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Safety, Activity, and Immune Correlates of Anti–PD-1 Antibody in Cancer

Why this mattered

This paper helped turn cancer immunotherapy from a proof-of-principle into a broadly actionable treatment paradigm. Earlier checkpoint work, especially CTLA-4 blockade, had shown that releasing inhibitory signals on T cells could produce durable tumor regression, but with substantial toxicity and clearest impact in melanoma. Topalian and colleagues showed that blocking PD-1 could produce objective, often durable responses across multiple advanced cancers, including non-small-cell lung cancer, melanoma, and renal-cell carcinoma. The lung-cancer signal was especially important: it challenged the prevailing view that only highly immunogenic tumors such as melanoma were natural targets for immune checkpoint therapy.

The study also made a new clinical logic possible. Instead of treating cancer only by targeting tumor-intrinsic mutations or cytotoxic vulnerability, clinicians could target an adaptive immune-resistance pathway used by tumors to suppress antitumor T-cell activity. The absence of a defined maximum tolerated dose, the manageable overall safety profile despite serious immune-related pulmonary toxicity, and the durability of many responses suggested that PD-1 blockade could become a repeatable therapeutic platform rather than an exceptional rescue therapy.

Its exploratory PD-L1 analysis pointed toward another major shift: immunotherapy could be guided by features of the tumor-immune microenvironment. The finding that responses occurred in PD-L1-positive tumors and not in the small PD-L1-negative group was preliminary, but it helped frame PD-L1 as a clinically useful, if imperfect, biomarker. Subsequent breakthroughs built directly on this foundation: approved PD-1 and PD-L1 inhibitors across many tumor types, combination checkpoint blockade, immunotherapy-first strategies in lung cancer and melanoma, and the broader idea that durable cancer control can come from reactivating host immunity rather than directly attacking every malignant cell.

Abstract

BACKGROUND: Blockade of programmed death 1 (PD-1), an inhibitory receptor expressed by T cells, can overcome immune resistance. We assessed the antitumor activity and safety of BMS-936558, an antibody that specifically blocks PD-1. METHODS: We enrolled patients with advanced melanoma, non-small-cell lung cancer, castration-resistant prostate cancer, or renal-cell or colorectal cancer to receive anti-PD-1 antibody at a dose of 0.1 to 10.0 mg per kilogram of body weight every 2 weeks. Response was assessed after each 8-week treatment cycle. Patients received up to 12 cycles until disease progression or a complete response occurred. RESULTS: A total of 296 patients received treatment through February 24, 2012. Grade 3 or 4 drug-related adverse events occurred in 14% of patients; there were three deaths from pulmonary toxicity. No maximum tolerated dose was defined. Adverse events consistent with immune-related causes were observed. Among 236 patients in whom response could be evaluated, objective responses (complete or partial responses) were observed in those with non-small-cell lung cancer, melanoma, or renal-cell cancer. Cumulative response rates (all doses) were 18% among patients with non-small-cell lung cancer (14 of 76 patients), 28% among patients with melanoma (26 of 94 patients), and 27% among patients with renal-cell cancer (9 of 33 patients). Responses were durable; 20 of 31 responses lasted 1 year or more in patients with 1 year or more of follow-up. To assess the role of intratumoral PD-1 ligand (PD-L1) expression in the modulation of the PD-1-PD-L1 pathway, immunohistochemical analysis was performed on pretreatment tumor specimens obtained from 42 patients. Of 17 patients with PD-L1-negative tumors, none had an objective response; 9 of 25 patients (36%) with PD-L1-positive tumors had an objective response (P=0.006). CONCLUSIONS: Anti-PD-1 antibody produced objective responses in approximately one in four to one in five patients with non-small-cell lung cancer, melanoma, or renal-cell cancer; the adverse-event profile does not appear to preclude its use. Preliminary data suggest a relationship between PD-L1 expression on tumor cells and objective response. (Funded by Bristol-Myers Squibb and others; ClinicalTrials.gov number, NCT00730639.).

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