Safety, activity, and immune correlates of anti–PD-1 antibody in cancer
Open accessAbstract
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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PD-L1 expression on tumor cells is regarded as the most available biomarker to predict the efficacy of ICIs in NSCLC and other malignancies.
“So far, PD-L1 expression on tumor cells is regarded as the most available biomarker to predict the efficacy of ICIs in NSCLC and other malignancies.”
From The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti–Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC (2019) · cites this paper as [8]
The Discussion describes tumor PD-L1 expression as a candidate marker for response to anti–PD-1 therapy, and the Results report responses in 9 of 25 patients with PD-L1–positive tumors versus none of 17 with PD-L1–negative tumors. But the paper calls this analysis preliminary and says further studies are needed; it does not establish PD-L1 as the most available biomarker or address predictive efficacy across ICIs generally. Page numbers are not provided in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measuredA linear relationship has been reported between the proportion of ICI benefit and PD-L1 expression in NSCLC tumor sections.
“A linear relationship has been reported between the proportion of ICI benefit and PD-L1 expression in NSCLC tumor sections.7,8”
From The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti–Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC (2019) · cites this paper as [8]
The Results section (PD-L1 Expression in Tumors; page unavailable) reports objective responses in 9 of 25 patients with PD-L1–positive tumors and none of 17 with PD-L1–negative tumors. That supports an association with response to anti–PD-1 treatment, but the analysis pooled cancer types, included only 10 patients with NSCLC, and compared positive with negative specimens; it did not establish a linear relationship between expression level and benefit specifically in NSCLC. (LLM, conf=0.87)
Experimental — accuracy not yet measuredResponse rate was 38%, in line with published clinical data of anti-PD-1 therapy in metastatic melanoma patients.
“There were 16 responders (from here on, referred to as R) and 26 nonresponders (NR), yielding a response rate of 38%, which is in line with published clinical data of anti–PD-1 therapy in metastatic melanoma patients (5, 6).”
From The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients (2018) · cites this paper as [5]
Antibodies against CTLA-4 (ipilimumab) or PD1 (nivolumab) induce quick and intense tumor regression in melanoma and NSCLC patients and are under clinical investigation in other solid tumors, including colorectal cancer.
“Antibodies against CTLA-4 (ipilimumab) or PD1 (nivolumab) have been shown to induce quick and intense tumor regression in melanoma and NSCLC patients and are currently under clinical investigation in other solid tumors, including CRC [132, 133]”
From Primary and acquired resistance to EGFR-targeted therapies in colorectal cancer: impact on future treatment strategies (2014) · cites this paper as [133]
Clinical blockade of B7-H1/PD-1 may rescue T cell effector functions in vivo and results in significant objective clinical responses.
“A promising aspect is that clinical blockade of B7-H1/PD-1, the key T cell exhaustion pathway, may rescue T cell effector functions in vivo, and results in significant objective clinical responses [32,33].”
From T cell anergy, exhaustion, senescence, and stemness in the tumor microenvironment (2013) · cites this paper as [33]
PD-L1 expression on tumor cells was correlated with treatment efficacy in melanoma patients.
“Although PD-L1 expression on tumor cells was correlated with treatment efficacy in melanoma patients (67, 108), it was not in patients with squamous cell carcinoma, non-small cell lung cancer and Merkel cell carcinoma (70, 72, 74).”
From Anti-PD-1 and Anti-CTLA-4 Therapies in Cancer: Mechanisms of Action, Efficacy, and Limitations (2018) · cites this paper as [108]
PD-L1 expression on tumor cells correlates with clinical response in certain settings such as NSCLC.
“A correlation between PD-L1 expression on tumor cells and clinical response is seen in certain circumstances (e.g., in NSCLC); however, in other cases, substantial responses can be observed in some patients with PD-L1-negative tumors, which highlights the difficulty of using PD-L1 as a single biomarker (34,143,144).”
From The Next Decade of Immune Checkpoint Therapy (2021) · cites this paper as [34]
Substantial responses can occur in some patients with PD-L1-negative tumors, which shows the difficulty of using PD-L1 alone as a biomarker.
“however, in other cases, substantial responses can be observed in some patients with PD-L1-negative tumors, which highlights the difficulty of using PD-L1 as a single biomarker (34,143,144).”
From The Next Decade of Immune Checkpoint Therapy (2021) · cites this paper as [34]
PD-L1 expression is predictive of positive response to ICI in NSCLC.
“To evaluate the potential interaction with PD-L1 expression, which is predictive of a positive response to ICI in NSCLC,30 we further separated the cohort into three tertiles according to PD-L1 expression levels (0, 1–49% and ≥50%).”
From <i>Faecalibacterium prausnitzii</i> strain EXL01 boosts efficacy of immune checkpoint inhibitors (2024) · cites this paper as [30]
Clinical studies have shown that only 30% and 40% of melanoma patients benefit from PD-1 inhibitors, and PD-1 blockade therapy is ineffective in most patients.
“However, clinical studies have shown that only 30% and 40% of melanoma patients benefit from PD‐1 inhibitors, and PD‐1 blockade therapy is ineffective in most patients. 414 , 415 , 416”
From Hypoxia signaling in cancer: Implications for therapeutic interventions (2023) · cites this paper as [416]
Many tumours turn off T cells specific for tumour antigens by binding to check-point receptors such as PD-1 or CTLA4, and treatments blocking these interactions have therapeutic potential.
“Many tumours turn off T cells specific for tumour antigens by binding to ‘check-point’ receptors such as PD-1 or CTLA4, and new treatments that block these receptor–ligand interactions have great therapeutic potential [77,78].”
From Evolution of the immune system in humans from infancy to old age (2015) · cites this paper as [77]
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- Authors
- Topalian, S. L., Hodi, F. S., Brahmer, J. R., Gettinger, S. N., Smith, D. C., McDermott, D. F., Powderly, J. D., Carvajal, R. D., Sosman, J. A., Atkins, M. B., Leming, P. D., Spigel, D. R., Antonia, S. J., Horn, L., Drake, C. G., Pardoll, D. M., Chen, L., Sharfman, W. H., Anders, R. A., Taube, J. M., McMiller, T. L., Xu, H., Korman, A. J., Jure-Kunkel, M., Agrawal, S., McDonald, D., Kollia, G. D., Gupta, A., Wigginton, J. M., & Sznol, M.
- Affiliations
- Johns Hopkins University (US)
- Dana-Farber Cancer Institute (US)
- Yale Cancer Center (US)
- University of Michigan (US)
- Beth Israel Deaconess Medical Center (US)
- Carolina BioOncology Institute (US)
- Memorial Sloan Kettering Cancer Center (US)
- Vanderbilt University Medical Center (US)
- New York Oncology Hematology (US)
- Sarah Cannon Research Institute (GB)
- Moffitt Cancer Center (US)
- Bristol-Myers Squibb (United States) (US)
- ORCID
- Topalian, Suzanne L.
- Hodi, F. Stephen
- Brahmer, Julie R.
- Gettinger, Scott N.
- Smith, David C.
- McDermott, David F.
- Powderly, John D.
- Carvajal, Richard D.
- Sosman, Jeffrey A.
- Atkins, Michael B.
- Leming, Philip D.
- Spigel, David R.
- Antonia, Scott J.
- Horn, Leora
- Drake, Charles G.
- Pardoll, Drew M.
- Chen, Lieping
- Sharfman, William H.
- Anders, Robert A.
- Taube, Janis M.
- McMiller, Tracee L.
- Korman, Alan J.
- Agrawal, Shruti
- Gupta, Ashok
- Sznol, Mario
- Venue
- New England Journal of Medicine
- Publisher
- Massachusetts Medical Society
- Published
- 2012-06-28
- Volume
- 366
- Issue
- 26
- Pages
- 2443-2454
- ISSN
- 0028-4793 (ISSN-L)
- 1533-4406
- PMC
- PMC3544539
- OpenAlex
- W2160834915
- Semantic Scholar
- ada133745281f73cc7b8e4043b55844d1ea95de5
- Cited by
- 12,628
- References
- 26
- Citations by year
- 2026: 420 · 2025: 563 · 2024: 629 · 2023: 808 · 2022: 848 · 2021: 960 · 2020: 1155 · 2019: 1055 · 2018: 1077 · 2017: 1245 · 2016: 1201 · 2015: 1063 · 2014: 813 · 2013: 629 · 2012: 140
- FWCI
- 415.40
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- New England Journal of Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Mayo Clinic
- Bristol-Myers Squibb
- Massachusetts General Hospital
- Yale University
- Vanderbilt University
- University of Michigan
- Johns Hopkins University
- Yale Cancer Center
- Vanderbilt University Medical Center
- Genentech
- Sidney Kimmel Comprehensive Cancer Center
- National Cancer Institute (P30CA076292, R01CA142779)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- anti-PD-1, anti-PD-1 therapy, immune checkpoint inhibitors, melanoma, non-small cell lung cancer, renal cell carcinoma, castration-resistant prostate cancer, colorectal cancer, PD-L1 expression, immune-related adverse events, pulmonary toxicity, antitumor immunity, immune resistance, durable response, maximum tolerated dose, dose-limiting toxicity
- MeSH terms
- Nivolumab, Adult, Antibodies, Monoclonal, Antineoplastic Agents, Carcinoma, Non-Small-Cell Lung, Carcinoma, Renal Cell, Dose-Response Relationship, Drug, Female, Humans, Ligands, Male, Melanoma, Neoplasms, Prostatic Neoplasms, Colorectal Neoplasms, Programmed Cell Death 1 Receptor
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