Two immune-enhanced molecular subtypes differ in inflammation, checkpoint signaling and outcome of advanced head and neck squamous cell carcinoma

References

• Siegel RL, Miller KD, Jemal A. Cancer Statistics, 2017. CA Cancer J Clin. 2017;67:7–30. doi:10.3322/caac.21387.
   PubMed Web of Science ®Google Scholar
• Chi AC, Day TA, Neville BW. Oral cavity and oropharyngeal squamous cell carcinoma–an update. CA Cancer J Clin. 2015;65:401–21. doi:10.3322/caac.21293. PMID:26215712
   PubMed Web of Science ®Google Scholar
• Cooper JS, Zhang Q, Pajak TF, Forastiere AA, Jacobs J, Saxman SB, Kish JA, Kim HE, Cmelak AJ, Rotman M, et al. Long-term follow-up of the RTOG 9501/intergroup phase III trial: postoperative concurrent radiation therapy and chemotherapy in high-risk squamous cell carcinoma of the head and neck. Int J Radiat Oncol Biol Phys. 2012;84:1198–205. doi:10.1016/j.ijrobp.2012.05.008. PMID:22749632
   PubMed Web of Science ®Google Scholar
• Wolchok JD. PD-1 Blockers. Cell. 2015;162:937. doi:10.1016/j.cell.2015.07.045. PMID:26317459
   PubMed Web of Science ®Google Scholar
• Seiwert TY, Burtness B, Mehra R, Weiss J, Berger R, Eder JP, et al. Safety and clinical activity of pembrolizumab for treatment of recurrent or metastatic squamous cell carcinoma of the head and neck (KEYNOTE-012): an open-label, multicentre, phase 1b trial. Lancet Oncol. 2016;17:956–65. doi:10.1016/S1470-2045(16)30066-3. PMID:27247226
   PubMed Web of Science ®Google Scholar
• Ferris RL, Blumenschein G, Jr., Fayette J, Guigay J, Colevas AD, Licitra L, et al. Nivolumab for Recurrent Squamous-Cell Carcinoma of the Head and Neck. N Engl J Med. 2016;375:1856–67. doi:10.1056/NEJMoa1602252. PMID:27718784
   PubMed Web of Science ®Google Scholar
• Chow LQ, Haddad R, Gupta S, Mahipal A, Mehra R, Tahara M, Berger R, Eder JP, Burtness B, Lee SH, et al. Antitumor Activity of Pembrolizumab in Biomarker-Unselected Patients With Recurrent and/or Metastatic Head and Neck Squamous Cell Carcinoma: Results From the Phase Ib KEYNOTE-012 Expansion Cohort. J Clin Oncol. 2016;34:3838–3845. doi:10.1200/JCO.2016.68.1478. PMID: 27646946
   PubMed Web of Science ®Google Scholar
• Bauml J, Seiwert TY, Pfister DG, Worden F, Liu SV, Gilbert J, Saba NF, Weiss J, Wirth L, Sukari A, et al. Pembrolizumab for Platinum- and Cetuximab-Refractory Head and Neck Cancer: Results From a Single-Arm, Phase II Study. J Clin Oncol. 2017;35:1542–9. doi:10.1200/JCO.2016.70.1524. PMID:28328302
   PubMed Web of Science ®Google Scholar
• Chow MT, Moller A, Smyth MJ. Inflammation and immune surveillance in cancer. Semin Cancer Biol. 2012;22:23–32. doi:10.1016/j.semcancer.2011.12.004. PMID:22210181
   PubMed Web of Science ®Google Scholar
• Geary CD, Sun JC. Memory responses of natural killer cells. Semin Immunol. 2017;31:11–19. doi:10.1016/j.smim.2017.08.012.PMID:28863960
   PubMed Web of Science ®Google Scholar
• Chikuma S. CTLA-4, an Essential Immune-Checkpoint for T-Cell Activation. Curr Top Microbiol Immunol. 2017 [Epub ahead of print]. doi:10.1007/82_2017_61. PMID:28900679
   PubMed Web of Science ®Google Scholar
• Swatler J, Kozlowska E. [Immune checkpointtargeted cancer immunotherapies]. Postepy Hig Med Dosw (Online). 2016;70:25–42. doi:10.5604/17322693.1192926. PMID:26864062
   PubMedGoogle Scholar
• Ndiaye C, Mena M, Alemany L, Arbyn M, Castellsague X, Laporte L, et al. HPV DNA, E6/E7 mRNA, and p16INK4 a detection in head and neck cancers: a systematic review and meta-analysis. Lancet Oncol. 2014;15:1319–31. doi:10.1016/S1470-2045(14)70471-1. PMID:25439690
   PubMed Web of Science ®Google Scholar
• Maxwell JH, Grandis JR, Ferris RL. HPV-Associated Head and Neck Cancer: Unique Features of Epidemiology and Clinical Management. Annu Rev Med. 2016;67:91–101. doi:10.1146/annurev-med-051914-021907. PMID:26332002
   PubMed Web of Science ®Google Scholar
• 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;137:2846–57. doi:10.1002/ijc.29649. PMID:26095926
   PubMed Web of Science ®Google Scholar
• Moskovitz JM, Moy J, Seiwert TY, Ferris RL. Immunotherapy for Head and Neck Squamous Cell Carcinoma: A Review of Current and Emerging Therapeutic Options. Oncologist. 2017;22:680–693. doi:10.1634/theoncologist.2016-0318. PMID:28507203
   PubMed Web of Science ®Google Scholar
• Chen F, Zhang Y, Parra E, Rodriguez J, Behrens C, Akbani R, Lu Y, Kurie JM, Gibbons DL, Mills GB, et al. Multiplatform-based molecular subtypes of non-small-cell lung cancer. Oncogene. 2017;36:1384–93. doi:10.1038/onc.2016.303. PMID:27775076
   PubMed Web of Science ®Google Scholar
• Bindea G, Mlecnik B, Tosolini M, Kirilovsky A, Waldner M, Obenauf AC, Angell H, Fredriksen T, Lafontaine L, Berger A, et al. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity. 2013;39:782–95. doi:10.1016/j.immuni.2013.10.003. PMID:24138885
   PubMed Web of Science ®Google Scholar
• Camus M, Tosolini M, Mlecnik B, Pages F, Kirilovsky A, Berger A, Costes A, Bindea G, Charoentong P, Bruneval P, et al. Coordination of intratumoral immune reaction and human colorectal cancer recurrence. Cancer Res. 2009;69:2685–93. doi:10.1158/0008-5472.CAN-08-2654. PMID:19258510
   PubMed Web of Science ®Google Scholar
• Chung CH, Parker JS, Karaca G, Wu J, Funkhouser WK, Moore D, et al. Molecular classification of head and neck squamous cell carcinomas using patterns of gene expression. Cancer Cell. 2004;5:489–500. doi:10.1016/S1535-6108(04)00112-6. PMID:15144956
   PubMed Web of Science ®Google Scholar
• Walter V, Yin X, Wilkerson MD, Cabanski CR, Zhao N, Du Y, Ang MK, Hayward MC, Salazar AH, Hoadley KA, et al. Molecular subtypes in head and neck cancer exhibit distinct patterns of chromosomal gain and loss of canonical cancer genes. PLoS One. 2013;8:e56823. doi:10.1371/journal.pone.0056823. PMID:23451093
   PubMed Web of Science ®Google Scholar
• Saloura V, Zuo Z, Koeppen H, Keck MK, Khattri A, Boe M, et al. Correlation of T-cell inflamed phenotype with mesenchymal subtype, expression of PD-L1, and other immune checkpoints in head and neck cancer. Journal of Clinical Oncology. 2014;32:6009-.
   Web of Science ®Google Scholar
• Wood O, Woo J, Seumois G, Savelyeva N, McCann KJ, Singh D, Jones T, Peel L, Breen MS, Ward M, et al. Gene expression analysis of TIL rich HPV-driven head and neck tumors reveals a distinct B-cell signature when compared to HPV independent tumors. Oncotarget. 2016; 7:56781–97. doi:10.18632/oncotarget.10788. PMID:27462861
   PubMed Web of Science ®Google Scholar
• Marelli G, Sica A, Vannucci L, Allavena P. Inflammation as target in cancer therapy. Curr Opin Pharmacol. 2017;35:57–65. doi:10.1016/j.coph.2017.05.007. PMID:28618326
   PubMed Web of Science ®Google Scholar
• Koontongkaew S. The tumor microenvironment contribution to development, growth, invasion and metastasis of head and neck squamous cell carcinomas. J Cancer. 2013;4:66–83. doi:10.7150/jca.5112. PMID:23386906
   PubMed Web of Science ®Google Scholar
• Chiarugi P. Cancer-associated fibroblasts and macrophages: Friendly conspirators for malignancy. Oncoimmunology. 2013;2:e25563. doi:10.4161/onci.25563. PMID:24319632
   PubMed Web of Science ®Google Scholar
• Sun W, Wei FQ, Li WJ, Wei JW, Zhong H, Wen YH, Lei WB, Chen L, Li H, Lin HQ, et al. A positive-feedback loop between tumour infiltrating activated Treg cells and type 2-skewed macrophages is essential for progression of laryngeal squamous cell carcinoma. Br J Cancer. 2017 [Epub ahead of print]. doi:10.1038/bjc.2017.329. PMID:28949956.
   PubMed Web of Science ®Google Scholar
• Takahashi H, Sakakura K, Kudo T, Toyoda M, Kaira K, Oyama T, Chikamatsu K. Cancer-associated fibroblasts promote an immunosuppressive microenvironment through the induction and accumulation of protumoral macrophages. Oncotarget. 2017;8:8633–47. PMID:28052009
   PubMed Web of Science ®Google Scholar
• Chang KP, Kao HK, Yen TC, Chang YL, Liang Y, Liu SC, Lee LY, Chang YL, Kang CJ, Chen IH, et al. Overexpression of macrophage inflammatory protein-3alpha in oral cavity squamous cell carcinoma is associated with nodal metastasis. Oral Oncol. 2011;47:108–13. doi:10.1016/j.oraloncology.2010.11.012. PMID:21163685
   PubMed Web of Science ®Google Scholar
• Valero C, Pardo L, Lopez M, Garcia J, Camacho M, Quer M, León X. Pretreatment count of peripheral neutrophils, monocytes, and lymphocytes as independent prognostic factor in patients with head and neck cancer. Head Neck. 2017;39:219–26. doi:10.1002/hed.24561. PMID:27534525
   PubMed Web of Science ®Google Scholar
• Satgunaseelan L, Gupta R, Madore J, Chia N, Lum T, Palme CE, Boyer M, Scolyer RA, Clark JR. Programmed cell death-ligand 1 expression in oral squamous cell carcinoma is associated with an inflammatory phenotype. Pathology. 2016;48:574–80. doi:10.1016/j.pathol.2016.07.003. PMID:27590194
   PubMed Web of Science ®Google Scholar
• 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;34:4132–41. doi:10.1200/JCO.2016.68.2955. PMID:27863190
   PubMed Web of Science ®Google Scholar
• Beyranvand Nejad E, van der Sluis TC, van Duikeren S, Yagita H, Janssen GM, van Veelen PA, Melief CJ, van der Burg SH, Arens R. Tumor Eradication by Cisplatin Is Sustained by CD80/86-Mediated Costimulation of CD8+ T Cells. Cancer Res. 2016;76:6017–29. doi:10.1158/0008-5472.CAN-16-0881. PMID:27569212
   PubMed Web of Science ®Google Scholar
• Huber-Ruano I, Raventos C, Cuartas I, Sanchez-Jaro C, Arias A, Parra JL, Wosikowski K, Janicot M, Seoane J. An antisense oligonucleotide targeting TGF-beta2 inhibits lung metastasis and induces CD86 expression in tumor-associated macrophages. Ann Oncol;28:2278–85. doi:10.1093/annonc/mdx314. PMID:28911087
   PubMed Web of Science ®Google Scholar
• Peng Y, Luo G, Zhou J, Wang X, Hu J, Cui Y, Li XC, Tan J, Yang S, Zhan R, et al. CD86 is an activation receptor for NK cell cytotoxicity against tumor cells. PLoS One. 2013;8:e83913. doi:10.1371/journal.pone.0083913. PMID:24349559
   PubMed Web of Science ®Google Scholar
• Seth P, Csizmadia E, Hedblom A, Vuerich M, Xie H, Li M, Longhi MS, Wegiel B. Deletion of Lactate Dehydrogenase-A in Myeloid Cells Triggers Antitumor Immunity. Cancer Res. 2017;77:3632–43. doi:10.1158/0008-5472.CAN-16-2938. PMID:28446465
   PubMed Web of Science ®Google Scholar
• Bu LL, Yu GT, Wu L, Mao L, Deng WW, Liu JF, Kulkarni AB, Zhang WF, Zhang L, Sun ZJ. STAT3 Induces Immunosuppression by Upregulating PD-1/PD-L1 in HNSCC. J Dent Res. 2017;96:1027–34. doi:10.1177/0022034517712435. PMID:28605599
   PubMed Web of Science ®Google Scholar
• Calles A, Liao X, Sholl LM, Rodig SJ, Freeman GJ, Butaney M, Lydon C, Dahlberg SE, Hodi FS, Oxnard GR, et al. Expression of PD-1 and Its Ligands, PD-L1 and PD-L2, in Smokers and Never Smokers with KRAS-Mutant Lung Cancer. J Thorac Oncol. 2015;10:1726–35. doi:10.1097/JTO.0000000000000687. PMID:26473645
   PubMed Web of Science ®Google Scholar
• Tosolini M, Kirilovsky A, Mlecnik B, Fredriksen T, Mauger S, Bindea G, Berger A, Bruneval P, Fridman WH, Pagès F, et al. Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res. 2011;71:1263–71. doi:10.1158/0008-5472.CAN-10-2907. PMID:21303976
   PubMed Web of Science ®Google Scholar
• Sandoval F, Terme M, Nizard M, Badoual C, Bureau MF, Freyburger L, Clement O, Marcheteau E, Gey A, Fraisse G, et al. Mucosal imprinting of vaccine-induced CD8(+) T cells is crucial to inhibit the growth of mucosal tumors. Sci Transl Med. 5:172ra20. PMID:23408053
   PubMed Web of Science ®Google Scholar
• Balermpas P, Rodel F, Weiss C, Rodel C, Fokas E. Tumor-infiltrating lymphocytes favor the response to chemoradiotherapy of head and neck cancer. Oncoimmunology. 2014;3:e27403. doi:10.4161/onci.27403. PMID:24711959
   PubMed Web of Science ®Google Scholar
• Badoual C, Hans S, Merillon N, Van Ryswick C, Ravel P, Benhamouda N, Levionnois E, Nizard M, Si-Mohamed A, Besnier N, et al. PD-1-expressing tumor-infiltrating T cells are a favorable prognostic biomarker in HPV-associated head and neck cancer. Cancer Res. 2013;73:128–38. doi:10.1158/0008-5472.CAN-12-2606. PMID:23135914
   PubMed Web of Science ®Google Scholar
• Distel LV, Fickenscher R, Dietel K, Hung A, Iro H, Zenk J, Nkenke E, Büttner M, Niedobitek G, Grabenbauer GG. Tumour infiltrating lymphocytes in squamous cell carcinoma of the oro- and hypopharynx: prognostic impact may depend on type of treatment and stage of disease. Oral Oncol. 2009;45:e167–74. doi:10.1016/j.oraloncology.2009.05.640. PMID:19576838
   PubMed Web of Science ®Google Scholar
• Wilkerson MD, Hayes DN. ConsensusClusterPlus: a class discovery tool with confidence assessments and item tracking. Bioinformatics. 2010;26:1572–3. doi:10.1093/bioinformatics/btq170. PMID:20427518
   PubMed Web of Science ®Google Scholar
• Liu Y, Hayes DN, Nobel A, Marron JS. Statistical Significance of Clustering for High-Dimension, Low sample Size Data. Journal of the American Statistical Association. 2008;103:1281–93. doi:10.1198/016214508000000454.
   Web of Science ®Google Scholar
• Becht E, Giraldo NA, Lacroix L, Buttard B, Elarouci N, Petitprez F, Selves J, Laurent-Puig P, Sautès-Fridman C, Fridman WH, et al. Estimating the population abundance of tissue-infiltrating immune and stromal cell populations using gene expression. Genome Biol. 2016;17:218. doi:10.1186/s13059-016-1070-5. PMID:27765066.
   PubMed Web of Science ®Google Scholar