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Improved understanding of expression of immune checkpoint receptors (ICR) on tumor-infiltrating lymphocytes (TIL) may facilitate more effective immunotherapy in head and neck cancer (HNC) patients. A higher frequency of PD-1 + TIL has been reported in human papillomavirus (HPV) + HNC patients, despite the role of PD-1 in T-cell exhaustion. This discordance led us to hypothesize that the extent of PD-1 expression more accurately defines T-cell function and prognostic impact, because PD-1 high T cells may be more exhausted than PD-1 low T cells and may influence clinical outcome and response to anti-PD-1 immunotherapy. In this study, PD-1 expression was indeed upregulated on HNC patient TIL, and the frequency of these PD-1 + TIL was higher in HPV + patients ( P = 0.006), who nonetheless experienced significantly better clinical outcome. However, PD-1 high CD8 + TILs were more frequent in HPV - patients and represented a more dysfunctional subset with compromised IFN-γ secretion. Moreover, HNC patients with higher frequencies of PD-1 high CD8 + TIL showed significantly worse disease-free survival and higher hazard ratio for recurrence ( P &lt; 0.001), while higher fractions of PD-1 low T cells associated with HPV positivity and better outcome. In a murine HPV + HNC model, anti-PD-1 mAb therapy differentially modulated PD-1 high/low populations, and tumor rejection associated with loss of dysfunctional PD-1 high CD8 + T cells and a significant increase in PD-1 low TIL. Thus, the extent of PD-1 expression on CD8 + TIL provides a potential biomarker for anti-PD-1-based immunotherapy. Cancer Res; 77(22); 6353-64. ©2017 AACR .

PD-1 Status in CD8+ T Cells Associates with Survival and Anti-PD-1 Therapeutic Outcomes in Head and Neck Cancer