A novel cyclic peptide targeting LAG-3 for cancer immunotherapy by activating antigen-specific CD8+ T cell responses

Acta Pharmaceutica Sinica B - Tập 10 - Trang 1047-1060 - 2020
Wenjie Zhai1, Xiuman Zhou1, Hongfei Wang1, Wanqiong Li2, Guanyu Chen2, Xinghua Sui2, Guodong Li1, Yuanming Qi1, Yanfeng Gao1,2
1School of Life Sciences, Zhengzhou University, Zhengzhou, 450001, China
2School of Pharmaceutical Sciences (Shenzhen), Sun Yat-sen University, Guangzhou, 510006, China

Tài liệu tham khảo

Gravitz, 2013, Cancer immunotherapy, Nature, 504, S1, 10.1038/504S1a Couzin-Frankel, 2013, Breakthrough of the year 2013. Cancer immunotherapy, Science, 342, 1432, 10.1126/science.342.6165.1432 Hodi, 2010, Improved survival with ipilimumab in patients with metastatic melanoma, N Engl J Med, 363, 711, 10.1056/NEJMoa1003466 Ferris, 2016, Nivolumab for recurrent squamous-cell carcinoma of the head and neck, N Engl J Med, 375, 1856, 10.1056/NEJMoa1602252 Nghiem, 2016, PD-1 blockade with pembrolizumab in advanced merkel-cell carcinoma, N Engl J Med, 374, 2542, 10.1056/NEJMoa1603702 Migden, 2018, PD-1 blockade with cemiplimab in advanced cutaneous squamous-cell carcinoma, N Engl J Med, 379, 341, 10.1056/NEJMoa1805131 Socinski, 2018, Atezolizumab for first-line treatment of metastatic nonsquamous NSCLC, N Engl J Med, 378, 2288, 10.1056/NEJMoa1716948 D'Angelo, 2018, Efficacy and safety of first-line avelumab treatment in patients with stage IV metastatic merkel cell carcinoma: a preplanned interim analysis of a clinical trial, JAMA Oncol, 4 Massard, 2016, Safety and efficacy of durvalumab (MEDI4736), an anti-programmed cell death ligand-1 immune checkpoint inhibitor, in patients with advanced urothelial bladder cancer, J Clin Oncol, 34, 3119, 10.1200/JCO.2016.67.9761 Zhao, 2017, Intrinsic resistance of solid tumors to immune checkpoint blockade therapy, Cancer Res, 77, 817, 10.1158/0008-5472.CAN-16-2379 Topalian, 2012, Safety, activity, and immune correlates of anti-PD-1 antibody in cancer, N Engl J Med, 366, 2443, 10.1056/NEJMoa1200690 Turnis, 2015, Inhibitory receptors as targets for cancer immunotherapy, Eur J Immunol, 45, 1892, 10.1002/eji.201344413 Baumeister, 2016, Coinhibitory pathways in immunotherapy for cancer, Annu Rev Immunol, 34, 539, 10.1146/annurev-immunol-032414-112049 Anderson, 2016, Lag-3, Tim-3, and TIGIT: co-inhibitory receptors with specialized functions in immune regulation, Immunity, 44, 989, 10.1016/j.immuni.2016.05.001 Thommen, 2015, Progression of lung cancer is associated with increased dysfunction of T cells defined by coexpression of multiple inhibitory receptors, Cancer Immunol Res, 3, 1344, 10.1158/2326-6066.CIR-15-0097 Rotte, 2018, Mechanistic overview of immune checkpoints to support the rational design of their combinations in cancer immunotherapy, Ann Oncol, 29, 71, 10.1093/annonc/mdx686 Wierz, 2018, Dual PD1/LAG3 immune checkpoint blockade limits tumor development in a murine model of chronic lymphocytic leukemia, Blood, 131, 1617, 10.1182/blood-2017-06-792267 Harris-Bookman, 2018, Expression of LAG-3 and efficacy of combination treatment with anti-LAG-3 and anti-PD-1 monoclonal antibodies in glioblastoma, Int J Cancer, 143, 3201, 10.1002/ijc.31661 Huard, 1997, Characterization of the major histocompatibility complex class II binding site on LAG-3 protein, Proc Natl Acad Sci U S A, 94, 5744, 10.1073/pnas.94.11.5744 Triebel, 1990, LAG-3, a novel lymphocyte activation gene closely related to CD4, J Exp Med, 171, 1393, 10.1084/jem.171.5.1393 Huard, 1994, Lymphocyte-activation gene 3/major histocompatibility complex class II interaction modulates the antigenic response of CD4+ T lymphocytes, Eur J Immunol, 24, 3216, 10.1002/eji.1830241246 Workman, 2004, Lymphocyte activation gene-3 (CD223) regulates the size of the expanding T cell population following antigen activation in vivo, J Immunol, 172, 5450, 10.4049/jimmunol.172.9.5450 Workman, 2005, Negative regulation of T cell homeostasis by lymphocyte activation gene-3 (CD223), J Immunol, 174, 688, 10.4049/jimmunol.174.2.688 Grosso, 2007, LAG-3 regulates CD8+ T cell accumulation and effector function in murine self- and tumor-tolerance systems, J Clin Investig, 117, 3383, 10.1172/JCI31184 Huang, 2004, Role of LAG-3 in regulatory T cells, Immunity, 21, 503, 10.1016/j.immuni.2004.08.010 Camisaschi, 2010, LAG-3 expression defines a subset of CD4+ CD25high Foxp3+ regulatory T cells that are expanded at tumor sites, J Immunol, 184, 6545, 10.4049/jimmunol.0903879 Baixeras, 1992, Characterization of the lymphocyte activation gene 3-encoded protein. A new ligand for human leukocyte antigen class II antigens, J Exp Med, 176, 327, 10.1084/jem.176.2.327 Andrews, 2017, LAG3 (CD223) as a cancer immunotherapy target, Immunol Rev, 276, 80, 10.1111/imr.12519 Ascierto, 2017, Ann Oncol, 28, 611, 10.1093/annonc/mdx440.011 Woo, 2012, Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T-cell function to promote tumoral immune escape, Cancer Res, 72, 917, 10.1158/0008-5472.CAN-11-1620 Goding, 2013, Restoring immune function of tumor-specific CD4+ T cells during recurrence of melanoma, J Immunol, 190, 4899, 10.4049/jimmunol.1300271 Matsuzaki, 2010, Tumor-infiltrating NY-ESO-1-specific CD8+ T cells are negatively regulated by LAG-3 and PD-1 in human ovarian cancer, Proc Natl Acad Sci U S A, 107, 7875, 10.1073/pnas.1003345107 Sliwkowski, 2013, Antibody therapeutics in cancer, Science, 341, 1192, 10.1126/science.1241145 Wieder, 2018, Immune checkpoint blockade therapy, J Allergy Clin Immunol, 142, 1403, 10.1016/j.jaci.2018.02.042 Fosgerau, 2015, Peptide therapeutics: current status and future directions, Drug Discov Today, 20, 122, 10.1016/j.drudis.2014.10.003 Weinmann, 2016, Cancer immunotherapy: selected targets and small-molecule modulators, ChemMedChem, 11, 450, 10.1002/cmdc.201500566 Vlieghe, 2010, Synthetic therapeutic peptides: science and market, Drug Discov Today, 15, 40, 10.1016/j.drudis.2009.10.009 Vladimer, 2017, Global survey of the immunomodulatory potential of common drugs, Nat Chem Biol, 13, 681, 10.1038/nchembio.2360 Zhang, 2018, Structure reconstruction of LyP-1: Lc(LyP-1) coupling by amide bond inspires the brain metastatic tumor targeted drug delivery, Mol Pharm, 15, 430, 10.1021/acs.molpharmaceut.7b00801 Magiera-Mularz, 2017, Bioactive macrocyclic inhibitors of the PD-1/PD-L1 immune checkpoint, Angew Chem Int Ed Engl, 56, 13732, 10.1002/anie.201707707 Molek, 2011, Peptide phage display as a tool for drug discovery: targeting membrane receptors, Molecules, 16, 857, 10.3390/molecules16010857 Jerabek-Willemsen, 2014, MicroScale thermophoresis: interaction analysis and beyond, J Mol Struct, 1077, 101, 10.1016/j.molstruc.2014.03.009 Hmama, 1998, Attenuation of HLA-DR expression by mononuclear phagocytes infected with Mycobacterium tuberculosis is related to intracellular sequestration of immature class II heterodimers, J Immunol, 161, 4882, 10.4049/jimmunol.161.9.4882 He, 2016, Lymphocyte-activation gene-3, an important immune checkpoint in cancer, Cancer Sci, 107, 1193, 10.1111/cas.12986 Ascierto, 2017, Initial efficacy of anti-lymphocyte activation gene-3 (anti-LAG-3; BMS-986016) in combination with nivolumab (nivo) in pts with melanoma (MEL) previously treated with anti–PD-1/PD-L1 therapy, J Clin Oncol, 35, 9520, 10.1200/JCO.2017.35.15_suppl.9520 Tumeh, 2014, PD-1 blockade induces responses by inhibiting adaptive immune resistance, Nature, 515, 568, 10.1038/nature13954 Zhao, 2019, SHP2 inhibition triggers anti-tumor immunity and synergizes with PD-1 blockade, Acta Pharm Sin B, 9, 304, 10.1016/j.apsb.2018.08.009 Cook, 2016, LAG-3 confers a competitive disadvantage upon antiviral CD8+ T cell responses, J Immunol, 197, 119, 10.4049/jimmunol.1401594 Scala, 1998, Lymphocyte activation gene-3 (LAG-3) expression and IFN-γ production are variably coregulated in different human T lymphocyte subpopulations, J Immunol, 161, 489, 10.4049/jimmunol.161.1.489 Giraldo, 2015, Orchestration and prognostic significance of immune checkpoints in the microenvironment of primary and metastatic renal cell cancer, Clin Cancer Res, 21, 3031, 10.1158/1078-0432.CCR-14-2926 Durham, 2014, Lymphocyte activation gene 3 (LAG-3) modulates the ability of CD4 T-cells to be suppressed in vivo, PLoS One, 9, 10.1371/journal.pone.0109080 Farsam, 2011, Antitumor and immunomodulatory properties of artemether and its ability to reduce CD4+ CD25+ FOXP3+ Treg cells in vivo, Int Immunopharmacol, 11, 1802, 10.1016/j.intimp.2011.07.008 Betts, 2012, Suppression of tumour-specific CD4+ T cells by regulatory T cells is associated with progression of human colorectal cancer, Gut, 61, 1163, 10.1136/gutjnl-2011-300970 Gagliani, 2013, Coexpression of CD49b and LAG-3 identifies human and mouse T regulatory type 1 cells, Nat Med, 19, 739, 10.1038/nm.3179