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Article

New Insights into the Impact of Human Papillomavirus on Oral Cancer in Young Patients: Proteomic Approach Reveals a Novel Role for S100A8

by
Marisol Miranda-Galvis
1,2,
Carolina Carneiro Soares
2,3,
Carolina Moretto Carnielli
4,
Jaqueline Ramalho Buttura
5,
Raisa Sales de Sá
2,
Estela Kaminagakura
6,
Fabio Albuquerque Marchi
7,8,
Adriana Franco Paes Leme
4,
Clóvis A. Lópes Pinto
9,
Alan Roger Santos-Silva
2,
Rogerio Moraes Castilho
1,10,
Luiz Paulo Kowalski
11,12 and
Cristiane Helena Squarize
1,10,*
1
Laboratory of Epithelial Biology, Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, Ann Arbor, MI 48109, USA
2
Oral Diagnosis Department, Piracicaba Dental School, University of Campinas (UNICAMP), Piracicaba 13414-903, SP, Brazil
3
Department of Microbiology, Immune Biology, and Genetics, Center for Molecular Biology, University of Vienna, 1030 Vienna, Austria
4
Brazilian Biosciences National Laboratory (LNBio), Brazilian Center for Research in Energy and Materials (CNPEM), Campinas 13083-970, SP, Brazil
5
Laboratory of Bioinformatics and Computational Biology, A.C.Camargo Cancer Center (CIPE), São Paulo 01508-010, SP, Brazil
6
Department of Bioscience and Oral Diagnosis, Science and Technology Institute, University of São Paulo State (UNESP), São José dos Campos 01049-010, SP, Brazil
7
Center for Translational Research in Oncology, Cancer Institute of the State of São Paulo (ICESP), São Paulo 01246-000, SP, Brazil
8
Comprehensive Center for Precision Oncology, University of São Paulo, São Paulo 05508-900, SP, Brazil
9
Department of Anatomic Pathology, A.C.Camargo Cancer Center, São Paulo 01509-001, SP, Brazil
10
Rogel Cancer Center, University of Michigan, Ann Arbor, MI 48109, USA
11
Head and Neck Surgery Department, Medical School, University of São Paulo, São Paulo 05508-900, SP, Brazil
12
Department of Head and Neck Surgery and Otorhinolaryngology, A.C.Camargo Cancer Center, São Paulo 01509-001, SP, Brazil
*
Author to whom correspondence should be addressed.
Cells 2023, 12(9), 1323; https://doi.org/10.3390/cells12091323
Submission received: 8 March 2023 / Revised: 29 April 2023 / Accepted: 2 May 2023 / Published: 5 May 2023
(This article belongs to the Collection Tumor Metabolism and Therapy)

Abstract

Human papillomavirus (HPV) infection has recently been linked to a subset of cancers affecting the oral cavity. However, the molecular mechanisms underlying HPV-driven oral squamous cell carcinoma (OSCC) onset and progression are poorly understood. Methods: We performed MS-based proteomics profiling based on HPV status in OSCC in young patients, following biological characterization and cell assays to explore the proteome functional landscape. Results: Thirty-nine proteins are differentially abundant between HPV (+) and HPV (−) OSCC. Among them, COPS3, DYHC1, and S100A8 are unfavorable for tumor recurrence and survival, in contrast to A2M and Serpine1, low levels of which show an association with better DFS. Remarkably, S100A8 is considered an independent prognostic factor for lower survival rates, and at high levels, it alters tumor-associated immune profiling, showing a lower proportion of M1 macrophages and dendritic cells. HPV (+) OSCC also displayed the pathogen-associated patterns receptor that, when activated, triggered the S100A8 and NFκB inflammatory responses. Conclusion: HPV (+) OSCC has a peculiar microenvironment pattern distinctive from HPV (−), involving the expression of pathogen-associated pattern receptors, S100A8 overexpression, and NFκB activation and responses, which has important consequences in prognosis and may guide therapeutic decisions.
Keywords: oral cancer; HPV; proteomics; prognosis; S100A8 oral cancer; HPV; proteomics; prognosis; S100A8

Share and Cite

MDPI and ACS Style

Miranda-Galvis, M.; Carneiro Soares, C.; Moretto Carnielli, C.; Ramalho Buttura, J.; Sales de Sá, R.; Kaminagakura, E.; Marchi, F.A.; Paes Leme, A.F.; Lópes Pinto, C.A.; Santos-Silva, A.R.; et al. New Insights into the Impact of Human Papillomavirus on Oral Cancer in Young Patients: Proteomic Approach Reveals a Novel Role for S100A8. Cells 2023, 12, 1323. https://doi.org/10.3390/cells12091323

AMA Style

Miranda-Galvis M, Carneiro Soares C, Moretto Carnielli C, Ramalho Buttura J, Sales de Sá R, Kaminagakura E, Marchi FA, Paes Leme AF, Lópes Pinto CA, Santos-Silva AR, et al. New Insights into the Impact of Human Papillomavirus on Oral Cancer in Young Patients: Proteomic Approach Reveals a Novel Role for S100A8. Cells. 2023; 12(9):1323. https://doi.org/10.3390/cells12091323

Chicago/Turabian Style

Miranda-Galvis, Marisol, Carolina Carneiro Soares, Carolina Moretto Carnielli, Jaqueline Ramalho Buttura, Raisa Sales de Sá, Estela Kaminagakura, Fabio Albuquerque Marchi, Adriana Franco Paes Leme, Clóvis A. Lópes Pinto, Alan Roger Santos-Silva, and et al. 2023. "New Insights into the Impact of Human Papillomavirus on Oral Cancer in Young Patients: Proteomic Approach Reveals a Novel Role for S100A8" Cells 12, no. 9: 1323. https://doi.org/10.3390/cells12091323

APA Style

Miranda-Galvis, M., Carneiro Soares, C., Moretto Carnielli, C., Ramalho Buttura, J., Sales de Sá, R., Kaminagakura, E., Marchi, F. A., Paes Leme, A. F., Lópes Pinto, C. A., Santos-Silva, A. R., Moraes Castilho, R., Kowalski, L. P., & Squarize, C. H. (2023). New Insights into the Impact of Human Papillomavirus on Oral Cancer in Young Patients: Proteomic Approach Reveals a Novel Role for S100A8. Cells, 12(9), 1323. https://doi.org/10.3390/cells12091323

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