Detection of Human Papillomavirus Integration in Brain Metastases from Oropharyngeal Tumors by Targeted Sequencing
Abstract
:1. Introduction
2. Materials and Methods
2.1. Tissue Collection
2.2. Immunohistochemistry for p16INK4a
2.3. RNAscope ISH for HPV16/18 E6/E7
2.4. PCR Detection of HPV Nucleic Acids
2.5. SureSelect Target Enrichment for Viral Nucleic Acids
2.6. Proteomics Sample Preparation
2.7. Liquid Chromatography Mass Spectrometry
2.8. Mass Spectrometry Data Processing
3. Results
3.1. Case Presentation
3.1.1. Case 1
3.1.2. Case 2
3.2. Molecular Analysis
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2020. CA Cancer J. Clin. 2020, 70, 7–30. [Google Scholar] [CrossRef]
- Vidal, L.; Gillison, M.L. Human papillomavirus in HNSCC: Recognition of a distinct disease type. Hematol. Oncol. Clin. N. Am. 2008, 22, 1125–1142, vii. [Google Scholar] [CrossRef] [PubMed]
- Ang, K.K.; Harris, J.; Wheeler, R.; Weber, R.; Rosenthal, D.I.; Nguyen-Tan, P.F.; Westra, W.H.; Chung, C.H.; Jordan, R.C.; Lu, C.; et al. Human papillomavirus and survival of patients with oropharyngeal cancer. N. Engl. J. Med. 2010, 363, 24–35. [Google Scholar] [CrossRef] [Green Version]
- Fakhry, C.; Westra, W.H.; Li, S.; Cmelak, A.; Ridge, J.A.; Pinto, H.; Forastiere, A.; Gillison, M.L. Improved survival of patients with human papillomavirus-positive head and neck squamous cell carcinoma in a prospective clinical trial. J. Natl. Cancer Inst. 2008, 100, 261–269. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gillison, M.L.; D’Souza, G.; Westra, W.; Sugar, E.; Xiao, W.; Begum, S.; Viscidi, R. Distinct risk factor profiles for human papillomavirus type 16-positive and human papillomavirus type 16-negative head and neck cancers. J. Natl. Cancer Inst. 2008, 100, 407–420. [Google Scholar] [CrossRef] [Green Version]
- Gillison, M.L.; Koch, W.M.; Capone, R.B.; Spafford, M.; Westra, W.H.; Wu, L.; Zahurak, M.L.; Daniel, R.W.; Viglione, M.; Symer, D.E.; et al. Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J. Natl. Cancer Inst. 2000, 92, 709–720. [Google Scholar] [CrossRef] [PubMed]
- O’Sullivan, B.; Huang, S.H.; Perez-Ordonez, B.; Massey, C.; Siu, L.L.; Weinreb, I.; Hope, A.; Kim, J.; Bayley, A.J.; Cummings, B.; et al. Outcomes of HPV-related oropharyngeal cancer patients treated by radiotherapy alone using altered fractionation. Radiother. Oncol. 2012, 103, 49–56. [Google Scholar] [CrossRef] [PubMed]
- Huang, S.H.; Perez-Ordonez, B.; Liu, F.F.; Waldron, J.; Ringash, J.; Irish, J.; Cummings, B.; Siu, L.L.; Kim, J.; Weinreb, I.; et al. Atypical clinical behavior of p16-confirmed HPV-related oropharyngeal squamous cell carcinoma treated with radical radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 2012, 82, 276–283. [Google Scholar] [CrossRef]
- Muller, S.; Khuri, F.R.; Kono, S.A.; Beitler, J.J.; Shin, D.M.; Saba, N.F. HPV positive squamous cell carcinoma of the oropharynx. Are we observing an unusual pattern of metastases? Head Neck Pathol. 2012, 6, 336–344. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ruzevick, J.; Olivi, A.; Westra, W.H. Metastatic squamous cell carcinoma to the brain: An unrecognized pattern of distant spread in patients with HPV-related head and neck cancer. J. Neurooncol. 2013, 112, 449–454. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tiedemann, D.; Jakobsen, K.K.; von Buchwald, C.; Gronhoj, C. Systematic review on location and timing of distant progression in human papillomavirus-positive and human papillomavirus-negative oropharyngeal squamous cell carcinomas. Head Neck 2019, 41, 793–798. [Google Scholar] [CrossRef]
- Trosman, S.J.; Koyfman, S.A.; Ward, M.C.; Al-Khudari, S.; Nwizu, T.; Greskovich, J.F.; Lamarre, E.D.; Scharpf, J.; Khan, M.J.; Lorenz, R.R.; et al. Effect of human papillomavirus on patterns of distant metastatic failure in oropharyngeal squamous cell carcinoma treated with chemoradiotherapy. JAMA Otolaryngol. Head Neck Surg. 2015, 141, 457–462. [Google Scholar] [CrossRef] [Green Version]
- Bulut, O.C.; Lindel, K.; Hauswald, H.; Brandt, R.; Klauschen, F.; Wolf, J.; Wolf, T.; Plinkert, P.K.; Simon, C.; Weichert, W.; et al. Clinical and molecular characteristics of HNSCC patients with brain metastases: A retrospective study. Eur. Arch. Otorhinolaryngol. 2014, 271, 1715–1722. [Google Scholar] [CrossRef]
- Liu, A.K.; Wu, J.; Berthelet, E.; Lalani, N.; Chau, N.; Tran, E.; Hamilton, S.N. Clinical features of head and neck cancer patients with brain metastases: A retrospective study of 88 cases. Oral Oncol. 2021, 112, 105086. [Google Scholar] [CrossRef]
- Jaber, J.J.; Murrill, L.; Clark, J.I.; Johnson, J.T.; Feustel, P.J.; Mehta, V. Robust Differences in p16-Dependent Oropharyngeal Squamous Cell Carcinoma Distant Metastasis: Implications for Targeted Therapy. Otolaryngol. Head Neck Surg. 2015, 153, 209–217. [Google Scholar] [CrossRef] [PubMed]
- Wichmann, G.; Rosolowski, M.; Krohn, K.; Kreuz, M.; Boehm, A.; Reiche, A.; Scharrer, U.; Halama, D.; Bertolini, J.; Bauer, U.; et al. The role of HPV RNA transcription, immune response-related gene expression and disruptive TP53 mutations in diagnostic and prognostic profiling of head and neck cancer. Int. J. Cancer 2015, 137, 2846–2857. [Google Scholar] [CrossRef] [PubMed]
- Pett, M.; Coleman, N. Integration of high-risk human papillomavirus: A key event in cervical carcinogenesis? J. Pathol. 2007, 212, 356–367. [Google Scholar] [CrossRef]
- Pinatti, L.M.; Walline, H.M.; Carey, T.E. Human Papillomavirus Genome Integration and Head and Neck Cancer. J. Dent. Res. 2018, 97, 691–700. [Google Scholar] [CrossRef]
- Cancer Genome Atlas Research Network; Albert Einstein College of Medicine; Analytical Biological Services; Barretos Cancer Hospital; Baylor College of Medicine; Beckman Research Institute of City of Hope; Buck Institute for Research on Aging; Canada’s Michael Smith Genome Sciences Centre; Harvard Medical School; Helen, F.; et al. Integrated genomic and molecular characterization of cervical cancer. Nature 2017, 543, 378–384. [Google Scholar] [CrossRef] [PubMed]
- Parfenov, M.; Pedamallu, C.S.; Gehlenborg, N.; Freeman, S.S.; Danilova, L.; Bristow, C.A.; Lee, S.; Hadjipanayis, A.G.; Ivanova, E.V.; Wilkerson, M.D.; et al. Characterization of HPV and host genome interactions in primary head and neck cancers. Proc. Natl. Acad. Sci. USA 2014, 111, 15544–15549. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vojtechova, Z.; Sabol, I.; Salakova, M.; Turek, L.; Grega, M.; Smahelova, J.; Vencalek, O.; Lukesova, E.; Klozar, J.; Tachezy, R. Analysis of the integration of human papillomaviruses in head and neck tumours in relation to patients’ prognosis. Int. J. Cancer 2016, 138, 386–395. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Koneva, L.A.; Zhang, Y.; Virani, S.; Hall, P.B.; McHugh, J.B.; Chepeha, D.B.; Wolf, G.T.; Carey, T.E.; Rozek, L.S.; Sartor, M.A. HPV Integration in HNSCC Correlates with Survival Outcomes, Immune Response Signatures, and Candidate Drivers. Mol. Cancer Res. 2018, 16, 90–102. [Google Scholar] [CrossRef] [Green Version]
- Walline, H.M.; Komarck, C.M.; McHugh, J.B.; Bellile, E.L.; Brenner, J.C.; Prince, M.E.; McKean, E.L.; Chepeha, D.B.; Wolf, G.T.; Worden, F.P.; et al. Genomic Integration of High-Risk HPV Alters Gene Expression in Oropharyngeal Squamous Cell Carcinoma. Mol. Cancer Res. 2016, 14, 941–952. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hashida, Y.; Taniguchi, A.; Yawata, T.; Hosokawa, S.; Murakami, M.; Hiroi, M.; Ueba, T.; Daibata, M. Prevalence of human cytomegalovirus, polyomaviruses, and oncogenic viruses in glioblastoma among Japanese subjects. Infect. Agent. Cancer 2015, 10, 3. [Google Scholar] [CrossRef] [Green Version]
- Li, H.; Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25, 1754–1760. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dobin, A.; Davis, C.A.; Schlesinger, F.; Drenkow, J.; Zaleski, C.; Jha, S.; Batut, P.; Chaisson, M.; Gingeras, T.R. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 2013, 29, 15–21. [Google Scholar] [CrossRef]
- Pino, L.K.; Just, S.C.; MacCoss, M.J.; Searle, B.C. Acquiring and Analyzing Data Independent Acquisition Proteomics Experiments without Spectrum Libraries. Mol. Cell Proteom. 2020, 19, 1088–1103. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gessulat, S.; Schmidt, T.; Zolg, D.P.; Samaras, P.; Schnatbaum, K.; Zerweck, J.; Knaute, T.; Rechenberger, J.; Delanghe, B.; Huhmer, A.; et al. Prosit: Proteome-wide prediction of peptide tandem mass spectra by deep learning. Nat. Methods 2019, 16, 509–518. [Google Scholar] [CrossRef]
- Searle, B.C.; Swearingen, K.E.; Barnes, C.A.; Schmidt, T.; Gessulat, S.; Kuster, B.; Wilhelm, M. Generating high quality libraries for DIA MS with empirically corrected peptide predictions. Nat. Commun. 2020, 11, 1548. [Google Scholar] [CrossRef] [Green Version]
- Amodei, D.; Egertson, J.; MacLean, B.X.; Johnson, R.; Merrihew, G.E.; Keller, A.; Marsh, D.; Vitek, O.; Mallick, P.; MacCoss, M.J. Improving Precursor Selectivity in Data-Independent Acquisition Using Overlapping Windows. J. Am. Soc. Mass Spectrom. 2019, 30, 669–684. [Google Scholar] [CrossRef]
- Chambers, M.C.; Maclean, B.; Burke, R.; Amodei, D.; Ruderman, D.L.; Neumann, S.; Gatto, L.; Fischer, B.; Pratt, B.; Egertson, J.; et al. A cross-platform toolkit for mass spectrometry and proteomics. Nat. Biotechnol. 2012, 30, 918–920. [Google Scholar] [CrossRef]
- Searle, B.C.; Pino, L.K.; Egertson, J.D.; Ting, Y.S.; Lawrence, R.T.; MacLean, B.X.; Villen, J.; MacCoss, M.J. Chromatogram libraries improve peptide detection and quantification by data independent acquisition mass spectrometry. Nat. Commun. 2018, 9, 5128. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Olmedo-Nieva, L.; Munoz-Bello, J.O.; Contreras-Paredes, A.; Lizano, M. The Role of E6 Spliced Isoforms (E6*) in Human Papillomavirus-Induced Carcinogenesis. Viruses 2018, 10, 45. [Google Scholar] [CrossRef] [Green Version]
- Schmitz, M.; Driesch, C.; Jansen, L.; Runnebaum, I.B.; Durst, M. Non-random integration of the HPV genome in cervical cancer. PLoS ONE 2012, 7, e39632. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bodelon, C.; Untereiner, M.E.; Machiela, M.J.; Vinokurova, S.; Wentzensen, N. Genomic characterization of viral integration sites in HPV-related cancers. Int. J. Cancer 2016, 139, 2001–2011. [Google Scholar] [CrossRef] [PubMed]
- Peter, M.; Rosty, C.; Couturier, J.; Radvanyi, F.; Teshima, H.; Sastre-Garau, X. MYC activation associated with the integration of HPV DNA at the MYC locus in genital tumors. Oncogene 2006, 25, 5985–5993. [Google Scholar] [CrossRef] [Green Version]
- de Bree, R.; Mehta, D.M.; Snow, G.B.; Quak, J.J. Intracranial metastases in patients with squamous cell carcinoma of the head and neck. Otolaryngol. Head Neck Surg. 2001, 124, 217–221. [Google Scholar] [CrossRef] [PubMed]
- Ghosh-Laskar, S.; Agarwal, J.P.; Yathiraj, P.H.; Tanawade, P.; Panday, R.; Gupta, T.; Budrukkar, A.; Murthy, V. Brain metastasis from nonnasopharyngeal head and neck squamous cell carcinoma: A case series and review of literature. J. Cancer Res. Ther. 2016, 12, 1160–1163. [Google Scholar] [CrossRef] [PubMed]
- Harle, A.; Guillet, J.; Thomas, J.; Demange, J.; Dolivet, G.; Peiffert, D.; Leroux, A.; Sastre-Garau, X. HPV insertional pattern as a personalized tumor marker for the optimized tumor diagnosis and follow-up of patients with HPV-associated carcinomas: A case report. BMC Cancer 2019, 19, 277. [Google Scholar] [CrossRef] [PubMed]
- Li, T.; Unger, E.R.; Batra, D.; Sheth, M.; Steinau, M.; Jasinski, J.; Jones, J.; Rajeevan, M.S. Universal Human Papillomavirus Typing Assay: Whole-Genome Sequencing following Target Enrichment. J. Clin. Microbiol. 2017, 55, 811–823. [Google Scholar] [CrossRef] [Green Version]
- Montgomery, N.D.; Parker, J.S.; Eberhard, D.A.; Patel, N.M.; Weck, K.E.; Sharpless, N.E.; Hu, Z.; Hayes, D.N.; Gulley, M.L. Identification of Human Papillomavirus Infection in Cancer Tissue by Targeted Next-generation Sequencing. Appl. Immunohistochem. Mol. Morphol. 2016, 24, 490–495. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carpen, T.; Syrjanen, S.; Jouhi, L.; Randen-Brady, R.; Haglund, C.; Makitie, A.; Mattila, P.S.; Hagstrom, J. Epstein-Barr virus (EBV) and polyomaviruses are detectable in oropharyngeal cancer and EBV may have prognostic impact. Cancer Immunol. Immunother. 2020, 69, 1615–1626. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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McEllin, B.; Searle, B.C.; DePledge, L.; Sun, G.; Cobbs, C.; Karimi, M. Detection of Human Papillomavirus Integration in Brain Metastases from Oropharyngeal Tumors by Targeted Sequencing. Viruses 2021, 13, 1536. https://doi.org/10.3390/v13081536
McEllin B, Searle BC, DePledge L, Sun G, Cobbs C, Karimi M. Detection of Human Papillomavirus Integration in Brain Metastases from Oropharyngeal Tumors by Targeted Sequencing. Viruses. 2021; 13(8):1536. https://doi.org/10.3390/v13081536
Chicago/Turabian StyleMcEllin, Brian, Brian C. Searle, Lisa DePledge, George Sun, Charles Cobbs, and Mohsen Karimi. 2021. "Detection of Human Papillomavirus Integration in Brain Metastases from Oropharyngeal Tumors by Targeted Sequencing" Viruses 13, no. 8: 1536. https://doi.org/10.3390/v13081536