Immunotherapy for head and neck squamous cell carcinoma: A review of current and emerging therapeutic options

Oncologist

Volumn 22, Issue 6, 2017, Pages 680-693

  Moskovitz, Jessica M ^a   Moy, Jennifer ^a   Seiwert, Tanguy Y ^b   Ferris, Robert L ^a,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

Head and neck squamous cell carcinoma; Immunotherapy; Lymphocyte; Neoplasm of head and neck

Indexed keywords

ACALABRUTINIB; ATEZOLIZUMAB; AZD9150; CARBOXYMETHYLCELLULOSE POLYCYTIDYLIC POLYINOSINIC ACID POLYLYSINE; CETUXIMAB; DOCETAXEL; DURVALUMAB; ENADENOTUCIREV; ENOBLITUZUMAB; EPACADOSTAT; FPA008; IMMUNOMODULATING AGENT; INCB050465; IPILIMUMAB; ITACITINIB; METHOTREXATE; MOGAMULIZUMAB; MOTOLIMOD; N [2 (2,3 DIFLUOROBENZYLTHIO) 6 (2,3 DIHYDROXY 1 METHYLPROPOXY) 4 PYRIMIDINYL] 1 AZETIDINESULFONAMIDE; NIVOLUMAB; PEMBROLIZUMAB; PLX3397; SELUMETINIB; TAK 659; TALIMOGENE LAHERPAREPVEC; TICILIMUMAB; UNCLASSIFIED DRUG; UNINDEXED DRUG; VACCINE; VARLILUMAB; VORINOSTAT; TUMOR MARKER;

CHEMOTHERAPY; DRUG MONITORING; HEAD AND NECK SQUAMOUS CELL CARCINOMA; IMMUNOTHERAPY; MELANOMA; NON SMALL CELL LUNG CANCER; NONHUMAN; OVERALL SURVIVAL; PAPILLOMAVIRUS INFECTION; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; HEAD AND NECK TUMOR; HUMAN; IMMUNE SYSTEM; IMMUNOLOGY; PATHOLOGY; SQUAMOUS CELL CARCINOMA;

BIOMARKERS, TUMOR; CARCINOMA, SQUAMOUS CELL; HEAD AND NECK NEOPLASMS; HUMANS; IMMUNE SYSTEM; IMMUNOTHERAPY;

EID: 85020905767     PISSN: 10837159     EISSN: 1549490X     Source Type: Journal    
DOI: 10.1634/theoncologist.2016-0318     Document Type: Review

References (93)

1. Hanahan D, Weinberg RA. Hallmarks of cancer:The next generation. Cell 2011;144:646-674.
2. Thomas ED, Lochte HL Jr, Lu WC et al. Intravenous infusion of bone marrow in patients receiving radiation and chemotherapy. N Engl J Med 1957; 257:491-496.
3. Ferris RL. Immunology and immunotherapy of head and neck cancer. J Clin Oncol 2015;33:3293-3304.
4. Beatty GL, Gladney WL. Immune escape mechanisms as a guide for cancer immunotherapy. Clin Cancer Res 2015;21:687-692.
5. Fuertes MB, Kacha AK, Kline J et al. Host type I IFN signals are required for antitumor CD81 T cell responses through CD8{alpha}1 dendritic cells. J Exp Med 2011;208:2005-2016.
6. Boon T, Cerottini JC, Van den Eynde B et al. Tumor antigens recognized by T lymphocytes. Annu Rev Immunol 1994;12:337-365.
7. Jie HB, Gildener-Leapman N, Li J et al. Intratumoral regulatory T cells upregulate immunosuppressive molecules in head and neck cancer patients. Br J Cancer 2013;109:2629-2635.
8. Allen CT, Judd NP, Bui JD et al. The clinical implications of antitumor immunity in head and neck cancer. Laryngoscope 2012;122:144-157.
9. Whiteside TL. Immunobiology of head and neck cancer. CancerMetastasis Rev 2005;24:95-105.
10. Pries R, Wollenberg B. Cytokines in head and neck cancer. Cytokine Growth Factor Rev 2006;17:141-146.
11. Gildener-Leapman N, Ferris RL, Bauman JE. Promising systemic immunotherapies in head and neck squamous cell carcinoma. Oral Oncol 2013;49:1089-1096.
12. Badoual C, Sandoval F, Pere H et al. Better understanding tumor-host interaction in head and neck cancer to improve the design and development of immunotherapeutic strategies. Head Neck 2010; 32:946-958.
13. Duray A, Demoulin S, Hubert P et al. Immune suppression in head and neck cancers: A review. Clin Dev Immunol 2010;2010:701657.
14. Kim R, Emi M,Tanabe K. Cancer immunoediting from immune surveillance to immune escape. Immunology 2007;121:1-14.
15. Saloura V, Zou Z, Koeppen H et al. Correlation of T-cell inflamed phenotype with mesenchymal subtype, expression of PD-L1, and other immune checkpoints in head and neck cancer. J Clin Oncol 2014;32:(suppl 5):6009a.
16. Topalian SL, Weiner GJ, Pardoll DM. Cancer immunotherapy comes of age. J Clin Oncol 2011;29:4828-4836.
17. Pardoll DM. Cancer Immunology. In: Abeloff’s Clincial Oncology. 5th ed. Philadelphia: Saunders, 2014:6, 78-97.
18. Sckisel GD, Bouchlaka MN, Monjazeb AM et al. Out-of-sequence signal 3 paralyzes primary CD4(1) Tcell-dependent immunity. Immunity 2015;43:240-250.
19. Baruah P, Lee M, Odutoye T et al. Decreased levels of alternative co-stimulatory receptors OX40 and 4-1BB characterise T cells from head and neck cancer patients. Immunobiology 2012;217:669-675.
20. Bauman JE, Ferris RL. Integrating novel therapeutic monoclonal antibodies into the management of head and neck cancer. Cancer 2014;120:624-632.
21. Lynch DH. The promise of 4-1BB (CD137)-mediated immunomodulation and the immunotherapy of cancer. Immunol Rev 2008;222:277-286.
22. Chapoval AI, Ni J, Lau JS et al. B7-H3: A costimulatory molecule for T cell activation and IFN-gamma production. Nat Immunol 2001;2:269-274.
23. Loos M, Hedderich DM, Friess H et al. B7-h3 and its role in antitumor immunity. Clin Dev Immunol 2010;2010:683875.
24. Katayama A, Takahara M, Kishibe K et al. Expression of B7-H3 in hypopharyngeal squamous cell carcinoma as a predictive indicator for tumor metastasis and prognosis. Int J Oncol 2011;38:1219-1226.
25. Lawrence MS, Stojanov P, Polak P et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 2013;499:214-218.
26. Champiat S, Ferté C, Lebel-Binay S et al. Exomics and immunogenics: Bridging mutational load and immune checkpoints efficacy. Oncoimmunology 2014;3:e27817.
27. Ogino T, Shigyo H, Ishii H et al. HLA class I antigen down-regulation in primary laryngeal squamous cell carcinoma lesions as a poor prognostic marker. Cancer Res 2006;66:9281-9289.
28. Concha-Benavente F, Srivastava R, Ferrone S et al. Immunological and clinical significance of HLA class I antigen processing machinery component defects in malignant cells. Oral Oncol 2016;58:52-58.
29. Mizukami Y, Kono K, Maruyama T et al. Downregulation of HLA Class I molecules in the tumour is associated with a poor prognosis in patients with oesophageal squamous cell carcinoma. Br J Cancer 2008;99:1462-1467.
30. Workman CJ, Rice DS, Dugger KJ et al. Phenotypic analysis of the murine CD4-related glycoprotein, CD223 (LAG-3). Eur J Immunol 2002;32:2255-2263.
31. Liang B, Workman C, Lee J et al. Regulatory T cells inhibit dendritic cells by lymphocyte activation gene-3 engagement of MHC class II. J Immunol 2008;180:5916-5926.
32. Zitvogel L, Kroemer G. Targeting PD-1/PD-L1 interactions for cancer immunotherapy. Oncoimmunology 2012;1:1223-1225.
33. Peggs KS, Quezada SA, Chambers CA. Blockade of CTLA-4 on both effector and regulatory Tcell compartments contributes to the antitumor activity of anti-CTLA-4 antibodies. J Exp Med 2009;206:1717-1725.
34. Honeychurch J, Cheadle EJ, Dovedi SJ et al. Immuno-regulatory antibodies for the treatment of cancer. Expert Opin Biol Ther 2015;15:787-801.
35. Strauss L, Bergmann C, Gooding W et al. The frequency and suppressor function of CD41CD25highFoxp31 T cells in the circulation of patients with squamous cell carcinoma of the head and neck. Clin Cancer Res 2007;13:6301-6311.
36. Monney L, Sabatos CA, Gaglia JL et al. Th1-specific cell surface protein Tim-3 regulatesmacrophage activation and severity of an autoimmune disease. Nature 2002;415:536-541.
37. Trivedi S, Srivastava RM, Concha-Benavente F et al. Anti-EGFR targeted monoclonal antibody isotype influences antitumor cellular immunity in head and neck cancer patients. Clin Cancer Res 2016;22:5229-5237.
38. Concha-Benavente F, Srivastava RM, Trivedi S et al. Identification of the cell-intrinsic and -extrinsic pathways downstream of EGFR and IFNg that induce PD-L1 expression in head and neck cancer. Cancer Res 2016;76:1031-1043.
39. Jie HB, Schuler PJ, Lee SC et al. CTLA-4(1) regulatory T cells increased in cetuximab-treated head and neck cancer patients suppress NK cell cytotoxicity and correlate with poor prognosis. Cancer Res 2015;75:2200-2210.
40. Vetto JT, Lum S, Morris A et al. Presence of the T-cell activation marker OX-40 on tumor infiltrating lymphocytes and draining lymph node cells from patients with melanoma and head and neck cancers. Am J Surg 1997;174:258-265.
41. Roselli M, Cereda V, di Bari MG et al. Effects of conventional therapeutic interventions on the number and function of regulatory Tcells. Oncoimmunology 2013;2:e27025.
42. Scharovsky OG, Mainetti LE, Rozados VR. Metronomic chemotherapy: Changing the paradigm that more is better. Curr Oncol 2009;16:7-15.
43. Deng L, Liang H, Burnette B et al. Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice. J Clin Invest 2014;124:687-695.
44. Hodge JW, Ardiani A, Farsaci B et al. The tipping point for combination therapy: Cancer vaccines with radiation, chemotherapy, or targeted small molecule inhibitors. Semin Oncol 2012;39:323-339.
45. Vermorken JB, Mesia R, Rivera F et al. Platinum-based chemotherapy plus cetuximab in head and neck cancer. N Engl J Med 2008;359:1116-1127.
46. Chow LQ, Burtness B,Weiss J et al. A phase Ib study of pembrolizumab (Pembro; MK-3475) in patients (Pts) with human papilloma virus (HPV)-positive and negative head and neck cancer (HNC). Ann Oncol 2014;25:1-41.
47. Chow L, Mehra R, Haddad R et al. Antitumor activity of the Anti-PD1 antibody pembrolizumab in subgroups of patients with recurrent/metastatic head and neck squamous cell carcinoma (R/M HNSCC): Exploratory analyses from KEYNOTE-012. Eur J Cancer 2015;51(suppl 3):S579.
48. Seiwert Ty, Burtness B,Weiss J et al. Inflamedphenotype gene expression signatures to predict benefit from the anti-PD1 antibody pembrolizumab in PDL11 head and neck cancer patients. J Clin Oncol 2015;33(suppl):6017a.
49. Seiwert TY, Burtness B,Weiss J et al. A phase Ib study of MK-3475 in patients with human papillomavirus (HPV)-associated and non-HPV-associated head and neck (H/N) cancer. J Clin Oncol 2014; 32(suppl):6011a.
50. Clinical Trials.gov. Available at: https://clinicaltrials.gov/. Accessed July 29, 2016.
51. Ferris RL, Blumenschein GR, Fayette J et al. Further evaluations of nivolumab (nivo) versus investigator’s choice (IC) chemotherapy for recurrent or metastatic (R/M) squamous cell carcinoma of the head and neck (SCCHN): CheckMate 141. J Clin Oncol 2016;34(supl; 6009a).
52. Gillison ML, Blumenschein GR, Fayette J et al. Nivolumab (nivo) vs investigator’s choice (IC) for recurrent or metastatic (R/M) head and neck squamous cell carcinoma (HNSCC): Checkmate-141. AACR Annual Meeting; New Orleans, LA, 2016; CT099a.
53. Ferris RL, Blumenschein G Jr, Fayette J et al. Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N Engl J Med 2016;375:1856-1867.
54. Song X, Pak M, Chavez C et al. Pharmacokinetics and pharmacodynamics of MEDI4736, a fully human anti-programmed death ligand 1 (PD-L1) monoclonal antibody, in patients with advanced solid tumors. J Clin Oncol 2015;33(suppl):e14009a.
55. Schoppy DW, Sunwoo JB. Immunotherapy for head and neck squamous cell carcinoma. Hematol Oncol Clin North Am 2015;29:1033-1043.
56. Gough MJ, Crittenden MR, Sarff M et al. Adjuvant therapy with agonistic antibodies to CD134 (OX40) increases local control after surgical or radiation therapy of cancer in mice. J Immunother 2010; 33:798-809.
57. Curti BD, Kovacsovics-Bankowski M, Morris N et al. OX40 is a potent immune-stimulating target in late-stage cancer patients. Cancer Res 2013;73:7189-7198.
58. Vonderheide RH, Glennie MJ. Agonistic CD40 antibodies and cancer therapy. Clin Cancer Res 2013;19:1035-1043.
59. Posner MR, Cavacini LA, Upton MP et al. Surface membrane-expressed CD40 is present on tumor cells from squamous cell cancer of the head and neck in vitro and in vivo and regulates cell growth in tumor cell lines. Clin Cancer Res 1999;5:2261-2270.
60. CaoW, Cavacini LA, Tillman KC et al. CD40 function in squamous cell cancer of the head and neck. Oral Oncol 2005;41:462-469.
61. Beatty GL, Torigian DA, Chiorean EG et al. A phase I study of an agonist CD40 monoclonal antibody (CP-870,893) in combination with gemcitabine in patients with advanced pancreatic ductal adenocarcinoma. Clin Cancer Res 2013;19:6286-6295.
62. Johnson P, Challis R, Chowdhury F et al. Clinical and biological effects of an agonist anti-CD40 antibody:A Cancer Research UK phase I study. Clin Cancer Res 2015;21:1321-1328.
63. Sathawane D, Kharat RS, Halder S et al. Monocyte CD40 expression in head and neck squamous cell carcinoma (HNSCC). Hum Immunol 2013;74:1-5.
64. Marur S, Forastiere AA. Head and neck squamous cell carcinoma: Update on epidemiology, diagnosis, and treatment. Mayo Clin Proc 2016;91:386-396.
65. Bernier J, Cooper JS. Chemoradiation after surgery for high-risk head and neck cancer patients:How strong is the evidence? The Oncologist 2005; 10:215-224.
66. Bernier J, Domenge C, Ozsahin Met al. Postoperative irradiation with or without concomitant chemotherapy for locally advanced head and neck cancer. N Engl JMed 2004;350:1945-1952.
67. Cooper JS, Pajak TF, Forastiere AA et al. Postoperative concurrent radiotherapy and chemotherapy for high-risk squamous-cell carcinoma of the head and neck. N Engl J Med. 2004;350:1937-1944.
68. Cooper JS, Zhang Q, Pajak TF 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;84:1198-1205.
69. Chan TA, Wolchok JD, Snyder A. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl JMed 2015;373:1984.
70. Twyman-Saint Victor C, Rech AJ, Maity A et al. Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature 2015;520:373-377.
71. Wolchok JD, Kluger H, Callahan MK et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl JMed 2013;369:122-133.
72. Larkin J, Hodi FS,Wolchok JD. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med 2015;373:1270-1271.
73. Rizvi N, Chaft J, Balmanoukian A et al. Tumor response from durvalumab (MEDI4736)1tremelimumab treatment in patients with advanced nonsmall cell lung cancer (NSCLC) is observed regardless of PD-L1 status. J Immunother Cancer. 2015;3 (suppl 2):193.
74. Woo SR, TurnisME, GoldbergMV et al. Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T-cell function to promote tumoral immune escape. Cancer Res 2012;72:917-927.
75. Sakuishi K, Apetoh L, Sullivan JMet al. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J Exp Med 2010;207:2187-2194.
76. Fourcade J, Sun Z, Benallaoua M et al. Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD81 T cell dysfunction in melanoma patients. J Exp Med 2010;207:2175-2186.
77. Melero I, Shuford WW, Newby SA et al. Monoclonal antibodies against the 4-1BB T-cell activation molecule eradicate established tumors. Nat Med 1997;3:682-685.
78. Vahle AK, Hermann S, Schäfers M et al. Multimodal imaging analysis of an orthotopic head and neck cancer mouse model and application of anti-CD137 tumor immune therapy. Head Neck 2016;38:542-549.
79. Lucido CT, Vermeer PD, Wieking BG et al. CD137 enhancement of HPV positive head and neck squamous cell carcinoma tumor clearance. Vaccines (Basel) 2014;2:841-853.
80. Kohrt HE, Colevas AD, Houot R et al. Targeting CD137 enhances the efficacy of cetuximab. J Clin Invest 2014;124:2668-2682.
81. Srivastava RM, Trivedi S, Concha-Benavente F et al. CD137 stimulation enhances cetuximabinduced natural killer: Dendritic cell priming of antitumor T-cell immunity in patients with head and neck cancer. Clin Cancer Res 2017;23:707-716.
82. Stephenson RM, Lim CM, Matthews M et al. TLR8 stimulation enhances cetuximab-mediated natural killer cell lysis of head and neck cancer cells and dendritic cell cross-priming of EGFR-specific CD81 T cells. Cancer Immunol Immunother 2013;62:1347-1357.
83. Topalian SL, Taube JM, Anders RA et al. Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy. Nat Rev Cancer 2016;16:275-287.
84. Patel SP, Kurzrock R. PD-L1 expression as a predictive biomarker in cancer immunotherapy. Mol Cancer Ther 2015;14:847-856.
85. Yearley J, Gibson C, Yu N et al. 18 LBA PD-L2 expression in human tumors: relevance to anti-PD-1 therapy in cancer. Eur J Cancer 2015;51(suppl 3):S718.
86. Seiwert TY, Burtness B, Mehra R 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;17:956-965.
87. Ribas A, Robert C, Hodi FS et al. Association of response to programmed death receptor 1 (PD-1) blockade with pembrolizumab (MK-3475) with an interferon-inflammatory immune gene signature. Proc Am Soc Clin Oncol 2015;33:3001a.
88. Hales RK, Banchereau J, Ribas A et al. Assessing oncologic benefit in clinical trials of immunotherapy agents. Ann Oncol 2010;21:1944-1951.
89. Bertrand A, Kostine M, Barnetche T et al. Immune related adverse events associated with anti-CTLA-4 antibodies: Systematic review and meta-analysis. BMCMed 2015;13:211.
90. Kähler KC, Hassel JC, Heinzerling L et al. Management of side effects of immune checkpoint blockade by anti-CTLA-4 and anti-PD-1 antibodies in metastatic melanoma. J Dtsch Dermatol Ges 2016; 14:662-681.
91. Nishino M, Sholl LM, Hodi FS et al. Anti-PD-1-related pneumonitis during cancer immunotherapy. N Engl J Med 2015;373:288-290.
92. Robert C, Schachter J, Long GV et al. Pembrolizumab versus ipilimumab in advancedmelanoma. N Engl JMed 2015;372:2521-2532.
93. Michot JM, Bigenwald C, Champiat S et al. Immune-related adverse events with immune checkpoint blockade: A comprehensive review. Eur J Cancer 2016;54:139-148.