A novel bispecific antibody for EGFR-directed blockade of the PD-1/PD-L1 immune checkpoint

References

• Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol. 2008;26:677–704. doi:10.1146/annurev.immunol.26.021607.090331. PMID:18173375.
   PubMed Web of Science ®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 Mar 28;4(127):127ra37. doi:10.1126/scitranslmed.3003689.
   PubMed Web of Science ®Google Scholar
• Massi D, Brusa D, Merelli B, Ciano M, Audrito V, Serra S, Buonincontri R, Baroni G, Nassini R, Minocci D, et al. PD-L1 marks a subset of melanomas with a shorter overall survival and distinct genetic and morphological characteristics. Ann Oncol. 2014 Dec;25(12):2433–42. doi:10.1093/annonc/mdu452.
   PubMed Web of Science ®Google Scholar
• Shimoji M, Shimizu S, Sato K, Suda K, Kobayashi Y, Tomizawa K, Takemoto T, Mitsudomi T. Clinical and pathologic features of lung cancer expressing programmed cell death ligand 1 (PD-L1). Lung Cancer. 2016 Aug;98:69–75. doi:10.1016/j.lungcan.2016.04.021.
   PubMed Web of Science ®Google Scholar
• Thompson RH, Gillett MD, Cheville JC, Lohse CM, Dong H, Webster WS, Krejci KG, Lobo JR, Sengupta S, Chen L, et al. Costimulatory B7-H1 in renal cell carcinoma patients: Indicator of tumor aggressiveness and potential therapeutic target. Proc Natl Acad Sci U S A. 2004 Dec 7;101(49):17174–9. doi:10.1073/pnas.0406351101.
   PubMed Web of Science ®Google Scholar
• Chen N, Fang W, Zhan J, Hong S, Tang Y, Kang S, Zhang Y, He X, Zhou T, Qin T, et al. Upregulation of PD-L1 by EGFR activation mediates the immune escape in EGFR-driven NSCLC: Implication for optional immune targeted therapy for NSCLC patients with EGFR mutation. J Thorac Oncol. 2015 Jun;10(6):910–23. doi:10.1097/JTO.0000000000000500.
   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 Aug;8(8):793–800. doi:10.1038/nm730.
   PubMed Web of Science ®Google Scholar
• Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012 Jun 28;366(26):2443–54. doi:10.1056/NEJMoa1200690.
   PubMed Web of Science ®Google Scholar
• Weber JS, D'Angelo SP, Minor D, Hodi FS, Gutzmer R, Neyns B, Hoeller C, Khushalani NI, Miller WH, Jr, Lao CD, et al. Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate 037): A randomised, controlled, open-label, phase 3 trial. Lancet Oncol. 2015 Apr;16(4):375–84. doi:10.1016/S1470-2045(15)70076-8.
   PubMed Web of Science ®Google Scholar
• 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 Jun 25;372(26):2521–32. doi:10.1056/NEJMoa1503093.
   PubMed Web of Science ®Google Scholar
• Brahmer J, Reckamp KL, Baas P, Crino L, Eberhardt WE, Poddubskaya E, Antonia S, Pluzanski A, Vokes EE, Holgado E, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 2015 Jul 9;373(2):123–35. doi:10.1056/NEJMoa1504627.
   PubMed Web of Science ®Google Scholar
• Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, Patnaik A, Aggarwal C, Gubens M, Horn L, et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med. 2015 May 21;372(21):2018–28. doi:10.1056/NEJMoa1501824.
   PubMed Web of Science ®Google Scholar
• Nedrow JR, Josefsson A, Park S, Ranka S, Roy S, Sgouros G. Imaging of programmed death ligand-1 (PD-L1): Impact of protein concentration on distribution of anti-PD-L1 SPECT agent in an immunocompetent melanoma murine model. J Nucl Med. 2017 Oct;58(10):1560–66. doi:10.2967/jnumed.117.193268.
   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 January 15;76(2):472–9. doi:10.1158/0008-5472.CAN-15-2141.
   PubMed Web of Science ®Google Scholar
• Rokita M, Stec R, Bodnar L, Charkiewicz R, Korniluk J, Smoter M, Cichowicz M, Chyczewski L, Niklinski J, Kozlowski W, et al. Overexpression of epidermal growth factor receptor as a prognostic factor in colorectal cancer on the basis of the allred scoring system. Onco Targets Ther. 2013 July 24;6:967–76. doi:10.2147/OTT.S42446.
   PubMed Web of Science ®Google Scholar
• Selvaggi G, Novello S, Torri V, Leonardo E, De Giuli P, Borasio P, Mossetti C, Ardissone F, Lausi P, Scagliotti GV. Epidermal growth factor receptor overexpression correlates with a poor prognosis in completely resected non-small-cell lung cancer. Ann Oncol. 2004 January 01;15(1):28–32. doi:10.1093/annonc/mdh011.
   PubMed Web of Science ®Google Scholar
• Ciardiello F, Tortora G. EGFR antagonists in cancer treatment. N Engl J Med. 2008 Mar 13;358(11):1160–74. doi:10.1056/NEJMra0707704.
   PubMed Web of Science ®Google Scholar
• Thakur MK, Wozniak AJ. Spotlight on necitumumab in the treatment of non-small-cell lung carcinoma. Lung Cancer (Auckl). 2017 February 13;8:13–9.
   PubMed Web of Science ®Google Scholar
• Kroesen BJ, Nieken J, Sleijfer DT, Molema G, de Vries EG, Groen HJ, Helfrich W, The TH, Mulder NH, de Leij L. Approaches to lung cancer treatment using the CD3 x EGP-2-directed bispecific monoclonal antibody BIS-1. Cancer Immunol Immunother. 1997;45(3–4):203–6. doi:10.1007/s002620050433. PMID:9435874.
   PubMed Web of Science ®Google Scholar
• Krupka C, Kufer P, Kischel R, Zugmaier G, Lichtenegger FS, Kohnke T, Vick B, Jeremias I, Metzeler KH, Altmann T, et al. Blockade of the PD-1/PD-L1 axis augments lysis of AML cells by the CD33/CD3 BiTE antibody construct AMG 330: Reversing a T-cell-induced immune escape mechanism. Leukemia. 2016 February 01;30(2):484–91. doi:10.1038/leu.2015.214.
   PubMed Web of Science ®Google Scholar
• Aktas E, Kucuksezer UC, Bilgic S, Erten G, Deniz G. Relationship between CD107a expression and cytotoxic activity. Cell Immunol. 2009;254(2):149–54. doi:10.1016/j.cellimm.2008.08.007. PMID:18835598.
   PubMed Web of Science ®Google Scholar
• Zimmer L, Goldinger SM, Hofmann L, Loquai C, Ugurel S, Thomas I, Schmidgen MI, Gutzmer R, Utikal JS, Goppner D, et al. Neurological, respiratory, musculoskeletal, cardiac and ocular side-effects of anti-PD-1 therapy. Eur J Cancer. 2016 Jun;60:210–25. doi:10.1016/j.ejca.2016.02.024.
   PubMed Web of Science ®Google Scholar
• Akbay EA, Koyama S, Carretero J, Altabef A, Tchaicha JH, Christensen CL, Mikse OR, Cherniack AD, Beauchamp EM, Pugh TJ, et al. Activation of the PD-1 pathway contributes to immune escape in EGFR-driven lung tumors. Cancer Discov. 2013 December 01;3(12):1355–63. doi:10.1158/2159-8290.CD-13-0310.
   PubMed Web of Science ®Google Scholar
• Concha-Benavente F, Srivastava RM, Ferrone S, Ferris RL. EGFR-mediated tumor immunoescape: The imbalance between phosphorylated STAT1 and phosphorylated STAT3. Oncoimmunology. 2013 December 01;2(12):e27215. doi:10.4161/onci.27215.
   PubMed Web of Science ®Google Scholar
• Leibowitz MS, Srivastava RM, Andrade Filho PA, Egloff AM, Wang L, Seethala RR, Ferrone S, Ferris RL. SHP2 is overexpressed and inhibits pSTAT1-mediated APM component expression, T-cell attracting chemokine secretion, and CTL recognition in head and neck cancer cells. Clin Cancer Res. 2013 February 15;19(4):798–808. doi:10.1158/1078-0432.CCR-12-1517.
   PubMed Web of Science ®Google Scholar
• Brinkmann U, Kontermann RE. The making of bispecific antibodies. MAbs. 2017 March 01;9(2):182–212. doi:10.1080/19420862.2016.1268307.
   PubMed Web of Science ®Google Scholar
• Grenga I, Donahue RN, Lepone LM, Richards J, Schlom J. A fully human IgG1 anti-PD-L1 MAb in an in vitro assay enhances antigen-specific T-cell responses. Clin Transl Immunology. 2016 May 20;5(5):e83. doi:10.1038/cti.2016.27.
   PubMedGoogle Scholar
• Stewart R, Morrow M, Hammond SA, Mulgrew K, Marcus D, Poon E, Watkins A, Mullins S, Chodorge M, Andrews J, et al. Identification and pre-clinical characterization of MEDI4736, an antagonistic anti-PD-L1 monoclonal antibody. Cancer Immunol Res. 2015 Sep 3;(9):1052–62. doi:10.1158/2326-6066.CIR-14-0191.
   PubMed Web of Science ®Google Scholar
• Herbst RS, Soria JC, Kowanetz M, Fine GD, Hamid O, Gordon MS, Sosman JA, McDermott DF, Powderly JD, Gettinger SN, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature. 2014 Nov 27;515(7528):563–7. doi:10.1038/nature14011.
   PubMed Web of Science ®Google Scholar
• Heery CR, O'Sullivan Coyne GH, Madan RA, Schlom J, von Heydebreck A, Cuillerot J-M, Sabzevari H, Gulley J L. Phase I open-label, multiple ascending dose trial of MSB0010718C, an anti-PD-L1 monoclonal antibody, in advanced solid malignancies. J Clin Oncol. 2014; 32(Suppl 15):3064.
   Google Scholar
• Kelly K, Patel MR, Infante JR, Iannotti N, Nikolinakos P, Leach J, Wang D, Chandler JC, Jerusalem GHC, Gurtler JS, et al. Avelumab (MSB0010718C), an anti-PD-L1 antibody, in patients with metastatic or locally advanced solid tumors: Assessment of safety and tolerability in a phase I, openlabel expansion study. J Clin Oncol. 2015; 33(suppl; abstr 3044).
   Google Scholar
• Kaufman HL, Russell J, Hamid O, Bhatia S, Terheyden P, D'Angelo SP, Shih KC, Lebbe C, Linette GP, Milella M, et al. Avelumab in patients with chemotherapy-refractory metastatic merkel cell carcinoma: A multicentre, single-group, open-label, phase 2 trial. Lancet Oncol. 2016 October 01;17(10):1374–85. doi:10.1016/S1470-2045(16)30364-3.
   PubMed Web of Science ®Google Scholar
• Boyerinas B, Jochems C, Fantini M, Heery CR, Gulley JL, Tsang KY, Schlom J. Antibody-dependent cellular cytotoxicity activity of a novel anti-PD-L1 antibody avelumab (MSB0010718C) on human tumor cells. Cancer Immunology Research. 2015 Oct;3(10):1148–57. doi:10.1158/2326-6066.CIR-15-0059.
   PubMed Web of Science ®Google Scholar
• Fujii R, Friedman ER, Richards J, Tsang KY, Heery CR, Schlom J, Hodge JW. Enhanced killing of chordoma cells by antibody-dependent cell-mediated cytotoxicity employing the novel anti-PD-L1 antibody avelumab. Oncotarget. 2016 June 07;7(23):33498–511. doi:10.18632/oncotarget.9256.
   PubMedGoogle Scholar
• He Y, Hendriks D, van Ginkel R, Samplonius D, Bremer E, Helfrich W. Melanoma-directed activation of apoptosis using a bispecific antibody directed at MCSP and TRAIL receptor-2/death receptor-5. J Invest Dermatol. 2016 Feb;136(2):541–4. doi:10.1016/j.jid.2015.11.009.
   PubMed Web of Science ®Google Scholar
• Helfrich W, Haisma HJ, Magdolen V, Luther T, Bom VJ, Westra J, van der Hoeven R, Kroesen BJ, Molema G, de Leij L. A rapid and versatile method for harnessing scFv antibody fragments with various biological effector functions. J Immunol Methods. 2000 April 03;237(1–2):131–45. doi:10.1016/S0022-1759(99)00220-3.
   PubMed Web of Science ®Google Scholar
• Piccione EC, Juarez S, Liu J, Tseng S, Ryan CE, Narayanan C, Wang L, Weiskopf K, Majeti R. A bispecific antibody targeting CD47 and CD20 selectively binds and eliminates dual antigen expressing lymphoma cells. MAbs. 2015;7(5):946–56. doi:10.1080/19420862.2015.1062192. PMID:26083076.
   PubMed Web of Science ®Google Scholar
• Kroesen BJ, Ter Haar A, Spakman H, Willemse P, Sleijfer DT, de Vries EG, Mulder NH, Berendsen HH, Limburg PC, The TH. Local antitumour treatment in carcinoma patients with bispecific-monoclonal-antibody-redirected T cells. Cancer Immunol Immunother. 1993 Nov;37(6):400–7. doi:10.1007/BF01526797.
   PubMed Web of Science ®Google Scholar
• Heskamp S, Hobo W, Molkenboer-Kuenen JD, Olive D, Oyen WJ, Dolstra H, Boerman OC. Noninvasive imaging of tumor PD-L1 expression using radiolabeled anti-PD-L1 antibodies. Cancer Res. 2015 July 15;75(14):2928–36. doi:10.1158/0008-5472.CAN-14-3477.
   PubMed Web of Science ®Google Scholar