5,031
Views
102
CrossRef citations to date
0
Altmetric
Original Research

Treatment-naïve HPV+ head and neck cancers display a T-cell-inflamed phenotype distinct from their HPV- counterparts that has implications for immunotherapy

, , , , , & show all
Article: e1498439 | Received 18 Apr 2018, Accepted 04 Jul 2018, Published online: 30 Jul 2018

References

  • Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252–264.
  • Topalian SL, Drake CG, Pardoll DM. Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell. 2015;27:450–461.
  • Del Paggio JC. Immunotherapy: cancer immunotherapy and the value of cure. Nat Rev Clin Oncol. 2018;10:253.
  • Ferlay J, Shin H-R, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010;127:2893–2917.
  • Baxi S, Fury M, Ganly I, Rao S, Pfister DG. Ten years of progress in head and neck cancers. J Natl Compr Canc Netw. 2012;10:806–810.
  • Marur S, D’Souza G, Westra WH, Forastiere AA. HPV-associated head and neck cancer: a virus-related cancer epidemic. Lancet Oncol. 2010;11:781–789.
  • Nichols AC, Palma DA, Dhaliwal SS, Tan S, Theuer J, Chow W, Rajakumar C, Um S, Mundi N, Berk S, et al. The epidemic of human papillomavirus and oropharyngeal cancer in a Canadian population. Current Oncology. 2013;20:212–219.
  • The Cancer Genome Atlas Research Network. Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature. 2015;517:576–582.
  • Mittal S, Banks L. Molecular mechanisms underlying human papillomavirus E6 and E7 oncoprotein-induced cell transformation. Mutat Res Rev Mutat. 2017;772:23–35.
  • 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;363:24–35.
  • Fakhry C, Westra WH, Li S, Cmelak A, Ridge JA, Pinto H, Forastiere A, Gillison ML. 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.
  • Solomon B, Young RJ, Bressel M, Urban D, Hendry S, Thai A, Angel C, Haddad A, Kowanetz M, Fua T, et al. Prognostic Significance of PD-L1+and CD8+immune cells in HPV+oropharyngeal squamous cell carcinoma. Cancer Immunol Res. 2018;6:295–304.
  • Mandal R, Şenbabaoğlu Y, Desrichard A, Havel JJ, Dalin MG, Riaz N, Lee K-W, Ganly I, Hakimi AA, Chan TA, et al. The head and neck cancer immune landscape and its immunotherapeutic implications. JCI Insight. 2016;1:e89829.
  • Montler R, Bell RB, Thalhofer C, Leidner R, Feng Z, Fox BA, Cheng AC, Bui TG, Tucker C, Hoen H, et al. OX40, PD-1 and CTLA-4 are selectively expressed on tumor-infiltrating T cells in head and neck cancer. Clin Transl Immunol. 2016;5:e70.
  • Lyford-Pike S, Peng S, Young GD, Taube JM, Westra WH, Akpeng B, Bruno TC, Richmon JD, Wang H, Bishop JA, et al. Evidence for a role of the PD-1: PD-L1pathway in immune resistance of HPV-associated head and neck squamous cell carcinoma. Cancer Res. 2013;73:1733–1741.
  • Feng Z, Bethmann D, Kappler M, Ballesteros-Merino C, Eckert A, Bell RB, Cheng A, Bui T, Leidner R, Urba WJ, et al. Multiparametric immune profiling in HPV- oral squamous cell cancer. JCI Insight. 2017;2(14). pii: 93652. doi:10.1172/jci.insight.93652.
  • Gajewski TF, Schreiber H, Fu Y-X. Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol. 2013;14:1014–1022.
  • Newman AM, Liu CL, Green MR, Gentles AJ, Feng W, Xu Y, Hoang CD, Diehn M, Alizadeh AA. Robust enumeration of cell subsets from tissue expression profiles. Nat Methods. 2015;12:453–457.
  • Hoadley KA, Yau C, Hinoue T, Wolf DM, Lazar AJ, Drill E, Shen R, Taylor AM, Cherniack AD, Thorsson V, et al. Cell-of-origin patterns dominate the molecular classification of 10,000 tumors from 33 types of cancer. Cell. 2018;173:291–296.
  • Mucida D, Salek-Ardakani S. Regulation of TH17 cells in the mucosal surfaces. J Allergy Clin Immunol. 2009;123:997–1003.
  • Fang D, Zhu J. Dynamic balance between master transcription factors determines the fates and functions of CD4 T cell and innate lymphoid cell subsets. J Exp Med. 2017;214:1861–1876.
  • Gameiro SF, Zhang A, Ghasemi F, Barrett JW, Nichols AC, Mymryk JS. Analysis of class I major histocompatibility complex gene transcription in human tumors caused by human papillomavirus infection. Viruses. 2017;9:252.
  • Muller AJ, DuHadaway JB, Donover PS, Sutanto-Ward E, Prendergast GC. Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy. Nat Med. 2005;11:312–319.
  • Lund RJ, Chen Z, Scheinin J, Lahesmaa R. Early target genes of IL-12 and STAT4 signaling in th cells. J Immunol. 2004;172:6775–6782.
  • Shi Q, Yin Z, Zhao B, Sun F, Yu H, Yin X, Zhang L, Wang S. PGE2 elevates IL-23 production in human dendritic cells via a cAMP dependent pathway. Mediators Inflamm. 2015;2015:984690–984697. doi:10.1155/2015/984690.
  • Pflanz S, Timans JC, Cheung J, Rosales R, Kanzler H, Gilbert J, Hibbert L, Churakova T, Travis M, Vaisberg E, et al. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4+ T cells. Immunity. 2002;16:779–790.
  • Mitchell DA, Batich KA, Gunn MD, Huang M-N, Sanchez-Perez L, Nair SK, Congdon KL, Reap EA, Archer GE, Desjardins A, et al. Tetanus toxoid and CCL3 improve dendritic cell vaccines in mice and glioblastoma patients. Nature. 2015;519:366–369.
  • Castellino F, Huang AY, Altan-Bonnet G, Stoll S, Scheinecker C, Germain RN. Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell-dendritic cell interaction. Nature. 2006;440:890–895.
  • Chen F, Yin S, Niu L, Luo J, Wang B, Xu Z, Yang G. Expression of the chemokine receptor CXCR3 correlates with dendritic cell recruitment and prognosis in gastric cancer. Genet Test Mol Biomarkers. 2018;22:35–42.
  • Mikucki ME, Skitzki JJ, Frelinger JG, Odunsi K, Gajewski TF, Luster AD, Evans SS. Unlocking tumor vascular barriers with CXCR3: implications for cancer immunotherapy. Oncoimmunology. 2016;5:e1116675.
  • Anderson AC, Joller N, Kuchroo VK. Lag-3, Tim-3, and TIGIT: co-inhibitory receptors with specialized functions in immune regulation. Immunity. 2016;44:989–1004.
  • Jie H-B, Gildener-Leapman N, Li J, Srivastava RM, Gibson SP, Whiteside TL, Ferris RL. Intratumoral regulatory T cells upregulate immunosuppressive molecules in head and neck cancer patients. Br J Cancer. 2013;109:2629–2635.
  • Simoni Y, Becht E, Fehlings M, Loh CY, Koo S-L, Teng KWW, Yeong JPS, Nahar R, Zhang T, Kared H, et al. Bystander CD8+ T cells are abundant and phenotypically distinct in human tumour infiltrates. Nature. 2018;557:575–579.
  • de Ruiter EJ, Ooft ML, Devriese LA, Willems SM. The prognostic role of tumor infiltrating T-lymphocytes in squamous cell carcinoma of the head and neck: A systematic review and meta-analysis. Oncoimmunology. 2017;6:e1356148.
  • Gros A, Parkhurst MR, Tran E, Pasetto A, Robbins PF, Ilyas S, Prickett TD, Gartner JJ, Crystal JS, Roberts IM, et al. Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients. Nat Med. 2016;22:433–438.
  • Routy B, Le Chatelier E, Derosa L, Duong CPM, Alou MT, Daillère R, Fluckiger A, Messaoudene M, Rauber C, Roberti MP, et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science. 2018;359:91–97.
  • Sadelain M, Rivière I, Riddell S. Therapeutic T cell engineering. Nature. 2017;545:423–431.
  • Yarchoan M, Hopkins A, Jaffee EM. Tumor mutational burden and response rate to PD-1 inhibition. N Engl J Med. 2017;377:2500–2501.
  • Chen X, Yan B, Lou H, Shen Z, Tong F, Zhai A, Wei L, Zhang F. Immunological network analysis in HPV associated head and neck squamous cancer and implications for disease prognosis. Mol Immunol. 2018;96:28–36.
  • Keck MK, Zuo Z, Khattri A, Stricker TP, Brown CD, Imanguli M, Rieke D, Endhardt K, Fang P, Brägelmann J, et al. Integrative analysis of head and neck cancer identifies two biologically distinct HPV and three non-HPV subtypes. Clin Cancer Res. 2015;21:870–881.
  • Chakravarthy A, Henderson S, Thirdborough SM, Ottensmeier CH, Su X, Lechner M, Feber A, Thomas GJ, Fenton TR. Human papillomavirus drives tumor development throughout the head and neck: improved prognosis is associated with an immune response largely restricted to the oropharynx. J Clin Oncol. 2016;34:4132–4141.
  • Conti-Freitas LC, Foss-Freitas MC, Mamede RCM, Foss NT. Interferon-gamma and interleukin-10 production by mononuclear cells from patients with advanced head and neck cancer. Clinics (Sao Paulo). 2012;67:587–590.
  • Calzascia T, Pellegrini M, Hall H, Sabbagh L, Ono N, Elford AR, Mak TW, Ohashi PS. TNF-alpha is critical for antitumor but not antiviral T cell immunity in mice. J Clin Invest. 2007;117:3833–3845.
  • Spranger S, Bao R, Gajewski TF. Melanoma-intrinsic β-catenin signalling prevents anti-tumour immunity. Nature. 2015;523:231–235.
  • Gajewski TF, Corrales L, Williams J, Horton B, Sivan A, Spranger S. Cancer immunotherapy targets based on understanding the t cell-inflamed versus non-T cell-inflamed tumor microenvironment. Adv Exp Med Biol. 2017;1036:19–31.
  • Nguyen N, Bellile E, Thomas D, McHugh J, Rozek L, Virani S, Peterson L, Carey TE, Walline H, Moyer J, et al. Tumor infiltrating lymphocytes and survival in patients with head and neck squamous cell carcinoma. Head Neck. 2016;38:1074–1084.
  • Gameiro SF, Kolendowski B, Zhang A, Barrett JW, Nichols AC, Torchia J, Mymryk JS. Human papillomavirus dysregulates the cellular apparatus controlling the methylation status of H3K27 in different human cancers to consistently alter gene expression regardless of tissue of origin. Oncotarget. 2017;8(42):27564–725761.
  • Thorsson V, Gibbs DL, Brown SD, Wolf D, Bortone DS, Ou Yang T-H, Porta-Pardo E, Gao GF, Plaisier CL, Eddy JA, et al. The immune landscape of cancer. Immunity. 2018;48:812–814.
  • Mayakonda A, Koeffler HP. Maftools: efficient analysis, visualization and summarization of MAF files from large-scale cohort based cancer studies. bioRxiv. 2016;052662. doi:10.1101/052662.