPV-23 in onlyReceived 2 March 2017 Accepted 28 March2017 Published 18 May 2017Citation Atkinson KV, Bishop LA, Rhodes G,Salez N, McEwan NR, Hegarty MJ, Robey J,Harding N, Wetherell S, Lauder RM, Pickup RW,Wilkinson M, Gatherer D. 2017. Genomesequence of human papillomavirus 23 strainHPV-23/Lancaster/2015. Genome Announc5:e00257-17. https://doi.org/10.1128/genomeA.00257-17.Copyright © 2017 Atkinson et al. This is anopen-access article distributed under the termsof the Creative Commons Attribution 4.0International license.Address correspondence to Derek Gatherer,d.gatherer@lancaster.ac.uk.* Present address: Kate V. Atkinson, UniversityCollege London Hospitals NHS FoundationTrust, London, United Kingdom.VIRUSEScrossmVolume 5 Issue 20 e00257-17 genomea.asm.org 1 on May 23, 2017 by UNIVERSITY COLLEGE OF WALEShttp://genomea.asm.org/Downloaded from 2 individuals (0.7%). Of 9 deep-sequenced nonoverlapping subsets of individualsfrom our 51 swabs, we detected HPV-23 in all but one. Our frequency is therefore atleast 8/51 (15%) and possibly much higher. The signiﬁcance of this clinically impor-tant papillomavirus at the prevalence in our sample remains a matter for speculation(BAM ﬁles, alignments, and phylogenetic trees are available from https://doi.org/10.17635/lancaster/researchdata/134).Accession number(s). The genome sequence of HPV-23/Lancaster/2015 has beendeposited in GenBank under the accession number KY652675.ACKNOWLEDGMENTSK.V.A. received a Service Increment from Teaching (SIFT) studentship from UniversityHospitals of Morecambe Bay (UHMB) National Health Service (NHS) Foundation Trust,United Kingdom, and performed this work as part of the requirements for the degreeof Master of Science (M.Sc.). Rosetrees Trust, United Kingdom, provided additionalfunding for deep sequencing (grant M395).REFERENCES1. Harari A, Chen Z, Burk RD. 2014. Human papillomavirus genomics: past,present and future. Curr Probl Dermatol 45:1–18. https://doi.org/10.1159/000355952.2. Kremsdorf D, Favre M, Jablonska S, Obalek S, Rueda LA, Lutzner MA,Blanchet-Bardon C, Van Voorst Vader PC, Orth G. 1984. Molecular clon-ing and characterization of the genomes of nine newly recognizedhuman papillomavirus types associated with epidermodysplasia verru-ciformis. J Virol 52:1013–1018.3. Chan SY, Delius H, Halpern AL, Bernard HU. 1995. Analysis of genomicsequences of 95 papillomavirus types: uniting typing, phylogeny, andtaxonomy. J Virol 69:3074–3083.4. Berkhout RJ, Tieben LM, Smits HL, Bavinck JN, Vermeer BJ, ter ScheggetJ. 1995. Nested PCR approach for detection and typing of epidermodys-plasia verruciformis-associated human papillomavirus types in cutane-ous cancers from renal transplant recipients. J Clin Microbiol 33:690–695.5. de Villiers EM. 1998. Human papillomavirus infections in skin cancers.Biomed Pharmacother 52:26–33.6. Assadoullina A, Bialasiewicz AA, de Villiers EM, Richard G. 2000.Detection of HPV-20, HPV-23, and HPV-DL332 in a solitary eyelidsyringoma. Am J Ophthalmol 129:99–101. https://doi.org/10.1016/S0002-9394(99)00292-5.7. Li YH, Chen G, Dong XP, Chen HD. 2004. Detection of epidermodysplasiaverruciformis-associated human papillomavirus DNA in nongenital seb-orrhoeic keratosis. Br J Dermatol 151:1060–1065. https://doi.org/10.1111/j.1365-2133.2004.06244.x.8. Sigaroodi A, Nadji SA, Naghshvar F, Nategh R, Emami H, Velayati AA.2012. Human papillomavirus is associated with breast cancer in thenorth part of Iran. ScientiﬁcWorldJournal 2012:837191. https://doi.org/10.1100/2012/837191.9. Umanoff N, Werner B, Rady PL, Tyring S, Carlson JA. 2015. Persistenttoenail onycholysis associated with beta-papillomavirus infection of thenail bed. Am J Dermatopathol 37:329–333. https://doi.org/10.1097/DAD.0000000000000110.10. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast andmemory-efﬁcient alignment of short DNA sequences to the humangenome. Genome Biol 10:R25. https://doi.org/10.1186/gb-2009-10-3-r25.11. Li H, Durbin R. 2010. Fast and accurate long-read alignment withBurrows-Wheeler transform. Bioinformatics 26:589–595. https://doi.org/10.1093/bioinformatics/btp698.12. de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H. 2004.Classiﬁcation of papillomaviruses. Virology 324:17–27. https://doi.org/10.1016/j.virol.2004.03.033.13. Forslund O, Johansson H, Madsen KG, Kofoed K. 2013. The nasal mucosacontains a large spectrum of human papillomavirus types from theBetapapillomavirus and Gammapapillomavirus genera. J Infect Dis 208:1335–1341. https://doi.org/10.1093/infdis/jit326.Atkinson et al.Volume 5 Issue 20 e00257-17 genomea.asm.org 2 on May 23, 2017 by UNIVERSITY COLLEGE OF WALEShttp://genomea.asm.org/Downloaded from 

The genome of human papillomavirus type 23 (HPV-23; family Papillomaviridae, genus Betapapillomavirus, species Betapapillomavirus 2, type 23) was assembled by deep sequencing from nasopharyngeal swabs. The assembled genome is 2.7% divergent over its full length from the single complete genome of HPV-23 in GenBank (accession no. U31781). We named the strain HPV-23/Lancaster/2015

McEwan, Neil R.

Hegarty, Matthew J.

Open Access Institutional Repository at Robert Gordon University

   AUTHOR(S):   TITLE:    YEAR:   Publisher citation:    OpenAIR citation:    Publisher copyright statement:      OpenAIR takedown statement:   This publication is made freely available under ________ open access.      This is the ______________________ version of an article originally published by ____________________________ in __________________________________________________________________________________________ (ISSN _________; eISSN __________). This publication is distributed under a CC ____________ license. ____________________________________________________ Section 6 of the “Repository policy for OpenAIR @ RGU” (available from http://www.rgu.ac.uk/staff-and-current-students/library/library-policies/repository-policies) provides guidance on the criteria under which RGU will consider withdrawing material from OpenAIR. If you believe that this item is subject to any of these criteria, or for any other reason should not be held on OpenAIR, then please contact openair-help@rgu.ac.uk with the details of the item and the nature of your complaint.  Genome Sequence of HumanPapillomavirus 23 StrainHPV-23/Lancaster/2015Kate V. Atkinson,a* Lisa A. Bishop,a,b Glenn Rhodes,c Nicolas Salez,dNeil R. McEwan,e Matthew J. Hegarty,e Julie Robey,f Nicola Harding,fSimon Wetherell,f Robert M. Lauder,a Roger W. Pickup,a,c Mark Wilkinson,bDerek GathereraDivision of Biomedical & Life Sciences, Faculty of Health & Medicine, Lancaster University, Lancaster, UnitedKingdoma; Royal Lancaster Inﬁrmary, Lancaster, United Kingdomb; Centre for Ecology & Hydrology, LakeEcosystems Group, Lancaster Environment Centre, Lancaster University, Lancaster, United Kingdomc; UMR_D190, Emergence des Pathologies Virales, Aix-Marseille University, Marseille, Franced; Institute of Biological,Environmental & Rural Sciences, Aberystwyth University, Aberystwyth, United Kingdome; Queen SquareMedical Practice, Lancaster, United KingdomfABSTRACT The genome of human papillomavirus type 23 (HPV-23; family Papillo-maviridae, genus Betapapillomavirus, species Betapapillomavirus 2, type 23) was as-sembled by deep sequencing from nasopharyngeal swabs. The assembled genomeis 2.7% divergent over its full length from the single complete genome of HPV-23 inGenBank (accession no. U31781). We named the strain HPV-23/Lancaster/2015.The family Papillomaviridae consists of more than 120 viral types divided into 49genera (1). Within the genus Betapapillomavirus, type 23 of species Betapapilloma-virus 2 (HPV-23) is represented in GenBank by a single complete genome (2) composedof a circular double-stranded DNA of 7.3 kb (accession no. U31781), as well as twoshorter fragments (3, 4). HPV-23 is a clinically signiﬁcant papillomavirus, having beenimplicated in epidermodysplasia verruciformis (2), skin cancer (5), ocular syringoma (6),nongenital seborrhoeic keratosis (7), breast cancer (8), and toenail onycholysis (9).Volunteers were recruited from a general practice surgery and a general hospital inLancaster, UK (54.05°N, 2.80°W). Nasopharyngeal swabs were taken between 16 De-cember 2014 and 25 February 2015. Ethical approval was granted by the UK NationalResearch Ethics Service, reference 14/LO/1634, NIHR Clinical Research Network (UKCRN)portfolio, ID 17799. All methods were carried out in accordance with the relevantguidelines and regulations.Pooled RNA from 51 swabs was deep sequenced using an Illumina Nextera XT libraryand HiSeq 2500 system (SRA GenBank accession no. SRP092324). An HPV-23 genomewas assembled using Bowtie 1.1.1 (10) and BWA 0.7.12-r1039 (11), with U31781 as thetemplate. The assembled genome is 7,317 bases in length, differing from U31781 by188 substitutions (2.7%). A 6-base deletion in the new genome starts at position 5418,within the L2 gene. A further single-base deletion occurs at position 7193, in the 3=direction from the L1 gene. The predicted protein sequences are derived by referenceto U31781 and differ at 62 amino acid residues (2.4%), without nonsense substitutions.de Villiers et al. (12) recommend that a nucleotide divergence of 15% be used as thethreshold for designation of a new type of human papillomavirus. The new strain istherefore well within the range of diversity expected within type 23 and has beendesignated HPV-23/Lancaster/2015. It is only the second full-length genome of HPV-23to be described.Forslund et al. (13) found HPV types of the Betapapillomavirus 2 species in 9% ofnasal swabs in a study of 312 Danish health care staff, but they detected HPV-23 in onlyReceived 2 March 2017 Accepted 28 March2017 Published 18 May 2017Citation Atkinson KV, Bishop LA, Rhodes G,Salez N, McEwan NR, Hegarty MJ, Robey J,Harding N, Wetherell S, Lauder RM, Pickup RW,Wilkinson M, Gatherer D. 2017. Genomesequence of human papillomavirus 23 strainHPV-23/Lancaster/2015. Genome Announc5:e00257-17. https://doi.org/10.1128/genomeA.00257-17.Copyright © 2017 Atkinson et al. This is anopen-access article distributed under the termsof the Creative Commons Attribution 4.0International license.Address correspondence to Derek Gatherer,d.gatherer@lancaster.ac.uk.* Present address: Kate V. Atkinson, UniversityCollege London Hospitals NHS FoundationTrust, London, United Kingdom.VIRUSEScrossmVolume 5 Issue 20 e00257-17 genomea.asm.org 1 on May 23, 2017 by UNIVERSITY COLLEGE OF WALEShttp://genomea.asm.org/Downloaded from 2 individuals (0.7%). Of 9 deep-sequenced nonoverlapping subsets of individualsfrom our 51 swabs, we detected HPV-23 in all but one. Our frequency is therefore atleast 8/51 (15%) and possibly much higher. The signiﬁcance of this clinically impor-tant papillomavirus at the prevalence in our sample remains a matter for speculation(BAM ﬁles, alignments, and phylogenetic trees are available from https://doi.org/10.17635/lancaster/researchdata/134).Accession number(s). The genome sequence of HPV-23/Lancaster/2015 has beendeposited in GenBank under the accession number KY652675.ACKNOWLEDGMENTSK.V.A. received a Service Increment from Teaching (SIFT) studentship from UniversityHospitals of Morecambe Bay (UHMB) National Health Service (NHS) Foundation Trust,United Kingdom, and performed this work as part of the requirements for the degreeof Master of Science (M.Sc.). Rosetrees Trust, United Kingdom, provided additionalfunding for deep sequencing (grant M395).REFERENCES1. Harari A, Chen Z, Burk RD. 2014. Human papillomavirus genomics: past,present and future. Curr Probl Dermatol 45:1–18. https://doi.org/10.1159/000355952.2. Kremsdorf D, Favre M, Jablonska S, Obalek S, Rueda LA, Lutzner MA,Blanchet-Bardon C, Van Voorst Vader PC, Orth G. 1984. Molecular clon-ing and characterization of the genomes of nine newly recognizedhuman papillomavirus types associated with epidermodysplasia verru-ciformis. J Virol 52:1013–1018.3. Chan SY, Delius H, Halpern AL, Bernard HU. 1995. Analysis of genomicsequences of 95 papillomavirus types: uniting typing, phylogeny, andtaxonomy. J Virol 69:3074–3083.4. Berkhout RJ, Tieben LM, Smits HL, Bavinck JN, Vermeer BJ, ter ScheggetJ. 1995. Nested PCR approach for detection and typing of epidermodys-plasia verruciformis-associated human papillomavirus types in cutane-ous cancers from renal transplant recipients. J Clin Microbiol 33:690–695.5. de Villiers EM. 1998. Human papillomavirus infections in skin cancers.Biomed Pharmacother 52:26–33.6. Assadoullina A, Bialasiewicz AA, de Villiers EM, Richard G. 2000.Detection of HPV-20, HPV-23, and HPV-DL332 in a solitary eyelidsyringoma. Am J Ophthalmol 129:99–101. https://doi.org/10.1016/S0002-9394(99)00292-5.7. Li YH, Chen G, Dong XP, Chen HD. 2004. Detection of epidermodysplasiaverruciformis-associated human papillomavirus DNA in nongenital seb-orrhoeic keratosis. Br J Dermatol 151:1060–1065. https://doi.org/10.1111/j.1365-2133.2004.06244.x.8. Sigaroodi A, Nadji SA, Naghshvar F, Nategh R, Emami H, Velayati AA.2012. Human papillomavirus is associated with breast cancer in thenorth part of Iran. ScientiﬁcWorldJournal 2012:837191. https://doi.org/10.1100/2012/837191.9. Umanoff N, Werner B, Rady PL, Tyring S, Carlson JA. 2015. Persistenttoenail onycholysis associated with beta-papillomavirus infection of thenail bed. Am J Dermatopathol 37:329–333. https://doi.org/10.1097/DAD.0000000000000110.10. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast andmemory-efﬁcient alignment of short DNA sequences to the humangenome. Genome Biol 10:R25. https://doi.org/10.1186/gb-2009-10-3-r25.11. Li H, Durbin R. 2010. Fast and accurate long-read alignment withBurrows-Wheeler transform. Bioinformatics 26:589–595. https://doi.org/10.1093/bioinformatics/btp698.12. de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H. 2004.Classiﬁcation of papillomaviruses. Virology 324:17–27. https://doi.org/10.1016/j.virol.2004.03.033.13. Forslund O, Johansson H, Madsen KG, Kofoed K. 2013. The nasal mucosacontains a large spectrum of human papillomavirus types from theBetapapillomavirus and Gammapapillomavirus genera. J Infect Dis 208:1335–1341. https://doi.org/10.1093/infdis/jit326.Atkinson et al.Volume 5 Issue 20 e00257-17 genomea.asm.org 2 on May 23, 2017 by UNIVERSITY COLLEGE OF WALEShttp://genomea.asm.org/Downloaded from 

Genome sequence of human papillomavirus 23 strain HPV-23/Lancaster/2015.

NERC Open Research Archive

Genome Sequence of HumanPapillomavirus 23 StrainHPV-23/Lancaster/2015Kate V. Atkinson,a* Lisa A. Bishop,a,b Glenn Rhodes,c Nicolas Salez,dNeil R. McEwan,e Matthew J. Hegarty,e Julie Robey,f Nicola Harding,fSimon Wetherell,f Robert M. Lauder,a Roger W. Pickup,a,c Mark Wilkinson,bDerek GathereraDivision of Biomedical & Life Sciences, Faculty of Health & Medicine, Lancaster University, Lancaster, UnitedKingdoma; Royal Lancaster Inﬁrmary, Lancaster, United Kingdomb; Centre for Ecology & Hydrology, LakeEcosystems Group, Lancaster Environment Centre, Lancaster University, Lancaster, United Kingdomc; UMR_D190, Emergence des Pathologies Virales, Aix-Marseille University, Marseille, Franced; Institute of Biological,Environmental & Rural Sciences, Aberystwyth University, Aberystwyth, United Kingdome; Queen SquareMedical Practice, Lancaster, United KingdomfABSTRACT The genome of human papillomavirus type 23 (HPV-23; family Papillo-maviridae, genus Betapapillomavirus, species Betapapillomavirus 2, type 23) was as-sembled by deep sequencing from nasopharyngeal swabs. The assembled genomeis 2.7% divergent over its full length from the single complete genome of HPV-23 inGenBank (accession no. U31781). We named the strain HPV-23/Lancaster/2015.The family Papillomaviridae consists of more than 120 viral types divided into 49genera (1). Within the genus Betapapillomavirus, type 23 of species Betapapilloma-virus 2 (HPV-23) is represented in GenBank by a single complete genome (2) composedof a circular double-stranded DNA of 7.3 kb (accession no. U31781), as well as twoshorter fragments (3, 4). HPV-23 is a clinically signiﬁcant papillomavirus, having beenimplicated in epidermodysplasia verruciformis (2), skin cancer (5), ocular syringoma (6),nongenital seborrhoeic keratosis (7), breast cancer (8), and toenail onycholysis (9).Volunteers were recruited from a general practice surgery and a general hospital inLancaster, UK (54.05°N, 2.80°W). Nasopharyngeal swabs were taken between 16 De-cember 2014 and 25 February 2015. Ethical approval was granted by the UK NationalResearch Ethics Service, reference 14/LO/1634, NIHR Clinical Research Network (UKCRN)portfolio, ID 17799. All methods were carried out in accordance with the relevantguidelines and regulations.Pooled RNA from 51 swabs was deep sequenced using an Illumina Nextera XT libraryand HiSeq 2500 system (SRA GenBank accession no. SRP092324). An HPV-23 genomewas assembled using Bowtie 1.1.1 (10) and BWA 0.7.12-r1039 (11), with U31781 as thetemplate. The assembled genome is 7,317 bases in length, differing from U31781 by188 substitutions (2.7%). A 6-base deletion in the new genome starts at position 5418,within the L2 gene. A further single-base deletion occurs at position 7193, in the 3=direction from the L1 gene. The predicted protein sequences are derived by referenceto U31781 and differ at 62 amino acid residues (2.4%), without nonsense substitutions.de Villiers et al. (12) recommend that a nucleotide divergence of 15% be used as thethreshold for designation of a new type of human papillomavirus. The new strain istherefore well within the range of diversity expected within type 23 and has beendesignated HPV-23/Lancaster/2015. It is only the second full-length genome of HPV-23to be described.Forslund et al. (13) found HPV types of the Betapapillomavirus 2 species in 9% ofnasal swabs in a study of 312 Danish health care staff, but they detected HPV-23 in onlyReceived 2 March 2017 Accepted 28 March2017 Published 18 May 2017Citation Atkinson KV, Bishop LA, Rhodes G,Salez N, McEwan NR, Hegarty MJ, Robey J,Harding N, Wetherell S, Lauder RM, Pickup RW,Wilkinson M, Gatherer D. 2017. Genomesequence of human papillomavirus 23 strainHPV-23/Lancaster/2015. Genome Announc5:e00257-17. https://doi.org/10.1128/genomeA.00257-17.Copyright © 2017 Atkinson et al. This is anopen-access article distributed under the termsof the Creative Commons Attribution 4.0International license.Address correspondence to Derek Gatherer,d.gatherer@lancaster.ac.uk.* Present address: Kate V. Atkinson, UniversityCollege London Hospitals NHS FoundationTrust, London, United Kingdom.VIRUSEScrossmVolume 5 Issue 20 e00257-17 genomea.asm.org 1 on May 22, 2017 by CEH WALLINGFORDhttp://genomea.asm.org/Downloaded from 2 individuals (0.7%). Of 9 deep-sequenced nonoverlapping subsets of individualsfrom our 51 swabs, we detected HPV-23 in all but one. Our frequency is therefore atleast 8/51 (15%) and possibly much higher. The signiﬁcance of this clinically impor-tant papillomavirus at the prevalence in our sample remains a matter for speculation(BAM ﬁles, alignments, and phylogenetic trees are available from https://doi.org/10.17635/lancaster/researchdata/134).Accession number(s). The genome sequence of HPV-23/Lancaster/2015 has beendeposited in GenBank under the accession number KY652675.ACKNOWLEDGMENTSK.V.A. received a Service Increment from Teaching (SIFT) studentship from UniversityHospitals of Morecambe Bay (UHMB) National Health Service (NHS) Foundation Trust,United Kingdom, and performed this work as part of the requirements for the degreeof Master of Science (M.Sc.). Rosetrees Trust, United Kingdom, provided additionalfunding for deep sequencing (grant M395).REFERENCES1. Harari A, Chen Z, Burk RD. 2014. Human papillomavirus genomics: past,present and future. Curr Probl Dermatol 45:1–18. https://doi.org/10.1159/000355952.2. Kremsdorf D, Favre M, Jablonska S, Obalek S, Rueda LA, Lutzner MA,Blanchet-Bardon C, Van Voorst Vader PC, Orth G. 1984. Molecular clon-ing and characterization of the genomes of nine newly recognizedhuman papillomavirus types associated with epidermodysplasia verru-ciformis. J Virol 52:1013–1018.3. Chan SY, Delius H, Halpern AL, Bernard HU. 1995. Analysis of genomicsequences of 95 papillomavirus types: uniting typing, phylogeny, andtaxonomy. J Virol 69:3074–3083.4. Berkhout RJ, Tieben LM, Smits HL, Bavinck JN, Vermeer BJ, ter ScheggetJ. 1995. Nested PCR approach for detection and typing of epidermodys-plasia verruciformis-associated human papillomavirus types in cutane-ous cancers from renal transplant recipients. J Clin Microbiol 33:690–695.5. de Villiers EM. 1998. Human papillomavirus infections in skin cancers.Biomed Pharmacother 52:26–33.6. Assadoullina A, Bialasiewicz AA, de Villiers EM, Richard G. 2000.Detection of HPV-20, HPV-23, and HPV-DL332 in a solitary eyelidsyringoma. Am J Ophthalmol 129:99–101. https://doi.org/10.1016/S0002-9394(99)00292-5.7. Li YH, Chen G, Dong XP, Chen HD. 2004. Detection of epidermodysplasiaverruciformis-associated human papillomavirus DNA in nongenital seb-orrhoeic keratosis. Br J Dermatol 151:1060–1065. https://doi.org/10.1111/j.1365-2133.2004.06244.x.8. Sigaroodi A, Nadji SA, Naghshvar F, Nategh R, Emami H, Velayati AA.2012. Human papillomavirus is associated with breast cancer in thenorth part of Iran. ScientiﬁcWorldJournal 2012:837191. https://doi.org/10.1100/2012/837191.9. Umanoff N, Werner B, Rady PL, Tyring S, Carlson JA. 2015. Persistenttoenail onycholysis associated with beta-papillomavirus infection of thenail bed. Am J Dermatopathol 37:329–333. https://doi.org/10.1097/DAD.0000000000000110.10. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast andmemory-efﬁcient alignment of short DNA sequences to the humangenome. Genome Biol 10:R25. https://doi.org/10.1186/gb-2009-10-3-r25.11. Li H, Durbin R. 2010. Fast and accurate long-read alignment withBurrows-Wheeler transform. Bioinformatics 26:589–595. https://doi.org/10.1093/bioinformatics/btp698.12. de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H. 2004.Classiﬁcation of papillomaviruses. Virology 324:17–27. https://doi.org/10.1016/j.virol.2004.03.033.13. Forslund O, Johansson H, Madsen KG, Kofoed K. 2013. The nasal mucosacontains a large spectrum of human papillomavirus types from theBetapapillomavirus and Gammapapillomavirus genera. J Infect Dis 208:1335–1341. https://doi.org/10.1093/infdis/jit326.Atkinson et al.Volume 5 Issue 20 e00257-17 genomea.asm.org 2 on May 22, 2017 by CEH WALLINGFORDhttp://genomea.asm.org/Downloaded from 

Genome sequence of human papillomavirus 23 strain HPV-23/Lancaster/2015

Aberystwyth UniversityGenome Sequence of Human Papillomavirus 23 Strain HPV-23/Lancaster/2015Atkinson, Kate V.; Bishop, Lisa A.; Rhodes, Glenn; Salez, Nicolas; McEwan, Neil; Hegarty, Matthew; Robey,Julie; Harding, Nicola; Wetherell, Simon; Lauder, Robert M.; Pickup, Roger W.; Wilkinson, Mark; Gatherer,DerekPublished in:Genome AnnouncementsDOI:10.1128/genomeA.00257-17Publication date:2017Citation for published version (APA):Atkinson, K. V., Bishop, L. A., Rhodes, G., Salez, N., McEwan, N., Hegarty, M., Robey, J., Harding, N.,Wetherell, S., Lauder, R. M., Pickup, R. W., Wilkinson, M., & Gatherer, D. (2017). Genome Sequence of HumanPapillomavirus 23 Strain HPV-23/Lancaster/2015. Genome Announcements, 5(20), [e00257-17].https://doi.org/10.1128/genomeA.00257-17Document LicenseCC BYGeneral rightsCopyright and moral rights for the publications made accessible in the Aberystwyth Research Portal (the Institutional Repository) areretained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by thelegal requirements associated with these rights.            • Users may download and print one copy of any publication from the Aberystwyth Research Portal for the purpose of private study orresearch.            • You may not further distribute the material or use it for any profit-making activity or commercial gain            • You may freely distribute the URL identifying the publication in the Aberystwyth Research PortalTake down policyIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediatelyand investigate your claim.tel: +44 1970 62 2400email: is@aber.ac.ukDownload date: 09. Jul. 2020Genome Sequence of HumanPapillomavirus 23 StrainHPV-23/Lancaster/2015Kate V. Atkinson,a* Lisa A. Bishop,a,b Glenn Rhodes,c Nicolas Salez,dNeil R. McEwan,e Matthew J. Hegarty,e Julie Robey,f Nicola Harding,fSimon Wetherell,f Robert M. Lauder,a Roger W. Pickup,a,c Mark Wilkinson,bDerek GathereraDivision of Biomedical & Life Sciences, Faculty of Health & Medicine, Lancaster University, Lancaster, UnitedKingdoma; Royal Lancaster Infirmary, Lancaster, United Kingdomb; Centre for Ecology & Hydrology, LakeEcosystems Group, Lancaster Environment Centre, Lancaster University, Lancaster, United Kingdomc; UMR_D190, Emergence des Pathologies Virales, Aix-Marseille University, Marseille, Franced; Institute of Biological,Environmental & Rural Sciences, Aberystwyth University, Aberystwyth, United Kingdome; Queen SquareMedical Practice, Lancaster, United KingdomfABSTRACT The genome of human papillomavirus type 23 (HPV-23; family Papillo-maviridae, genus Betapapillomavirus, species Betapapillomavirus 2, type 23) was as-sembled by deep sequencing from nasopharyngeal swabs. The assembled genomeis 2.7% divergent over its full length from the single complete genome of HPV-23 inGenBank (accession no. U31781). We named the strain HPV-23/Lancaster/2015.The family Papillomaviridae consists of more than 120 viral types divided into 49genera (1). Within the genus Betapapillomavirus, type 23 of species Betapapilloma-virus 2 (HPV-23) is represented in GenBank by a single complete genome (2) composedof a circular double-stranded DNA of 7.3 kb (accession no. U31781), as well as twoshorter fragments (3, 4). HPV-23 is a clinically significant papillomavirus, having beenimplicated in epidermodysplasia verruciformis (2), skin cancer (5), ocular syringoma (6),nongenital seborrhoeic keratosis (7), breast cancer (8), and toenail onycholysis (9).Volunteers were recruited from a general practice surgery and a general hospital inLancaster, UK (54.05°N, 2.80°W). Nasopharyngeal swabs were taken between 16 De-cember 2014 and 25 February 2015. Ethical approval was granted by the UK NationalResearch Ethics Service, reference 14/LO/1634, NIHR Clinical Research Network (UKCRN)portfolio, ID 17799. All methods were carried out in accordance with the relevantguidelines and regulations.Pooled RNA from 51 swabs was deep sequenced using an Illumina Nextera XT libraryand HiSeq 2500 system (SRA GenBank accession no. SRP092324). An HPV-23 genomewas assembled using Bowtie 1.1.1 (10) and BWA 0.7.12-r1039 (11), with U31781 as thetemplate. The assembled genome is 7,317 bases in length, differing from U31781 by188 substitutions (2.7%). A 6-base deletion in the new genome starts at position 5418,within the L2 gene. A further single-base deletion occurs at position 7193, in the 3=direction from the L1 gene. The predicted protein sequences are derived by referenceto U31781 and differ at 62 amino acid residues (2.4%), without nonsense substitutions.de Villiers et al. (12) recommend that a nucleotide divergence of 15% be used as thethreshold for designation of a new type of human papillomavirus. The new strain istherefore well within the range of diversity expected within type 23 and has beendesignated HPV-23/Lancaster/2015. It is only the second full-length genome of HPV-23to be described.Forslund et al. (13) found HPV types of the Betapapillomavirus 2 species in 9% ofnasal swabs in a study of 312 Danish health care staff, but they detected HPV-23 in onlyReceived 2 March 2017 Accepted 28 March2017 Published 18 May 2017Citation Atkinson KV, Bishop LA, Rhodes G,Salez N, McEwan NR, Hegarty MJ, Robey J,Harding N, Wetherell S, Lauder RM, Pickup RW,Wilkinson M, Gatherer D. 2017. Genomesequence of human papillomavirus 23 strainHPV-23/Lancaster/2015. Genome Announc5:e00257-17. https://doi.org/10.1128/genomeA.00257-17.Copyright © 2017 Atkinson et al. This is anopen-access article distributed under the termsof the Creative Commons Attribution 4.0International license.Address correspondence to Derek Gatherer,d.gatherer@lancaster.ac.uk.* Present address: Kate V. Atkinson, UniversityCollege London Hospitals NHS FoundationTrust, London, United Kingdom.VIRUSEScrossmVolume 5 Issue 20 e00257-17 genomea.asm.org 1 on May 23, 2017 by UNIVERSITY COLLEGE OF WALEShttp://genomea.asm.org/Downloaded from 2 individuals (0.7%). Of 9 deep-sequenced nonoverlapping subsets of individualsfrom our 51 swabs, we detected HPV-23 in all but one. Our frequency is therefore atleast 8/51 (15%) and possibly much higher. The significance of this clinically impor-tant papillomavirus at the prevalence in our sample remains a matter for speculation(BAM files, alignments, and phylogenetic trees are available from https://doi.org/10.17635/lancaster/researchdata/134).Accession number(s). The genome sequence of HPV-23/Lancaster/2015 has beendeposited in GenBank under the accession number KY652675.ACKNOWLEDGMENTSK.V.A. received a Service Increment from Teaching (SIFT) studentship from UniversityHospitals of Morecambe Bay (UHMB) National Health Service (NHS) Foundation Trust,United Kingdom, and performed this work as part of the requirements for the degreeof Master of Science (M.Sc.). Rosetrees Trust, United Kingdom, provided additionalfunding for deep sequencing (grant M395).REFERENCES1. Harari A, Chen Z, Burk RD. 2014. Human papillomavirus genomics: past,present and future. Curr Probl Dermatol 45:1–18. https://doi.org/10.1159/000355952.2. Kremsdorf D, Favre M, Jablonska S, Obalek S, Rueda LA, Lutzner MA,Blanchet-Bardon C, Van Voorst Vader PC, Orth G. 1984. Molecular clon-ing and characterization of the genomes of nine newly recognizedhuman papillomavirus types associated with epidermodysplasia verru-ciformis. J Virol 52:1013–1018.3. Chan SY, Delius H, Halpern AL, Bernard HU. 1995. Analysis of genomicsequences of 95 papillomavirus types: uniting typing, phylogeny, andtaxonomy. J Virol 69:3074–3083.4. Berkhout RJ, Tieben LM, Smits HL, Bavinck JN, Vermeer BJ, ter ScheggetJ. 1995. Nested PCR approach for detection and typing of epidermodys-plasia verruciformis-associated human papillomavirus types in cutane-ous cancers from renal transplant recipients. J Clin Microbiol 33:690–695.5. de Villiers EM. 1998. Human papillomavirus infections in skin cancers.Biomed Pharmacother 52:26–33.6. Assadoullina A, Bialasiewicz AA, de Villiers EM, Richard G. 2000.Detection of HPV-20, HPV-23, and HPV-DL332 in a solitary eyelidsyringoma. Am J Ophthalmol 129:99–101. https://doi.org/10.1016/S0002-9394(99)00292-5.7. Li YH, Chen G, Dong XP, Chen HD. 2004. Detection of epidermodysplasiaverruciformis-associated human papillomavirus DNA in nongenital seb-orrhoeic keratosis. Br J Dermatol 151:1060–1065. https://doi.org/10.1111/j.1365-2133.2004.06244.x.8. Sigaroodi A, Nadji SA, Naghshvar F, Nategh R, Emami H, Velayati AA.2012. Human papillomavirus is associated with breast cancer in thenorth part of Iran. ScientificWorldJournal 2012:837191. https://doi.org/10.1100/2012/837191.9. Umanoff N, Werner B, Rady PL, Tyring S, Carlson JA. 2015. Persistenttoenail onycholysis associated with beta-papillomavirus infection of thenail bed. Am J Dermatopathol 37:329–333. https://doi.org/10.1097/DAD.0000000000000110.10. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast andmemory-efficient alignment of short DNA sequences to the humangenome. Genome Biol 10:R25. https://doi.org/10.1186/gb-2009-10-3-r25.11. Li H, Durbin R. 2010. Fast and accurate long-read alignment withBurrows-Wheeler transform. Bioinformatics 26:589–595. https://doi.org/10.1093/bioinformatics/btp698.12. de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H. 2004.Classification of papillomaviruses. Virology 324:17–27. https://doi.org/10.1016/j.virol.2004.03.033.13. Forslund O, Johansson H, Madsen KG, Kofoed K. 2013. The nasal mucosacontains a large spectrum of human papillomavirus types from theBetapapillomavirus and Gammapapillomavirus genera. J Infect Dis 208:1335–1341. https://doi.org/10.1093/infdis/jit326.Atkinson et al.Volume 5 Issue 20 e00257-17 genomea.asm.org 2 on May 23, 2017 by UNIVERSITY COLLEGE OF WALEShttp://genomea.asm.org/Downloaded from 

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Genome Sequence of Human Papillomavirus 23 Strain HPV-23/Lancaster/2015

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