Tracking replicating HPV genomes in proliferating keratinocytes

ABSTRACT Human papillomavirus (HPV) genomes replicate and partition as minichromosomes alongside host chromatin during persistent infection. However, it is difficult to monitor genome dynamics in living cells because the small and compact genome will not easily tolerate expression cassettes. Here, w...

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Main Authors: Jonathan R. Shin, Ivan Avilov, Mario Schelhaas, Franck Gallardo, Alison A. McBride
Format: Article
Language:English
Published: American Society for Microbiology 2025-08-01
Series:mBio
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Online Access:https://journals.asm.org/doi/10.1128/mbio.01308-25
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author Jonathan R. Shin
Ivan Avilov
Mario Schelhaas
Franck Gallardo
Alison A. McBride
author_facet Jonathan R. Shin
Ivan Avilov
Mario Schelhaas
Franck Gallardo
Alison A. McBride
author_sort Jonathan R. Shin
collection DOAJ
description ABSTRACT Human papillomavirus (HPV) genomes replicate and partition as minichromosomes alongside host chromatin during persistent infection. However, it is difficult to monitor genome dynamics in living cells because the small and compact genome will not easily tolerate expression cassettes. Here, we use ANCHOR technology to detect HPV18 genomes in living cells. We incorporated the cis-element from ANCHOR technology into the late region of the HPV18 genome and expressed the ParB-GFP protein from an HPV18-dependent replicon. The replicon contains the HPV18 replication origin and viral transcriptional enhancer element and can replicate stably in keratinocytes when complemented by the HPV18 genome. This small replicon expresses the neomycin resistance gene in both bacteria and eukaryotic cells and has minimal prokaryotic elements that could induce innate immunity. This molecular tool enables us to indirectly monitor the presence of the virus by detecting these fluorescent proteins in live cells and allows for real-time tracking of replicating HPV18-ANCH3 genomes in proliferating keratinocytes to inform on models of HPV genome maintenance, tethering, and amplification. Here, we visualize the partitioning of the viral DNA in dividing cells and show that HPV18-ANCH genomes are distributed somewhat equally to daughter cells by attachment to host chromosomes.IMPORTANCEIn persistent human papillomavirus (HPV) infection, the viral genome is maintained at a constant copy number, replicates in synchrony with host DNA during S-phase, and is partitioned into daughter cells. The exact method by which HPVs partition to daughter cells is not well understood, and the elucidation of such mechanisms may reveal relevant pharmacological targets to combat persistent HPV infection.
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spelling doaj-art-988898014e7744888606a69117da99df2025-08-20T03:02:56ZengAmerican Society for MicrobiologymBio2150-75112025-08-0116810.1128/mbio.01308-25Tracking replicating HPV genomes in proliferating keratinocytesJonathan R. Shin0Ivan Avilov1Mario Schelhaas2Franck Gallardo3Alison A. McBride4Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USAInstitute of Cellular Virology, University of Münster, Münster, GermanyInstitute of Cellular Virology, University of Münster, Münster, GermanyNeoVirTech, Toulouse, FranceLaboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USAABSTRACT Human papillomavirus (HPV) genomes replicate and partition as minichromosomes alongside host chromatin during persistent infection. However, it is difficult to monitor genome dynamics in living cells because the small and compact genome will not easily tolerate expression cassettes. Here, we use ANCHOR technology to detect HPV18 genomes in living cells. We incorporated the cis-element from ANCHOR technology into the late region of the HPV18 genome and expressed the ParB-GFP protein from an HPV18-dependent replicon. The replicon contains the HPV18 replication origin and viral transcriptional enhancer element and can replicate stably in keratinocytes when complemented by the HPV18 genome. This small replicon expresses the neomycin resistance gene in both bacteria and eukaryotic cells and has minimal prokaryotic elements that could induce innate immunity. This molecular tool enables us to indirectly monitor the presence of the virus by detecting these fluorescent proteins in live cells and allows for real-time tracking of replicating HPV18-ANCH3 genomes in proliferating keratinocytes to inform on models of HPV genome maintenance, tethering, and amplification. Here, we visualize the partitioning of the viral DNA in dividing cells and show that HPV18-ANCH genomes are distributed somewhat equally to daughter cells by attachment to host chromosomes.IMPORTANCEIn persistent human papillomavirus (HPV) infection, the viral genome is maintained at a constant copy number, replicates in synchrony with host DNA during S-phase, and is partitioned into daughter cells. The exact method by which HPVs partition to daughter cells is not well understood, and the elucidation of such mechanisms may reveal relevant pharmacological targets to combat persistent HPV infection.https://journals.asm.org/doi/10.1128/mbio.01308-25HPVhuman papillomavirusDNA replicationpartitioningkeratinocytelive cell
spellingShingle Jonathan R. Shin
Ivan Avilov
Mario Schelhaas
Franck Gallardo
Alison A. McBride
Tracking replicating HPV genomes in proliferating keratinocytes
mBio
HPV
human papillomavirus
DNA replication
partitioning
keratinocyte
live cell
title Tracking replicating HPV genomes in proliferating keratinocytes
title_full Tracking replicating HPV genomes in proliferating keratinocytes
title_fullStr Tracking replicating HPV genomes in proliferating keratinocytes
title_full_unstemmed Tracking replicating HPV genomes in proliferating keratinocytes
title_short Tracking replicating HPV genomes in proliferating keratinocytes
title_sort tracking replicating hpv genomes in proliferating keratinocytes
topic HPV
human papillomavirus
DNA replication
partitioning
keratinocyte
live cell
url https://journals.asm.org/doi/10.1128/mbio.01308-25
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AT franckgallardo trackingreplicatinghpvgenomesinproliferatingkeratinocytes
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