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Novel Radiotracer for ImmunoPET Imaging of PD-1 Checkpoint Expression on Tumor Infiltrating Lymphocytes

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† ‡ § Radiology, School of Medicine, Bioengineering and §Materials Science and Engineering, Stanford University, Stanford, California 94305, United States
*E-mail: [email protected]. Phone: 650-725-2309. Fax: 650-724-4948.
Cite this: Bioconjugate Chem. 2015, 26, 10, 2062–2069
Publication Date (Web):August 26, 2015
https://doi.org/10.1021/acs.bioconjchem.5b00318
Copyright © 2015 American Chemical Society

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    Abstract

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    Immune checkpoint signaling through the programmed death 1 (PD-1) axis to its ligand (PD-L1) significantly dampens anti-tumor immune responses. Cancer patients treated with checkpoint inhibitors that block this suppressive signaling have exhibited objective response rates of 20–40% for advanced solid tumors, lymphomas, and malignant melanomas. This represents a tremendous advance in cancer treatment. Unfortunately, all patients do not respond to immune checkpoint blockade. Recent findings suggest that patients with tumor infiltrating lymphocytes (TILs) expressing PD-1 may be most likely to respond to αPD-1/PD-L1 checkpoint inhibitors. There is a compelling need for diagnostic and prognostic imaging tools to assess the PD-1 status of TILs in vivo. Here we have developed a novel immunoPET tracer to image PD-1 expressing TILs in a transgenic mouse model bearing melanoma. A 64Cu labeled anti-mouse antibody (IgG) PD-1 immuno positron emission tomography (PET) tracer was developed to detect PD-1 expressing murine TILs. Quality control of the tracer showed >95% purity by HPLC and >70% immunoreactivity in an in vitro cell binding assay. ImmunoPET scans were performed over 1–48 h on Foxp3+.LuciDTR4 mice bearing B16–F10 melanoma tumors. Mice receiving anti-PD-1 tracer (200 ± 10 μCi/10–12 μg/200 μL) revealed high tracer uptake in lymphoid organs and tumors. BLI images of FoxP3+ CD4+ Tregs known to express PD-1 confirmed lymphocyte infiltration of tumors at the time of PET imaging. Biodistribution measurements performed at 48 h revealed a high (11×) tumor to muscle uptake ratio of the PET tracer (p < 0.05). PD-1 tumors exhibited 7.4 ± 0.7%ID/g tracer uptake and showed a 2× fold signal decrease when binding was blocked by unlabeled antibody. To the best of our knowledge this data is the first report to image PD-1 expression in living subjects with PET. This radiotracer has the potential to assess the prognostic value of PD-1 in preclinical models of immunotherapy and may ultimately aid in predicting response to therapies targeting immune checkpoints.

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.bioconjchem.5b00318.

    • MALDI; in vitro live cell binding assay; Western blot analysis; immunofluorescent detection of PD-1 expression on TILs; materials and methods (PDF)

    • Movie of 64Cu-DOTA-anti-PD-1-mab immunoPET tracer in a melanoma mouse (MPG)

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