ArticleNature communications2023
Single cell transcriptomic analysis of HPV16-infected epithelium identifies a keratinocyte subpopulation implicated in cancer.
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Article in Nature communications, 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 21 papers.
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21citing papers in PubMed
6.4field-weighted citation impact, top 3% of its field
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Who cites it
21 citing papers in PubMed, 30 citations in OpenAlex.
- HPV-Associated Field Cancerization: Molecular Alterations in Histologically Normal Tissues and Implications for Early Detection and Cancer Prevention.Current issues in molecular biology · 2026Review
- Review
- Advancements in single-cell sequencing for cervical cancer research.Molecular and cellular biochemistry · 2026Review
- A prospective cohort study on the association between cervical microenvironmental factors and the efficacy of treating high-risk human papillomavirus infection comorbid with cervical diseases.Frontiers in cellular and infection microbiology · 2026Article
- Immune Responses to Human Papillomavirus After Infection and Vaccination.Current topics in microbiology and immunology · 2026Review
- Loss of ICOSL expression in the progression to cervical carcinoma.Proceedings of the National Academy of Sciences of the United States of America · 2025Article
- Role of T cell exhaustion and tissue-resident memory T cells in the expression and prognosis of colorectal cancer.Scientific reports · 2025Article
- Multi-omics analysis unveiled fibroblast-mediated pathogenesis in male genital lichen sclerosus.Cell & bioscience · 2025Article
- The ELF3-TRIM22-MAVS signaling axis regulates type I interferon and antiviral responses.Journal of virology · 2025Article
- A Single-Cell Transcriptome Atlas of Epithelial Subpopulations in HPV-Positive and HPV-Negative Head and Neck Cancers.Viruses · 2025Article
- Single-cell RNA sequencing highlights the unique tumor microenvironment of small cell neuroendocrine cervical carcinoma.Journal of translational medicine · 2025Article
- Integrated multi-omics analysis of single-cell and spatial transcriptomics reveals distinct hpv-associated immune microenvironment features and prognostic signatures in cervical cancer.Frontiers in immunology · 2025Article
- The local cellular response to Human Papillomavirus focuses on basal layer restoration as visualizedFrontiers in immunology · 2025Article
- ELF3 Overexpression Contributes to the Malignant Transformation of HPV16 E6/E7-Immortalized Keratinocytes by Promoting CCNE2 Expression.Journal of microbiology and biotechnology · 2024Article
- Why HPV16? Why, now, HPV42? How the discovery of HPV42 in rare cancers provides an opportunity to challenge our understanding about the transition between health and disease for common members of the healthy microbiota.FEMS microbiology reviews · 2024Review
- HPV induced R-loop formation represses innate immune gene expression while activating DNA damage repair pathways.PLoS pathogens · 2024Article
- Structure and transcription of integrated HPV DNA in vulvar carcinomas.NPJ genomic medicine · 2024Article
- The macrophage polarization inFrontiers in immunology · 2024Article
- Multiomic analysis of cervical squamous cell carcinoma identifies cellular ecosystems with biological and clinical relevance.Nature genetics · 2023Article
- Biogeographical Impacts of Dental, Oral, and Craniofacial Microbial Reservoirs.Journal of dental research · 2023Review
Corrections and comments
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Authors and funding
34 authors at 10 institutions in 2 countries.
Mary C Bedard *Division of Oncology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.
Tafadzwa Chihanga *Division of Oncology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.
Adrean CarlileDivision of Oncology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.
Robert JacksonSchool of Animal and Comparative Biomedical Sciences, University of Arizona, Tucson, AZ, 85721, USA.ORCID 0000-0001-9898-5546
Marion G BrusadelliDivision of Clinical Operations, Medpace, Cincinnati, OH, 45227, USA.
Denis LeeMcArdle Laboratory for Cancer Research, School of Medicine and Public Health, University of Wisconsin, Madison, WI, 53705, USA.
Andrew VonHandorfCenter for Autoimmune Genomics and Etiology (CAGE), Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.
Mark RochmanDivision of Allergy and Immunology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.ORCID 0000-0002-0818-927X
Phillip J DexheimerDivision of Biomedical Informatics, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.ORCID 0000-0003-3965-6894
Jeffrey ChalmersWilliam G. Lowrie Department of Chemical and Biomolecular Engineering, Ohio State University, 151 W. Woodruff Ave, Columbus, OH, 43210, USA.ORCID 0000-0003-1723-9774
Gerard NuovoDepartment of Pathology, Ohio State University Medical Center, Columbus, OH, 43210, USA.
Maria LehnDivision of Hematology/Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, 45267, USA.ORCID 0000-0001-8400-7733
David E J WilliamsCancer Biology Graduate Interdisciplinary Program, University of Arizona, Tucson, AZ, 85721, USA.
Aditi KulkarniUPMC Hillman Cancer Center, University of Pittsburgh, Pittsburgh, PA, 15232, USA.
Molly CareyDepartment of Obstetrics and Gynecology, University of Cincinnati Medical Center, Cincinnati, OH, 45267, USA.
Amanda JacksonDepartment of Obstetrics and Gynecology, University of Cincinnati Medical Center, Cincinnati, OH, 45267, USA.
Caroline BillingsleyDepartment of Obstetrics and Gynecology, University of Cincinnati Medical Center, Cincinnati, OH, 45267, USA.
Alice TangDepartment of Otolaryngology, University of Cincinnati, Cincinnati, OH, 45267, USA.
Chad ZenderDepartment of Otolaryngology, University of Cincinnati, Cincinnati, OH, 45267, USA.
Yash PatilDepartment of Otolaryngology, University of Cincinnati, Cincinnati, OH, 45267, USA.
Trisha M Wise-DraperDivision of Hematology/Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, 45267, USA.
Thomas J HerzogDepartment of Obstetrics and Gynecology, University of Cincinnati Medical Center, Cincinnati, OH, 45267, USA.
Robert L FerrisUPMC Hillman Cancer Center, University of Pittsburgh, Pittsburgh, PA, 15232, USA.
Ady KendlerDepartment of Pathology & Laboratory Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, 45267, USA.
Bruce J AronowDivision of Biomedical Informatics, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.ORCID 0000-0001-5109-6514
Matthew KofronDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.
Marc E RothenbergDivision of Allergy and Immunology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.ORCID 0000-0001-9790-6332
Matthew T WeirauchCenter for Autoimmune Genomics and Etiology (CAGE), Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.
Koenraad Van DoorslaerSchool of Animal and Comparative Biomedical Sciences, University of Arizona, Tucson, AZ, 85721, USA.ORCID 0000-0002-2985-0733
Kathryn A Wikenheiser-BrokampDepartment of Pathology & Laboratory Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, 45267, USA.ORCID 0000-0002-2932-3095
Paul F LambertMcArdle Laboratory for Cancer Research, School of Medicine and Public Health, University of Wisconsin, Madison, WI, 53705, USA.
Mike AdamDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA. Mike.Adam@cchmc.org.ORCID 0000-0003-4501-4740
S Steven PotterDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA. Steve.Potter@cchmc.org.ORCID 0000-0003-0726-0350
Susanne I WellsDivision of Oncology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA. Susanne.Wells@cchmc.org.ORCID 0000-0002-7234-676X
Cincinnati Children's Hospital Medical Center · USUniversity of Cincinnati · USUniversity of Arizona · USUniversity of Cincinnati Medical Center · USUniversity of Wisconsin–Madison · USMedpace (United States) · USThe Ohio State University · USThe Ohio State University Wexner Medical Center · USUniversity of Pittsburgh · USUPMC Hillman Cancer Center · US
Funding
VITAMIN AP30CA023074 · NCI · UNIVERSITY OF ARIZONA · PI Dan Theodorescu · 1985 to 2026
$110.2MVisualizing EBV and HCMV DNA Dynamics During InfectionP01CA022443 · NCI · UNIVERSITY OF WISCONSIN-MADISON · PI Paul F. Lambert · 1985 to 2026
$53.1MENVIRONMETAL CARCINOGENESIS AND MUTAGENESIST32ES007250 · NIEHS · UNIVERSITY OF CINCINNATI · PI MILLER, WILLIAM E · 1988 to 2024
$11.9MDefining Drivers of HPV-associated CarcinogenesisR35CA210807 · NCI · UNIVERSITY OF WISCONSIN-MADISON · PI Paul F. Lambert · 2017 to 2026
$9.2MGene Regulation as a Foundation for Autoimmune Disease PreventionU01AI130830 · NIAID · CINCINNATI CHILDRENS HOSP MED CTR · PI WEIRAUCH, MATTHEW TYSON · 2017 to 2021
$7.2MVirus-driven human gene misregulation in diseaseR01HG010730 · NHGRI · CINCINNATI CHILDRENS HOSP MED CTR · PI WEIRAUCH, MATTHEW TYSON · 2020 to 2023
$2.7MStrengthening epidermal defenses for the prevention of HPV infection and replicationR01CA228113 · NCI · CINCINNATI CHILDRENS HOSP MED CTR · PI WELLS, SUSANNE I · 2019 to 2023
$1.7MThe role of asymmetric protein dimethylation during the human papillomavirus lifecycleR01AI165638 · NIAID · UNIVERSITY OF ARIZONA · PI Koenraad Van Doorslaer · 2022 to 2026
$1.6MCharacterizing the role of cellular differentiation in productive papillomavirus amplificationR03DE030211 · NIDCR · UNIVERSITY OF ARIZONA · PI VAN DOORSLAER, KOENRAAD · 2021 to 2022
$307kSingle cell RNAseq guides discovery of viral and cellular drivers of RRP pathologiesF30AI157229 · NIAID · UNIVERSITY OF CINCINNATI · PI BEDARD, MARY · 2021 to 2023
$152kNCI NIH HHS P01 CA022443NCI NIH HHS P30 CA023074NCI NIH HHS R01 CA228113NCI NIH HHS R35 CA210807NHGRI NIH HHS R01 HG010730NIAID NIH HHS F30 AI157229NIAID NIH HHS R01 AI165638NIAID NIH HHS U01 AI130830NIDCR NIH HHS R03 DE030211NIEHS NIH HHS T32 ES007250
Abstract
Persistent HPV16 infection is a major cause of the global cancer burden. The viral life cycle is dependent on the differentiation program of stratified squamous epithelium, but the landscape of keratinocyte subpopulations which support distinct phases of the viral life cycle has yet to be elucidated. Here, single cell RNA sequencing of HPV16 infected compared to uninfected organoids identifies twelve distinct keratinocyte populations, with a subset mapped to reconstruct their respective 3D geography in stratified squamous epithelium. Instead of conventional terminally differentiated cells, an HPV-reprogrammed keratinocyte subpopulation (HIDDEN cells) forms the surface compartment and requires overexpression of the ELF3/ESE-1 transcription factor. HIDDEN cells are detected throughout stages of human carcinogenesis including primary human cervical intraepithelial neoplasias and HPV positive head and neck cancers, and a possible role in promoting viral carcinogenesis is supported by TCGA analyses. Single cell transcriptome information on HPV-infected versus uninfected epithelium will enable broader studies of the role of individual keratinocyte subpopulations in tumor virus infection and cancer evolution.
Indexed as
Carcinoma, Squamous CellOncogene Proteins, ViralPapillomavirus InfectionsCarcinogenesisEpitheliumFemaleHuman papillomavirus 16HumansKeratinocytesTranscriptomeOncogene Proteins, Viral
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