Anti-tumor efficacy of a combination therapy with PD-L1 targeted alpha therapy and adoptive cell transfer of PD-1 deficient melanoma-specific human T-lymphocytes

References

• Robert C, Schachter J, Long GV, Arance A, Grob JJ, Mortier L, Daud A, Carlino MS, McNeil C, Lotem M, et al. Pembrolizumab versus Ipilimumab in Advanced Melanoma. N Engl J Med. 2015;372(26):2521–8. doi:10.1056/NEJMoa1503093.
   PubMed Web of Science ®Google Scholar
• Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, Schadendorf D, Dummer R, Smylie M, Rutkowski P, et al. Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma. N Engl J Med. 2015;372(1):23–34. doi:10.1056/NEJMoa1504030.
   Web of Science ®Google Scholar
• Galon J, Bruni D. Approaches to treat immune hot, altered and cold tumours with combination immunotherapies. Nat Rev Drug Discov. 2019;18:197–218.
   PubMed Web of Science ®Google Scholar
• Hellmann MD, Friedman CF, Wolchok JD,Combinatorial Cancer Immunotherapies. Adv Immunol. 2016;130:251–277.
   PubMed Web of Science ®Google Scholar
• Buchan SL, Rogel A, Al-Shamkhani A. The immunobiology of CD27 and OX40 and their potential as targets for cancer immunotherapy. Blood. 2018;131(1):39–48. doi:10.1182/blood-2017-07-741025.
   PubMed Web of Science ®Google Scholar
• Wang H, Kaur G, Sankin AI, Chen F, Guan F, Zang X. Immune checkpoint blockade and CAR-T cell therapy in hematologic malignancies. J Hematol Oncol. 2019;12(1):20–59. doi:10.1186/s13045-019-0746-1.
   PubMed Web of Science ®Google Scholar
• Heczey A, Louis CU, Savoldo B, Dakhova O, Durett A, Grilley B, Liu H, Wu MF, Mei Z, Gee A, et al. CAR T Cells Administered in Combination with Lymphodepletion and PD-1 Inhibition to Patients with Neuroblastoma. Mol Ther. 2017;25(9):2214–2224. doi:10.1016/j.ymthe.2017.05.012.
   PubMed Web of Science ®Google Scholar
• Chapuis AG, Lee SM, Thompson JA, Roberts IM, Margolin KA, Bhatia S, Sloan HL, Lai I, Wagener F, Shibuya K, et al. Combined IL-21-primed polyclonal CTL plus CTLA4 blockade controls refractory metastatic melanoma in a patient. J Exp Med. 2016;213(7):1133–1139. doi:10.1084/jem.20152021.
   PubMed Web of Science ®Google Scholar
• Mullinax JE, Hall M, Prabhakaran S, Weber J, Khushalani N, Eroglu Z, Brohl AS, Markowitz J, Royster E, Richards A, et al. Combination of Ipilimumab and Adoptive Cell Therapy with Tumor-Infiltrating Lymphocytes for Patients with Metastatic Melanoma. Front Oncol. 2018;8:44. doi:10.3389/fonc.2018.00044.
   PubMed Web of Science ®Google Scholar
• Lamichhane P, Deshmukh R, Brown JA, Jakubski S, Parajuli P, Nolan T, Raja D, Badawy M, Yoon T, Zmiyiwsky M, et al. Novel Delivery Systems for Checkpoint Inhibitors. Medicines (Basel). 2019;6(3):74. doi:10.3390/medicines6030074.
   PubMedGoogle Scholar
• Rupp LJ, Schumann K, Roybal KT, Gate RE, Ye CJ, Lim WA, Marson A. CRISPR/Cas9-mediated PD-1 disruption enhances anti-tumor efficacy of human chimeric antigen receptor T cells. Sci Rep. 2017;7(1):737. doi:10.1038/s41598-017-00462-8.
   PubMed Web of Science ®Google Scholar
• Guo X, Jiang H, Shi B, Zhou M, Zhang H, Shi Z, Du G, Luo H, Wu X, Wang Y, et al. Disruption of PD-1 Enhanced the Anti-tumor Activity of Chimeric Antigen Receptor T Cells Against Hepatocellular Carcinoma. Front Pharmacol. 2018;9:1118. doi:10.3389/fphar.2018.01118.
   PubMed Web of Science ®Google Scholar
• Zhao Z, Shi L, Zhang W, Han J, Zhang S, Fu Z, Cai J. CRISPR knock out of programmed cell death protein 1 enhances anti-tumor activity of cytotoxic T lymphocytes. Oncotarget. 2018;9(4):5208–5215. doi:10.18632/oncotarget.23730.
   PubMedGoogle Scholar
• Marotte L, Simon S, Vignard V, Dupré E, Gantier M, Cruard J, Alberge J-B, Hussong M, Deleine C, Heslan J-M, et al. Increased antitumor efficacy of PD-1-deficient melanoma-specific human lymphocytes. J Immunother Cancer. 2020;8(1):e000311. doi:10.1136/jitc-2019-000311
   Google Scholar
• Lhuillier C, Rudqvist N-P, Yamazaki T, Zhang T, Charpentier M, Galluzzi L, Dephoure N, Clement CC, Santambrogio L, Zhou XK, et al. Radiotherapy-exposed CD8+ and CD4+ neoantigens enhance tumor control. J Clin Invest 2021;131.
   Google Scholar
• Gorin J-B, Ménager J, Gouard S, Maurel C, Guilloux Y, Faivre-Chauvet A, Morgenstern A, Bruchertseifer F, Chérel M, Davodeau F, et al. Antitumor immunity induced after α irradiation. Neoplasia. 2014;16(4):319–328. doi:10.1016/j.neo.2014.04.002
   Google Scholar
• Gorin J-B, Guilloux Y, Morgenstern A, Chérel M, Davodeau F, Gaschet J. Using α radiation to boost cancer immunity? Oncoimmunology 2014; 3:e954925.
   Google Scholar
• Allen KJH, Jiao R, Malo ME, Frank C, Fisher DR, Rickles D, Dadachova E. Comparative Radioimmunotherapy of Experimental Melanoma with Novel Humanized Antibody to Melanin Labeled with 213Bismuth and 177Lutetium. Pharmaceutics 2019;11: 348.
   Google Scholar
• Capitao M, Perrin J, Simon S, Gouard S, Chouin N, Bruchertseifer F, Morgenstern A, Rbah-Vidal L, Chérel M, Scotet E, et al. Anti-Tumor Efficacy of PD-L1 Targeted Alpha-Particle Therapy in a Human Melanoma Xenograft Model. Cancers (Basel) 2021; 13: 1256.
   Google Scholar
• Simon S, Vignard V, Florenceau L, Dreno B, Khammari A, Lang F, Labarriere N. PD-1 expression conditions T cell avidity within an antigen-specific repertoire. Oncoimmunology 2016;5:e1104448.
   Google Scholar
• Bankhead P, Loughrey MB, Fernández JA, Dombrowski Y, McArt DG, Dunne PD, McQuaid S, Gray RT, Murray LJ, Coleman HG, et al. QuPath: Open source software for digital pathology image analysis. Sci Rep 2017;7:16878.
   Google Scholar
• Taube JM, Anders RA, Young GD, Xu H, Sharma R, McMiller TL, Chen S, Klein AP, Pardoll DM, Topalian SL, et al. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med. 2012;4(127) 127ra37–7. doi: 10.1126/scitranslmed.3003689.
   PubMed Web of Science ®Google Scholar
• Malo ME, Allen KJH, Jiao R, Frank C, Rickles D, Dadachova E. Mechanistic Insights into Synergy between Melanin-Targeting Radioimmunotherapy and Immunotherapy in Experimental Melanoma. Int J Mol Sci. 2020;21(22):8721. doi:10.3390/ijms21228721.
   PubMed Web of Science ®Google Scholar
• Josefsson A, Nedrow JR, Park S, Banerjee SR, Rittenbach A, Jammes F, Tsui B, Sgouros SG. Imaging, Biodistribution, and Dosimetry of Radionuclide-Labeled PD-L1 Antibody in an Immunocompetent Mouse Model of Breast Cancer. Cancer Res. 2016;76(2):472–479. doi:10.1158/0008-5472.CAN-15-2141.
   PubMed Web of Science ®Google Scholar
• Rouanet J, Benboubker V, Akil H, Hennino A, Auzeloux P, Besse S, Pereira B, Delorme S, Mansard S, D’Incan M, et al. Immune checkpoint inhibitors reverse tolerogenic mechanisms induced by melanoma targeted radionuclide therapy. Cancer Immunol Immunother. 2020;69(10):2075–2088. doi:10.1007/s00262-020-02606-8.
   PubMed Web of Science ®Google Scholar
• Brossart P. The Role of Antigen Spreading in the Efficacy of Immunotherapies. Clinical Cancer Research. 2020;26(17):4442–4447. doi:10.1158/1078-0432.CCR-20-0305.
   PubMed Web of Science ®Google Scholar