Blockade of ErbB2 and PD-L1 using a bispecific antibody to improve targeted anti-ErbB2 therapy

References

• Mittal D, Caramia F, Michiels S, Joensuu H, Kellokumpu-Lehtinen PL, Sotiriou C, Loi S, Smyth MJ. Improved treatment of breast cancer with anti-HER2 therapy requires Interleukin-21 signaling in CD8+ T cells. Cancer Res. 2016;76:264–274.
   PubMed Web of Science ®Google Scholar
• Mortenson ED, Park S, Jiang Z, Wang S, Fu YX. Effective anti-neu-initiated antitumor responses require the complex role of CD4+ T cells. Clin Cancer Res. 2013;19:1476–1486.
   PubMed Web of Science ®Google Scholar
• Park S, Jiang Z, Mortenson ED, Deng L, Radkevich-Brown O, Yang X, Sattar H, Wang Y, Brown NK, Greene M, et al. The therapeutic effect of anti-HER2/neu antibody depends on both innate and adaptive immunity. Cancer Cell. 2010;18:160–170.
   PubMed Web of Science ®Google Scholar
• Stagg J, Loi S, Divisekera U, Ngiow SF, Duret H, Yagita H, Teng MW, Smyth MJ. Anti-ErbB-2 mAb therapy requires type I and II interferons and synergizes with anti-PD-1 or anti-CD137 mAb therapy. Proc Natl Acad Sci U S A. 2011;108:7142–7147.
   PubMed Web of Science ®Google Scholar
• Valabrega G, Montemurro F, Aglietta M. Trastuzumab: mechanism of action, resistance and future perspectives in HER2-overexpressing breast cancer. Ann Oncol. 2007;18:977–984.
   PubMed Web of Science ®Google Scholar
• Chaganty BKR, Qiu S, Gest A, Lu Y, Ivan C, Calin GA, Weiner LM, Fan Z. Trastuzumab upregulates PD-L1 as a potential mechanism of trastuzumab resistance through engagement of immune effector cells and stimulation of IFNgamma secretion. Cancer Lett. 2018;430:47–56.
   PubMed Web of Science ®Google Scholar
• Turcotte M, Allard D, Mittal D, Bareche Y, Buisseret L, Jose V, Pommey S, Delisle V, Loi S, Joensuu H, et al. CD73 promotes resistance to HER2/ErbB2 antibody therapy. Cancer Res. 2017;77:5652–5663.
   PubMed Web of Science ®Google Scholar
• Hou Y, Nitta H, Wei L, Banks PM, Parwani AV, Li Z. Evaluation of immune reaction and PD-L1 expression using multiplex immunohistochemistry in HER2-positive breast cancer: the association with response to anti-HER2 neoadjuvant therapy. Clin Breast Cancer. 2018;18:e237–e44.
   PubMed Web of Science ®Google Scholar
• Tsang JY, Au WL, Lo KY, Ni YB, Hlaing T, Hu J, Chan S-K, Chan K-F, Cheung S-Y, Tse GM, et al. PD-L1 expression and tumor infiltrating PD-1+ lymphocytes associated with outcome in HER2+ breast cancer patients. Breast Cancer Res Treat. 2017;162:19–30.
   PubMed Web of Science ®Google Scholar
• Hou Y, Nitta H, Wei L, Banks PM, Lustberg M, Wesolowski R, Ramaswamy B, Parwani AV, Li Z. PD-L1 expression and CD8-positive T cells are associated with favorable survival in HER2-positive invasive breast cancer. Breast J. 2018;24:911–919.
   PubMed Web of Science ®Google Scholar
• Su S, Zhao J, Xing Y, Zhang X, Liu J, Ouyang Q, Chen J, Su F, Liu Q, Song E. Immune checkpoint inhibition overcomes ADCP-induced immunosuppression by macrophages. Cell. 2018;175:442–57 e23.
   PubMed Web of Science ®Google Scholar
• Loi S, Giobbie-Hurder A, Gombos A, Bachelot T, Hui R, Curigliano G, Campone M, Biganzoli L, Bonnefoi H, Jerusalem G, et al. Pembrolizumab plus trastuzumab in trastuzumab-resistant, advanced, HER2-positive breast cancer (PANACEA): a single-arm, multicentre, phase 1b-2 trial. Lancet Oncol. 2019;20:371–382.
   PubMed Web of Science ®Google Scholar
• Sedykh SE, Prinz VV, Buneva VN, Nevinsky GA. Bispecific antibodies: design, therapy, perspectives. Drug Des Devel Ther. 2018;12:195–208.
   PubMed Web of Science ®Google Scholar
• Labrijn AF, Janmaat ML, Reichert JM, Parren P. Bispecific antibodies: a mechanistic review of the pipeline. Nat Rev Drug Discov. 2019;18(8):585–608.
   PubMed Web of Science ®Google Scholar
• Brack S, Attinger-Toller I, Schade B, Mourlane F, Klupsch K, Woods R, Hachemi H, von der Bey U, Koenig-Friedrich S, Bertschinger J, et al. A bispecific HER2-targeting FynomAb with superior antitumor activity and novel mode of action. Mol Cancer Ther. 2014;13:2030–2039.
   PubMed Web of Science ®Google Scholar
• Geuijen CAW, De Nardis C, Maussang D, Rovers E, Gallenne T, Hendriks LJA, Visser T, Nijhuis R, Logtenberg T, de Kruif J, et al. Unbiased combinatorial screening identifies a bispecific IgG1 that potently inhibits HER3 signaling via HER2-guided ligand blockade. Cancer Cell. 2018;33:922–36 e10.
   PubMed Web of Science ®Google Scholar
• Junttila TT, Li J, Johnston J, Hristopoulos M, Clark R, Ellerman D,  Wang BE, Li Y, Mathieu M, Li G. Antitumor efficacy of a bispecific antibody that targets HER2 and activates T cells. Cancer Res. 2014;74:5561–5571.
   PubMed Web of Science ®Google Scholar
• Li J, Ybarra R, Mak J, Herault A, De Almeida P, Arrazate A, Ziai J, Totpal K, Junttila MR, Walsh KB, et al. IFNgamma-induced chemokines are required for CXCR3-mediated T-cell recruitment and antitumor efficacy of anti-HER2/CD3 bispecific antibody. Clin Cancer Res. 2018;24:6447–6458.
   PubMed Web of Science ®Google Scholar
• Rius Ruiz I, Vicario R, Morancho B, Morales CB, Arenas EJ, Herter S, Freimoser-Grundschober A, Somandin J, Sam J, Ast O, et al. p95HER2-T cell bispecific antibody for breast cancer treatment. Sci Transl Med. 2018;10.pii: eaat1445.
   PubMed Web of Science ®Google Scholar
• Humphries MP, Hynes S, Bingham V, Cougot D, James J, Patel-Socha F, Parkes EE, Blayney JK, O’Rorke MA, Irwin GW, et al. Automated tumour recognition and digital pathology scoring unravels new role for PD-L1 in predicting good outcome in ER-/HER2+ breast cancer. J Oncol. 2018;2018:2937012.
   PubMedGoogle Scholar
• Kim A, Lee SJ, Kim YK, Park WY, Park DY, Kim JY, Lee CH, Gong G, Huh GY, Choi KU. Programmed death-ligand 1 (PD-L1) expression in tumour cell and tumour infiltrating lymphocytes of HER2-positive breast cancer and its prognostic value. Sci Rep. 2017;7:11671.
   PubMed Web of Science ®Google Scholar
• Kowanetz M, Zou W, Gettinger SN, Koeppen H, Kockx M, Schmid P, Kadel EE, Wistuba I, Chaft J, Rizvi NA, et al. Differential regulation of PD-L1 expression by immune and tumor cells in NSCLC and the response to treatment with atezolizumab (anti-PD-L1). Proc Natl Acad Sci U S A. 2018;115:E10119–E10126.
   PubMed Web of Science ®Google Scholar
• Castro F, Cardoso AP, Goncalves RM, Serre K, Oliveira MJ. Interferon-gamma at the crossroads of tumor immune surveillance or evasion. Front Immunol. 2018;9:847.
   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;515:563–567.
   PubMed Web of Science ®Google 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 characterization of MEDI4736, an antagonistic anti-PD-L1 monoclonal antibody. Cancer Immunol Res. 2015;3:1052–1062.
   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 Immunol Res. 2015;3:1148–1157.
   PubMed Web of Science ®Google Scholar
• Ali HR, Provenzano E, Dawson SJ, Blows FM, Liu B, Shah M,  Earl HM, Poole CJ, Hiller L, Dunn JA, et al. Association between CD8+ T-cell infiltration and breast cancer survival in 12,439 patients. Ann Oncol. 2014;25:1536–1543.
   PubMed Web of Science ®Google Scholar
• Zilio S, Serafini P. Neutrophils and Granulocytic MDSC: the Janus God of Cancer Immunotherapy. Vaccines (Basel). 2016;4.pii: E31.
   PubMed Web of Science ®Google Scholar
• Stagg J, Sharkey J, Pommey S, Young R, Takeda K, Yagita H, Johnstone RW, Smyth MJ. Antibodies targeted to TRAIL receptor-2 and ErbB-2 synergize in vivo and induce an antitumor immune response. Proc Natl Acad Sci U S A. 2008;105:16254–16259.
   PubMed Web of Science ®Google Scholar
• Labrijn AF, Meesters JI, Bunce M, Armstrong AA, Somani S, Nesspor TC, Chiu ML, Altintaş I, Verploegen S, Schuurman J, et al. Efficient generation of bispecific murine antibodies for pre-clinical investigations in syngeneic rodent models. Sci Rep. 2017;7:2476.
   PubMed Web of Science ®Google Scholar
• Labrijn AF, Meesters JI, de Goeij BE, van Den Bremer ET, Neijssen J, van Kampen MD, Strumane K, Verploegen S, Kundu A, Gramer MJ, et al. Efficient generation of stable bispecific IgG1 by controlled Fab-arm exchange. Proc Natl Acad Sci U S A. 2013;110:5145–5150.
   PubMed Web of Science ®Google Scholar
• Labrijn AF, Meesters JI, Priem P, de Jong RN, van Den Bremer ET, van Kampen MD, Gerritsen AF, Schuurman J, Parren PWHI. Controlled Fab-arm exchange for the generation of stable bispecific IgG1. Nat Protoc. 2014;9:2450–2463.
   PubMed Web of Science ®Google Scholar