HPV16 genome structure analysis in oropharyngeal cancer PDXs identifies tumors with integrated and episomal genomes

HPV + oropharyngeal squamous cell carcinoma (OPC) incidence recently surpassed cervical cancer and is the most common HPV-related cancer in the developed world. HPV16 is in ∼90 % of HPV + OPCs, with episomal genomes in the majority of cases. Most existing HPV16+ cancer cell lines derive from outside...

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Main Authors: Claire D. James, Raymonde O. Otoa, Aya H. Youssef, Christian T. Fontan, Malay K. Sannigrahi, Brad Windle, Devraj Basu, Iain M. Morgan
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Tumour Virus Research
Online Access:http://www.sciencedirect.com/science/article/pii/S2666679024000090
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author Claire D. James
Raymonde O. Otoa
Aya H. Youssef
Christian T. Fontan
Malay K. Sannigrahi
Brad Windle
Devraj Basu
Iain M. Morgan
author_facet Claire D. James
Raymonde O. Otoa
Aya H. Youssef
Christian T. Fontan
Malay K. Sannigrahi
Brad Windle
Devraj Basu
Iain M. Morgan
author_sort Claire D. James
collection DOAJ
description HPV + oropharyngeal squamous cell carcinoma (OPC) incidence recently surpassed cervical cancer and is the most common HPV-related cancer in the developed world. HPV16 is in ∼90 % of HPV + OPCs, with episomal genomes in the majority of cases. Most existing HPV16+ cancer cell lines derive from outside the oropharynx and harbor integrated HPV genomes. Thus, there is need for OPC preclinical models to evaluate standard and experimental therapeutics in the presence of episomal HPV16 oncogenic drivers. Here we characterize HPV genome structures in eight HPV16+ OPC patient-derived xenografts (PDXs), and evaluate their responses to standard chemotherapy. HPV genome state was investigated by combining Southern blot, T5 exonuclease assay, whole genome sequencing, and RNAseq data. This analysis revealed complexity and variation in integrated vs. episomal HPV forms across PDXs and demonstrated that four PDXs predominantly contain episomal HPV16. Episomal status did not ensure favorable in vivo responses to cisplatin therapy, despite the more favorable prognosis previously attributed to episomal HPV + tumors; this could be due to the small number present in the dataset. Our analysis establishes PDX models as test platforms for novel therapies designed to target maintenance of the episomal forms of HPV16 that commonly appear in OPC.
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spelling doaj-art-25412f60534049e8a4a58ea3cdbc617f2025-08-20T01:56:20ZengElsevierTumour Virus Research2666-67902024-12-011820028510.1016/j.tvr.2024.200285HPV16 genome structure analysis in oropharyngeal cancer PDXs identifies tumors with integrated and episomal genomesClaire D. James0Raymonde O. Otoa1Aya H. Youssef2Christian T. Fontan3Malay K. Sannigrahi4Brad Windle5Devraj Basu6Iain M. Morgan7Virginia Commonwealth University (VCU), Philips Institute for Oral Health Research, School of Dentistry, Richmond, VA, 23298, USAVirginia Commonwealth University (VCU), Philips Institute for Oral Health Research, School of Dentistry, Richmond, VA, 23298, USAVirginia Commonwealth University (VCU), Philips Institute for Oral Health Research, School of Dentistry, Richmond, VA, 23298, USAVirginia Commonwealth University (VCU), Philips Institute for Oral Health Research, School of Dentistry, Richmond, VA, 23298, USADept. Otorhinolaryngology-Head and Neck Surgery, The University of Pennsylvania, Philadelphia, PA, USAVirginia Commonwealth University (VCU), Philips Institute for Oral Health Research, School of Dentistry, Richmond, VA, 23298, USA; VCU Massey Cancer Center, Richmond, VA, 23298, USADept. Otorhinolaryngology-Head and Neck Surgery, The University of Pennsylvania, Philadelphia, PA, USA; Corresponding author.Virginia Commonwealth University (VCU), Philips Institute for Oral Health Research, School of Dentistry, Richmond, VA, 23298, USA; VCU Massey Cancer Center, Richmond, VA, 23298, USA; Corresponding author. Virginia Commonwealth University (VCU), Philips Institute for Oral Health Research, School of Dentistry, Richmond, VA, 23298, USA.HPV + oropharyngeal squamous cell carcinoma (OPC) incidence recently surpassed cervical cancer and is the most common HPV-related cancer in the developed world. HPV16 is in ∼90 % of HPV + OPCs, with episomal genomes in the majority of cases. Most existing HPV16+ cancer cell lines derive from outside the oropharynx and harbor integrated HPV genomes. Thus, there is need for OPC preclinical models to evaluate standard and experimental therapeutics in the presence of episomal HPV16 oncogenic drivers. Here we characterize HPV genome structures in eight HPV16+ OPC patient-derived xenografts (PDXs), and evaluate their responses to standard chemotherapy. HPV genome state was investigated by combining Southern blot, T5 exonuclease assay, whole genome sequencing, and RNAseq data. This analysis revealed complexity and variation in integrated vs. episomal HPV forms across PDXs and demonstrated that four PDXs predominantly contain episomal HPV16. Episomal status did not ensure favorable in vivo responses to cisplatin therapy, despite the more favorable prognosis previously attributed to episomal HPV + tumors; this could be due to the small number present in the dataset. Our analysis establishes PDX models as test platforms for novel therapies designed to target maintenance of the episomal forms of HPV16 that commonly appear in OPC.http://www.sciencedirect.com/science/article/pii/S2666679024000090
spellingShingle Claire D. James
Raymonde O. Otoa
Aya H. Youssef
Christian T. Fontan
Malay K. Sannigrahi
Brad Windle
Devraj Basu
Iain M. Morgan
HPV16 genome structure analysis in oropharyngeal cancer PDXs identifies tumors with integrated and episomal genomes
Tumour Virus Research
title HPV16 genome structure analysis in oropharyngeal cancer PDXs identifies tumors with integrated and episomal genomes
title_full HPV16 genome structure analysis in oropharyngeal cancer PDXs identifies tumors with integrated and episomal genomes
title_fullStr HPV16 genome structure analysis in oropharyngeal cancer PDXs identifies tumors with integrated and episomal genomes
title_full_unstemmed HPV16 genome structure analysis in oropharyngeal cancer PDXs identifies tumors with integrated and episomal genomes
title_short HPV16 genome structure analysis in oropharyngeal cancer PDXs identifies tumors with integrated and episomal genomes
title_sort hpv16 genome structure analysis in oropharyngeal cancer pdxs identifies tumors with integrated and episomal genomes
url http://www.sciencedirect.com/science/article/pii/S2666679024000090
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