Comparative analysis of the tumor microbiome, molecular profiles, and immune cell abundances by HPV status in mucosal head and neck cancers and their impact on survival

References

• Siegel RL, Miller KD, Wagle NS, Jemal A. Cancer statistics, 2023. CA Cancer J Clin. 2023;73(1):17–8. doi: 10.3322/caac.21763.
   PubMed Web of Science ®Google Scholar
• Cadoni G, Giraldi L, Petrelli L, Pandolfini M, Giuliani M, Paludetti G, Pastorino R, Leoncini E, Arzani D, Almadori G, et al. Prognostic factors in head and neck cancer: a 10-year retrospective analysis in a single-institution in Italy. Acta Otorhinolaryngol Ital Organo Uff Della Soc Ital Otorinolaringol E Chir Cerv-Facc. 2017;37(6):458–466. doi: 10.14639/0392-100X-1246.
   PubMed Web of Science ®Google Scholar
• Kreimer AR, Clifford GM, Boyle P, Franceschi S. Human papillomavirus types in head and neck squamous cell carcinomas worldwide: a systematic review. Cancer Epidemiol Biomark Prev Publ Am Assoc Cancer Res Cosponsored Am Soc Prev Oncol. 2005;14(2):467–475. doi: 10.1158/1055-9965.EPI-04-0551.
   Google Scholar
• Chaturvedi AK, Anderson WF, Lortet-Tieulent J, Curado MP, Ferlay J, Franceschi S, Rosenberg PS, Bray F, Gillison ML. Worldwide trends in incidence rates for oral cavity and oropharyngeal cancers. J Clin Oncol Off J Am Soc Clin Oncol. 2013;31(36):4550–4559. doi: 10.1200/JCO.2013.50.3870.
   PubMed Web of Science ®Google Scholar
• Hennessey PT, Westra WH, Califano JA. Human papillomavirus and head and neck squamous cell carcinoma: recent evidence and clinical implications. J Dent Res. 2009;88(4):300–306. doi: 10.1177/0022034509333371.
   PubMed Web of Science ®Google Scholar
• Perri F, Longo F, Caponigro F, Sandomenico F, Guida A, Della Vittoria Scarpati G, Ottaiano A, Muto P, Ionna F. Management of HPV-Related squamous cell carcinoma of the head and neck: pitfalls and Caveat. Cancers. 2020;12(4):975. doi: 10.3390/cancers12040975.
   PubMed Web of Science ®Google Scholar
• Peltanova B, Raudenska M, Masarik M. Effect of tumor microenvironment on pathogenesis of the head and neck squamous cell carcinoma: a systematic review. Mol Cancer. 2019;18(1):63. doi: 10.1186/s12943-019-0983-5.
   PubMedGoogle Scholar
• Kalogirou EM, Tosios KI, Christopoulos PF. The role of macrophages in oral squamous cell carcinoma. Front Oncol. 2021;11:611115. doi: 10.3389/fonc.2021.611115.
   PubMedGoogle Scholar
• Costa NL, Valadares MC, Souza PPC, Mendonça EF, Oliveira JC, Silva TA, Batista AC. Tumor-associated macrophages and the profile of inflammatory cytokines in oral squamous cell carcinoma. Oral Oncol. 2013;49(3):216–223. doi: 10.1016/j.oraloncology.2012.09.012.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Wen L, Gong L, Yang C, Zeng Y-H, Wang X-Z, Zhao Y-W, Wei Y-Q. Prognostic significance of tumor-associated macrophages in solid tumor: a meta-analysis of the literature. PLoS One. 2012;7(12):e50946. doi: 10.1371/journal.pone.0050946.
   PubMed Web of Science ®Google Scholar
• Hanakawa H, Orita Y, Sato Y, Takeuchi M, Ohno K, Gion Y, Tsukahara K, Tamamura R, Ito T, Nagatsuka H, et al. Regulatory T-cell infiltration in tongue squamous cell carcinoma. Acta Otolaryngol (Stockh). 2014;134(8):859–864. doi: 10.3109/00016489.2014.918279.
   PubMed Web of Science ®Google Scholar
• Boucek J, Mrkvan T, Chovanec M, Kuchar M, Betka J, Boucek V, Hladikova M, Betka J, Eckschlager T, Rihova B, et al. Regulatory T cells and their prognostic value for patients with squamous cell carcinoma of the head and neck. J Cell Mol Med. 2010;14(1–2):426–433. doi: 10.1111/j.1582-4934.2008.00650.x.
   PubMed Web of Science ®Google Scholar
• Curry JM, Sprandio J, Cognetti D, Luginbuhl A, Bar-Ad V, Pribitkin E, Tuluc M. Tumor microenvironment in head and neck squamous cell carcinoma. Semin Oncol. 2014;41(2):217–234. doi: 10.1053/j.seminoncol.2014.03.003.
   PubMed Web of Science ®Google Scholar
• Hoyd R, Wheeler C, Liu Y, Singh MSJ, Muniak M, Denko N, Carbone DP, Xiaokui M, & Spakowicz D. Exogenous sequences in tumors and immune cells (exotic): a tool for estimating the microbe abundances in tumor RNAseq data. Cancer Res Commun. 2023;3(11):2375–85.
   PubMedGoogle Scholar
• Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol. 1995;57(1):289–300. doi: 10.1111/j.2517-6161.1995.tb02031.x.
   Google Scholar
• R core team. R: a language and environment for statistical computing. R Foundation for Statistical Computing; 2021. https://www.R-project.org/.
   Google Scholar
• Ang KK, Harris J, Wheeler R, Weber R, Rosenthal DI, Nguyen-Tân PF, Westra WH, Chung CH, Jordan RC, Lu C, et al. Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med. 2010;363(1):24–35. doi: 10.1056/NEJMoa0912217.
   PubMed Web of Science ®Google Scholar
• Shiao SL, Kershaw KM, Limon JJ, You S, Yoon J, Ko EY, Guarnerio J, Potdar AA, McGovern DPB, Bose S, et al. Commensal bacteria and fungi differentially regulate tumor responses to radiation therapy. Cancer Cell. 2021;39(9):1202–1213.e6. doi: 10.1016/j.ccell.2021.07.002.
   PubMed Web of Science ®Google Scholar
• Geller LT, Barzily-Rokni M, Danino T, Jonas OH, Shental N, Nejman D, Gavert N, Zwang Y, Cooper ZA, Shee K, et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Science. 2017;357(6356):1156–1160. doi: 10.1126/science.aah5043.
   PubMed Web of Science ®Google Scholar
• Zhi X, Lamperska K, Golusinski P, Schork NJ, Luczewski L, Kolenda T, Golusinski W, Masternak MM. Gene expression analysis of head and neck squamous cell carcinoma survival and recurrence. Oncotarget. 2015;6(1):547–555. doi: 10.18632/oncotarget.2772.
   PubMedGoogle Scholar
• Johnson DE. Targeting proliferation and survival pathways in head and neck cancer for therapeutic benefit. Chin J Cancer. 2012;31(7):319–326. doi: 10.5732/cjc.011.10404.
   PubMedGoogle Scholar
• Meric-Bernstam F, Larkin J, Tabernero J, Bonini C. Enhancing anti-tumour efficacy with immunotherapy combinations. Lancet Lond Engl. 2021;397(10278):1010–1022. doi: 10.1016/S0140-6736(20)32598-8.
   PubMed Web of Science ®Google Scholar
• Cassetta L, Kitamura T. Macrophage targeting: opening new possibilities for cancer immunotherapy. Immunology. 2018;155(3):285–293. doi: 10.1111/imm.12976.
   PubMed Web of Science ®Google Scholar
• Ino Y, Yamazaki-Itoh R, Shimada K, Iwasaki M, Kosuge T, Kanai Y, Hiraoka N. Immune cell infiltration as an indicator of the immune microenvironment of pancreatic cancer. Br J Cancer. 2013;108(4):914–923. doi: 10.1038/bjc.2013.32.
   PubMed Web of Science ®Google Scholar
• Jetten N, Verbruggen S, Gijbels MJ, Post MJ, de Winther MPJ, Donners MMPC. Anti-inflammatory M2, but not pro-inflammatory M1 macrophages promote angiogenesis in vivo. Angiogenesis. 2014;17(1):109–118. doi: 10.1007/s10456-013-9381-6.
   PubMed Web of Science ®Google Scholar
• Boutilier AJ, Elsawa SF. Macrophage polarization states in the tumor microenvironment. Int J Mol Sci. 2021;22(13):6995. doi: 10.3390/ijms22136995.
   PubMed Web of Science ®Google Scholar
• Leblond MM, Pérès EA, Helaine C, Gérault AN, Moulin D, Anfray C, Divoux D, Petit E, Bernaudin M, Valable S, et al. M2 macrophages are more resistant than M1 macrophages following radiation therapy in the context of glioblastoma. Oncotarget. 2017;8(42):72597–72612. doi: 10.18632/oncotarget.19994.
   PubMedGoogle Scholar
• Chiang CS, Fu SY, Wang SC, Yu C-F, Chen F-H, Lin C-M, Hong J-H. Irradiation promotes an m2 macrophage phenotype in tumor hypoxia. Front Oncol. 2012;2:89. doi: 10.3389/fonc.2012.00089.
   PubMedGoogle Scholar
• Rahal OM, Wolfe AR, Mandal PK, Larson R, Tin S, Jimenez C, Zhang D, Horton J, Reuben JM, McMurray JS, et al. Blocking interleukin (IL)4- and IL13-mediated phosphorylation of STAT6 (Tyr641) decreases M2 polarization of macrophages and protects against macrophage-mediated radioresistance of inflammatory breast cancer. Int J Radiat Oncol Biol Phys. 2018;100(4):1034–1043. doi: 10.1016/j.ijrobp.2017.11.043.
   PubMed Web of Science ®Google Scholar
• Okubo M, Kioi M, Nakashima H, Sugiura K, Mitsudo K, Aoki I, Taniguchi H, Tohnai I. M2-polarized macrophages contribute to neovasculogenesis, leading to relapse of oral cancer following radiation. Sci Rep. 2016;6(1):27548. doi: 10.1038/srep27548.
   PubMedGoogle Scholar
• Teresa Pinto A, Laranjeiro Pinto M, Patrícia Cardoso A, Monteiro C, Teixeira Pinto M, Filipe Maia A, Castro P, Figueira R, Monteiro A, Marques M, et al. Ionizing radiation modulates human macrophages towards a pro-inflammatory phenotype preserving their pro-invasive and pro-angiogenic capacities. Sci Rep. 2016;6(1):18765. doi: 10.1038/srep18765.
   PubMedGoogle Scholar
• Seifert L, Werba G, Tiwari S, Giao Ly NN, Nguy S, Alothman S, Alqunaibit D, Avanzi A, Daley D, Barilla R, et al. Radiation therapy induces macrophages to suppress T-Cell responses against pancreatic tumors in mice. Gastroenterology. 2016;150(7):1659–1672.e5. doi: 10.1053/j.gastro.2016.02.070.
   PubMed Web of Science ®Google Scholar
• Genard G, Lucas S, Michiels C. Reprogramming of tumor-associated macrophages with anticancer therapies: radiotherapy versus chemo- and immunotherapies. Front Immunol. 2017;8:828. doi: 10.3389/fimmu.2017.00828.
   PubMed Web of Science ®Google Scholar
• Genard G, Wera AC, Huart C, le Calve B, Penninckx S, Fattaccioli A, Tabarrant T, Demazy C, Ninane N, Heuskin A-C, et al. Proton irradiation orchestrates macrophage reprogramming through NFκB signaling. Cell Death Dis. 2018;9(7):728. doi: 10.1038/s41419-018-0757-9.
   PubMedGoogle Scholar
• Papadavid E, Stratigos AJ, Falagas ME. Imiquimod: an immune response modifier in the treatment of precancerous skin lesions and skin cancer. Expert Opin Pharmacother. 2007;8(11):1743–1755. doi: 10.1517/14656566.8.11.1743.
   PubMed Web of Science ®Google Scholar
• Zanganeh S, Hutter G, Spitler R, Lenkov O, Mahmoudi M, Shaw A, Pajarinen JS, Nejadnik H, Goodman S, Moseley M, et al. Iron oxide nanoparticles inhibit tumour growth by inducing pro-inflammatory macrophage polarization in tumour tissues. Nat Nanotechnol. 2016;11(11):986–994. doi: 10.1038/nnano.2016.168.
   PubMed Web of Science ®Google Scholar
• Pathria P, Louis TL, Varner JA. Targeting tumor-associated macrophages in cancer. Trends Immunol. 2019;40(4):310–327. doi: 10.1016/j.it.2019.02.003.
   PubMed Web of Science ®Google Scholar
• Badoual C, Hans S, Rodriguez J, Peyrard S, Klein C, Agueznay NEH, Mosseri V, Laccourreye O, Bruneval P, Fridman WH, et al. Prognostic value of tumor-infiltrating CD4+ T-cell subpopulations in head and neck cancers. Clin Cancer Res. 2006;12(2):465–472. doi: 10.1158/1078-0432.CCR-05-1886.
   PubMed Web of Science ®Google Scholar
• Kim SS, Shen S, Miyauchi S, Sanders PD, Franiak-Pietryga I, Mell L, Gutkind JS, Cohen EEW, Califano JA, Sharabi AB, et al. B cells improve overall survival in HPV-Associated squamous cell carcinomas and are activated by radiation and PD-1 blockade. Clin Cancer Res. 2020;26(13):3345–3359. doi: 10.1158/1078-0432.CCR-19-3211.
   PubMed Web of Science ®Google Scholar
• Kim SS, Sumner WA, Miyauchi S, Cohen EEW, Califano JA, Sharabi AB. Role of B cells in responses to checkpoint blockade immunotherapy and overall survival of cancer patients. Clin Cancer Res. 2021;27(22):6075–6082. doi: 10.1158/1078-0432.CCR-21-0697.
   PubMed Web of Science ®Google Scholar