Preclinical immunoPET/CT imaging using Zr-89-labeled anti-PD-L1 monoclonal antibody for assessing radiation-induced PD-L1 upregulation in head and neck cancer and melanoma

References

• Ferris RL, Blumenschein G Jr, Fayette J, Guigay J, Colevas AD, Licitra L, Harrington K, Kasper S, Vokes EE, Even C et al. Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N Engl J Med 2016; 375:1856-67; PMID:27718784; https://doi.org/10.1056/NEJMoa1602252
   PubMed Web of Science ®Google Scholar
• Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369:122-33; PMID:23724867; https://doi.org/10.1056/NEJMoa1302369
   PubMed Web of Science ®Google Scholar
• Dovedi SJ, Adlard AL, Lipowska-Bhalla G, McKenna C, Jones S, Cheadle EJ, Stratford IJ, Poon E, Morrow M, Stewart R et al. Acquired resistance to fractionated radiotherapy can be overcome by concurrent PD-L1 blockade. Cancer Res 2014; 74:5458-68; PMID:25274032; https://doi.org/10.1158/0008-5472.CAN-14-1258
   PubMed Web of Science ®Google Scholar
• Deng L, Liang H, Burnette B, Beckett M, Darga T, Weichselbaum RR, Fu YX. Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice. J Clin Invest 2014; 124:687-95; PMID:24382348; https://doi.org/10.1172/JCI67313
   PubMed Web of Science ®Google Scholar
• Azad A, Yin Lim S, D'Costa Z, Jones K, Diana A, Sansom OJ, Kruger P, Liu S, McKenna WG, Dushek O, et al. PD-L1 blockade enhances response of pancreatic ductal adenocarcinoma to radiotherapy. EMBO Mol Med 2017; 9, 167–80; PMID:27932443; https://doi.org/10.15252/emmm.201606674.
   PubMed Web of Science ®Google Scholar
• Ilie M, Long-Mira E, Bence C, Butori C, Lassalle S, Bouhlel L, Fazzalari L, Zahaf K, Lalvée S, Washetine K et al. Comparative study of the PD-L1 status between surgically resected specimens and matched biopsies of NSCLC patients reveal major discordances: A potential issue for anti-PD-L1 therapeutic strategies. Ann Oncol 2016; 27:147-53; PMID:26483045; https://doi.org/10.1093/annonc/mdv489
   PubMed Web of Science ®Google Scholar
• McLaughlin J, Han G, Schalper KA, Carvajal-Hausdorf D, Pelekanou V, Rehman J, Velcheti V, Herbst R, LoRusso P, Rimm DL. Quantitative assessment of the heterogeneity of PD-L1 expression in non-small-cell lung cancer. JAMA Oncol 2016; 2:46-54; PMID:26562159; https://doi.org/10.1001/jamaoncol.2015.3638
   PubMed Web of Science ®Google Scholar
• Mansfield AS, Aubry MC, Moser JC, Harrington SM, Dronca RS, Park SS, Dong H. Temporal and spatial discordance of programmed cell death-ligand 1 expression and lymphocyte tumor infiltration between paired primary lesions and brain metastases in lung cancer. Ann Oncol 2016; 27:1953-8; PMID:27502709; https://doi.org/10.1093/annonc/mdw289
   PubMed Web of Science ®Google Scholar
• Sheng J, Fang W, Yu J, Chen N, Zhan J, Ma Y, Yang Y, Huang Y, Zhao H, Zhang L. Expression of programmed death ligand-1 on tumor cells varies pre and post chemotherapy in non-small cell lung cancer. Sci Rep 2016; 6:20090; PMID:26822379; https://doi.org/10.1038/srep20090 10.1038/srep23850
   PubMed Web of Science ®Google Scholar
• Lim SH, Hong M, Ahn S, Choi YL, Kim KM, Oh D, Ahn YC, Jung SH, Ahn MJ, Park K et al. Changes in tumour expression of programmed death-ligand 1 after neoadjuvant concurrent chemoradiotherapy in patients with squamous oesophageal cancer. Eur J Cancer 2016; 52:1-9; PMID:26623522; https://doi.org/10.1016/j.ejca.2015.09.019
   PubMed Web of Science ®Google Scholar
• Hettich M, Braun F, Bartholoma MD, Schirmbeck R, Niedermann G. High-resolution PET imaging with therapeutic antibody-based PD-1/PD-L1 checkpoint tracers. Theranostics 2016; 6:1629-40; PMID:27446497; https://doi.org/10.7150/thno.15253
   PubMed Web of Science ®Google Scholar
• Lesniak WG, Chatterjee S, Gabrielson M, Lisok A, Wharram B, Pomper MG, Nimmagadda S. PD-L1 detection in tumors using [(64)Cu]Atezolizumab with PET. Bioconjug Chem 2016; 27:2103-10; PMID:27458027; https://doi.org/10.1021/acs.bioconjchem.6b00348
   PubMed Web of Science ®Google Scholar
• Maute RL, Gordon SR, Mayer AT, McCracken MN, Natarajan A, Ring NG, Kimura R, Tsai JM, Manglik A, Kruse AC et al. Engineering high-affinity PD-1 variants for optimized immunotherapy and immuno-PET imaging. Proc Natl Acad Sci USA 2015; 112:E6506-14; PMID:26604307; https://doi.org/10.1073/pnas.1519623112
   PubMed Web of Science ®Google Scholar
• Chatterjee S, Lesniak WG, Miller MS, Lisok A, Sikorska E, Wharram B, Kumar D, Gabrielson M, Pomper MG, Gabelli SB et al. Rapid PD-L1 detection in tumors with PET using a highly specific peptide. Biochem Biophys Res Commun 2017; 483:258-63; PMID:28025143; https://doi.org/10.1016/j.bbrc.2016.12.156
   PubMed Web of Science ®Google Scholar
• McCabe KE, Wu AM. Positive progress in immunoPET—not just a coincidence. Cancer Biother Radiopharm 2010; 25:253-61; PMID:20578830; https://doi.org/10.1089/cbr.2010.0776
   PubMed Web of Science ®Google Scholar
• Hoover AC, Spanos WC, Harris GF, Anderson ME, Klingelhutz AJ, Lee JH. The role of human papillomavirus 16 E6 in anchorage-independent and invasive growth of mouse tonsil epithelium. Arch Otolaryngol Head Neck 2007; 133:495-502; PMID:17515506; https://doi.org/10.1001/archotol.133.5.495
   PubMedGoogle Scholar
• Zeng D, Guo Y, White AG, Cai Z, Modi J, Ferdani R, Anderson CJ. Comparison of conjugation strategies of cross-bridged macrocyclic chelators with cetuximab for copper-64 radiolabeling and PET imaging of EGFR in colorectal tumor-bearing mice. Mol Pharm 2014; 11:3980-7; PMID:24720806; https://doi.org/10.1021/mp500004m
   PubMed Web of Science ®Google Scholar
• Meares CF, McCall MJ, Reardan DT, Goodwin DA, Diamanti CI, McTigue M. Conjugation of antibodies with bifunctional chelating agents: Isothiocyanate and bromoacetamide reagents, methods of analysis, and subsequent addition of metal ions. Anal Biochem 1984; 142:68-78; PMID:6440451; https://doi.org/10.1016/0003-2697(84)90517-7
   PubMed Web of Science ®Google Scholar
• Lindmo T, Bunn PA Jr. Determination of the true immunoreactive fraction of monoclonal antibodies after radiolabeling. Methods Enzymol 1986; 121:678-91; PMID:3523136
   PubMed Web of Science ®Google Scholar
• Li J, Jie HB, Lei Y, Gildener-Leapman N, Trivedi S, Green T, Kane LP, Ferris RL. PD-1/SHP-2 inhibits Tc1/Th1 phenotypic responses and the activation of T cells in the tumor microenvironment. Cancer Res 2015; 75:508-18; PMID:25480946; https://doi.org/10.1158/0008-5472.CAN-14-1215
   PubMed Web of Science ®Google Scholar
• Schmitt NC, Trivedi S, Ferris RL. STAT1 activation is enhanced by cisplatin and variably affected by EGFR inhibition in HNSCC cells. Mol Cancer Ther 2015; 14:2103-11; PMID:26141950; https://doi.org/10.1158/1535-7163.MCT-15-0305
   PubMed Web of Science ®Google Scholar
• Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, Roche PC, Lu J, Zhu G, Tamada K et al. Tumor-associated B7-H1 promotes T-cell apoptosis: A potential mechanism of immune evasion. Nat Med 2002; 8:793-800; PMID:12091876; https://doi.org/10.1038/nm0902-1039c
   PubMed Web of Science ®Google Scholar
• Vanpouille-Box C, Diamond JM, Pilones KA, Zavadil J, Babb JS, Formenti SC, Barcellos-Hoff MH, Demaria S. TGFbeta is a master regulator of radiation therapy-induced antitumor immunity. Cancer Res 2015; 75:2232-42; PMID:25858148; https://doi.org/10.1158/0008-5472.CAN-14-3511
   PubMed Web of Science ®Google Scholar
• Schreiner B, Mitsdoerffer M, Kieseier BC, Chen L, Hartung HP, Weller M, Wiendl H. Interferon-beta enhances monocyte and dendritic cell expression of B7-H1 (PD-L1), a strong inhibitor of autologous T-cell activation: Relevance for the immune modulatory effect in multiple sclerosis. J Neuroimmunol 2004; 155:172-82; PMID:15342209; https://doi.org/10.1016/j.jneuroim.2004.06.013
   PubMed Web of Science ®Google Scholar
• Bellucci R, Martin A, Bommarito D, Wang K, Hansen SH, Freeman GJ, Ritz J. Interferon-gamma-induced activation of JAK1 and JAK2 suppresses tumor cell susceptibility to NK cells through upregulation of PD-L1 expression. Oncoimmunology 2015; 4:e1008824; PMID:26155422; https://doi.org/10.1080/2162402X.2015.1008824
   PubMed Web of Science ®Google Scholar
• Lugade AA, Sorensen EW, Gerber SA, Moran JP, Frelinger JG, Lord EM. Radiation-induced IFN-gamma production within the tumor microenvironment influences antitumor immunity. J Immunol 2008; 180:3132-9; PMID:18292536; https://doi.org/10.4049/jimmunol.180.5.3132
   PubMed Web of Science ®Google Scholar
• Shahabi V, Postow MA, Tuck D, Wolchok JD. Immune-priming of the tumor microenvironment by radiotherapy: Rationale for combination with immunotherapy to improve anticancer efficacy. Am J Clinical Oncol 2015; 38:90-7; PMID:25616204; https://doi.org/10.1097/COC.0b013e3182868ec8
   PubMed Web of Science ®Google Scholar
• Burnette BC, Liang H, Lee Y, Chlewicki L, Khodarev NN, Weichselbaum RR, Fu YX, Auh SL. The efficacy of radiotherapy relies upon induction of type i interferon-dependent innate and adaptive immunity. Cancer Res 2011; 71:2488-96; PMID:21300764; https://doi.org/10.1158/0008-5472.CAN-10-2820
   PubMed Web of Science ®Google Scholar
• Heskamp S, Hobo W, Molkenboer-Kuenen JDM, Olive D, Oyen WJG, Dolstra H, Boerman OC. Noninvasive imaging of tumor PD-L1 expression using radiolabeled anti-PD-L1 antibodies. Cancer Res 2015; 75:2928-36; PMID:25977331; https://doi.org/10.1158/0008-5472.CAN-14-3477
   PubMed Web of Science ®Google Scholar
• Chatterjee S, Lesniak WG, Gabrielson M, Lisok A, Wharram B, Sysa-Shah P, Azad BB, Pomper MG, Nimmagadda S. A humanized antibody for imaging immune checkpoint ligand PD-L1 expression in tumors. Oncotarget 2016; 7:10215-27; PMID:26848870; https://doi.org/10.18632/oncotarget.7143
   PubMed Web of Science ®Google Scholar
• Hettich M, Braun F, Bartholomä MD, Schirmbeck R, Niedermann G. High-resolution PET imaging with therapeutic antibody-based PD-1/PD-L1 checkpoint tracers. Theranostics 2016; 6:1629; PMID:27446497; https://doi.org/10.7150/thno.15253
   PubMed Web of Science ®Google Scholar
• Josefsson A, Nedrow JR, Park S, Banerjee SR, Rittenbach A, Jammes F, Tsui B, Sgouros G. Imaging, biodistribution, and dosimetry of radionuclide-labeled PD-L1 antibody in an immunocompetent mouse model of breast cancer. Cancer Res 2016; 76:472-9; PMID:26554829; https://doi.org/10.1158/0008-5472.CAN-15-2141
   PubMed Web of Science ®Google Scholar
• Lesniak WG, Chatterjee S, Gabrielson M, Lisok A, Wharram B, Pomper MG, Nimmagadda S. PD-L1 detection in tumors using [64Cu] atezolizumab with PET. Bioconjug Chem 2016; 27:2103-10; PMID:27458027; https://doi.org/10.1021/acs.bioconjchem.6b00348
   PubMed Web of Science ®Google Scholar
• Potchen EJ, Kinzie J, Curtis C, Siegel BA, Studer RK. Effect of irradiation on tumor microvascular permeability to macromolecules. Cancer 1972; 30:639-43; PMID:4677852; https://doi.org/10.1002/1097-0142(197209)30:3%3c639::AID-CNCR2820300308%3e3.0.CO;2-3
   PubMed Web of Science ®Google Scholar
• Kobayashi H, Reijnders K, English S, Yordanov AT, Milenic DE, Sowers AL, Citrin D, Krishna MC, Waldmann TA, Mitchell JB et al. Application of a macromolecular contrast agent for detection of alterations of tumor vessel permeability induced by radiation. Clin Cancer Res 2004; 10:7712-20; PMID:15570005; https://doi.org/10.1158/1078-0432.CCR-04-1175
   PubMed Web of Science ®Google Scholar