Fibrinogen-like Protein 1 Is a Major Immune Inhibitory Ligand of LAG-3

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 Andrews, 2017, LAG3 (CD223) as a cancer immunotherapy target, Immunol. Rev., 276, 80, 10.1111/imr.12519 Annunziato, 1996, Expression and release of LAG-3-encoded protein by human CD4+ T cells are associated with IFN-gamma production, FASEB J., 10, 769, 10.1096/fasebj.10.7.8635694 Annunziato, 1997, Opposite role for interleukin-4 and interferon-gamma on CD30 and lymphocyte activation gene-3 (LAG-3) expression by activated naive T cells, Eur. J. Immunol., 27, 2239, 10.1002/eji.1830270918 Ascierto, 2017, Checkpoint inhibitors in melanoma and early phase development in solid tumors: what’s the future?, J. Transl. Med., 15, 173, 10.1186/s12967-017-1278-5 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 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 Bettini, 2011, Cutting edge: accelerated autoimmune diabetes in the absence of LAG-3, J. Immunol., 187, 3493, 10.4049/jimmunol.1100714 Blackburn, 2009, Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection, Nat. Immunol., 10, 29, 10.1038/ni.1679 Bruniquel, 1998, Regulation of expression of the human lymphocyte activation gene-3 (LAG-3) molecule, a ligand for MHC class II, Immunogenetics, 48, 116, 10.1007/s002510050411 Camisaschi, 2010, LAG-3 expression defines a subset of CD4(+)CD25(high)Foxp3(+) regulatory T cells that are expanded at tumor sites, J. Immunol., 184, 6545, 10.4049/jimmunol.0903879 Cemerski, 2015, T cell activation and anti-tumor efficacy of anti-LAG-3 antibodies is independent of LAG-3 – MHCII blocking capacity, J. Immunother. Cancer, 3, 183, 10.1186/2051-1426-3-S2-P183 Chapoval, 2001, B7-H3: a costimulatory molecule for T cell activation and IFN-gamma production, Nat. Immunol., 2, 269, 10.1038/85339 Chen, 1992, Costimulation of antitumor immunity by the B7 counterreceptor for the T lymphocyte molecules CD28 and CTLA-4, Cell, 71, 1093, 10.1016/S0092-8674(05)80059-5 Chen, 1994, Tumor immunogenicity determines the effect of B7 costimulation on T cell-mediated tumor immunity, J. Exp. Med., 179, 523, 10.1084/jem.179.2.523 Chihara, 2018, Induction and transcriptional regulation of the co-inhibitory gene module in T cells, Nature, 558, 454, 10.1038/s41586-018-0206-z DeLong, 2018, Cytokine- and TCR-mediated regulation of T cell expression of Ly6C and Sca-1, J. Immunol., 200, 1761, 10.4049/jimmunol.1701154 Demchev, 2013, Targeted deletion of fibrinogen like protein 1 reveals a novel role in energy substrate utilization, PLoS ONE, 8, e58084, 10.1371/journal.pone.0058084 Dong, 2002, Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion, Nat. Med., 8, 793, 10.1038/nm730 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 Grosso, 2007, LAG-3 regulates CD8+ T cell accumulation and effector function in murine self- and tumor-tolerance systems, J. Clin. Invest., 117, 3383, 10.1172/JCI31184 Grosso, 2009, Functionally distinct LAG-3 and PD-1 subsets on activated and chronically stimulated CD8 T cells, J. Immunol., 182, 6659, 10.4049/jimmunol.0804211 Hara, 2001, Molecular cloning and functional expression analysis of a cDNA for human hepassocin, a liver-specific protein with hepatocyte mitogenic activity, Biochim. Biophys. Acta, 1520, 45, 10.1016/S0167-4781(01)00249-4 Hirano, 2005, Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity, Cancer Res., 65, 1089, 10.1158/0008-5472.1089.65.3 Horst, 2016, Modulation of liver tolerance by conventional and nonconventional antigen-presenting cells and regulatory immune cells, Cell. Mol. Immunol., 13, 277, 10.1038/cmi.2015.112 Huang, 2004, Role of LAG-3 in regulatory T cells, Immunity, 21, 503, 10.1016/j.immuni.2004.08.010 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 Huard, 1995, CD4/major histocompatibility complex class II interaction analyzed with CD4- and lymphocyte activation gene-3 (LAG-3)-Ig fusion proteins, Eur. J. Immunol., 25, 2718, 10.1002/eji.1830250949 Huard, 1996, T cell major histocompatibility complex class II molecules down-regulate CD4+ T cell clone responses following LAG-3 binding, Eur. J. Immunol., 26, 1180, 10.1002/eji.1830260533 Huard, 1997, Characterization of the major histocompatibility complex class II binding site on LAG-3 protein, Proc. Natl. Acad. Sci. USA, 94, 5744, 10.1073/pnas.94.11.5744 Kim, 2014, A draft map of the human proteome, Nature, 509, 575, 10.1038/nature13302 Kizuka, 2015, Clec4g (LSECtin) interacts with BACE1 and suppresses Aβ generation, FEBS Lett., 589, 1418, 10.1016/j.febslet.2015.04.060 Kouo, 2015, Galectin-3 shapes antitumor immune responses by suppressing CD8+ T cells via LAG-3 and inhibiting expansion of plasmacytoid dendritic cells, Cancer Immunol. Res., 3, 412, 10.1158/2326-6066.CIR-14-0150 Li, 2009, C-type lectin LSECtin interacts with DC-SIGNR and is involved in hepatitis C virus binding, Mol. Cell. Biochem., 327, 183, 10.1007/s11010-009-0056-y Li, 2010, Recombinant human hepassocin stimulates proliferation of hepatocytes in vivo and improves survival in rats with fulminant hepatic failure, Gut, 59, 817, 10.1136/gut.2008.171124 Liu, 2008, Fibrinogen-like protein 1, a hepatocyte derived protein is an acute phase reactant, Biochem. Biophys. Res. Commun., 365, 729, 10.1016/j.bbrc.2007.11.069 Liu, 2004, Characterization of a novel C-type lectin-like gene, LSECtin: demonstration of carbohydrate binding and expression in sinusoidal endothelial cells of liver and lymph node, J. Biol. Chem., 279, 18748, 10.1074/jbc.M311227200 Mao, 2016, Pathological α-synuclein transmission initiated by binding lymphocyte-activation gene 3, Science, 353, aah3374, 10.1126/science.aah3374 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. USA, 107, 7875, 10.1073/pnas.1003345107 Pettitt, 2009, Agouti C57BL/6N embryonic stem cells for mouse genetic resources, Nat. Methods, 6, 493, 10.1038/nmeth.1342 Pihlgren, 1996, Resting memory CD8+ T cells are hyperreactive to antigenic challenge in vitro, J. Exp. Med., 184, 2141, 10.1084/jem.184.6.2141 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 Samusik, 2016, Automated mapping of phenotype space with single-cell data, Nat. Methods, 13, 493, 10.1038/nmeth.3863 Schalper, 2015, Objective measurement and clinical significance of TILs in non-small cell lung cancer, J. Natl. Cancer Inst., 107, dju435, 10.1093/jnci/dju435 Shevach, 2009, Mechanisms of foxp3+ T regulatory cell-mediated suppression, Immunity, 30, 636, 10.1016/j.immuni.2009.04.010 Sica, 2003, B7-H4, a molecule of the B7 family, negatively regulates T cell immunity, Immunity, 18, 849, 10.1016/S1074-7613(03)00152-3 Stillman, 2006, Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death, J. Immunol., 176, 778, 10.4049/jimmunol.176.2.778 Tang, 2010, The DC-SIGN family member LSECtin is a novel ligand of CD44 on activated T cells, Eur. J. Immunol., 40, 1185, 10.1002/eji.200939936 Triebel, 1990, LAG-3, a novel lymphocyte activation gene closely related to CD4, J. Exp. Med., 171, 1393, 10.1084/jem.171.5.1393 van der Maaten, 2008, Visualizing data using t-SNE, J. Mach. Learn. Res., 9, 2579 Walunas, 1995, Ly-6C is a marker of memory CD8+ T cells, J. Immunol., 155, 1873, 10.4049/jimmunol.155.4.1873 Williams, 2017, The EGR2 targets LAG-3 and 4-1BB describe and regulate dysfunctional antigen-specific CD8+ T cells in the tumor microenvironment, J. Exp. Med., 214, 381, 10.1084/jem.20160485 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 Workman, 2003, The CD4-related molecule, LAG-3 (CD223), regulates the expansion of activated T cells, Eur. J. Immunol., 33, 970, 10.1002/eji.200323382 Workman, 2005, Negative regulation of T cell homeostasis by lymphocyte activation gene-3 (CD223), J. Immunol., 174, 688, 10.4049/jimmunol.174.2.688 Workman, 2002, Cutting edge: molecular analysis of the negative regulatory function of lymphocyte activation gene-3, J. Immunol., 169, 5392, 10.4049/jimmunol.169.10.5392 Workman, 2002, Phenotypic analysis of the murine CD4-related glycoprotein, CD223 (LAG-3), Eur. J. Immunol., 32, 2255, 10.1002/1521-4141(200208)32:8<2255::AID-IMMU2255>3.0.CO;2-A 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 Xu, 2014, LSECtin expressed on melanoma cells promotes tumor progression by inhibiting antitumor T-cell responses, Cancer Res., 74, 3418, 10.1158/0008-5472.CAN-13-2690 Yamamoto, 1993, Molecular cloning and initial characterization of a novel fibrinogen-related gene, HFREP-1, Biochem. Biophys. Res. Commun., 193, 681, 10.1006/bbrc.1993.1678 Yan, 2002, Cloning and characterization of a mouse liver-specific gene mfrep-1, up-regulated in liver regeneration, Cell Res., 12, 353, 10.1038/sj.cr.7290137 Yao, 2011, B7-h2 is a costimulatory ligand for CD28 in human, Immunity, 34, 729, 10.1016/j.immuni.2011.03.014