Combinatorial blockade for cancer immunotherapy: targeting emerging immune checkpoint receptors

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Oncology meets immunology: the cancer-immunity cycle.

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Cutting Edge: TIGIT Has T Cell-Intrinsic Inhibitory Functions

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Genome-wide analysis identifies NR4A1 as a key mediator of T cell dysfunction

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Tiragolumab plus atezolizumab versus placebo plus atezolizumab as a first-line treatment for PD-L1-selected non-small-cell lung cancer (CITYSCAPE): primary and follow-up analyses of a randomised, double-blind, phase 2 study

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Induction and transcriptional regulation of the co-inhibitory gene module in T cells

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Targeted deletion of PD-1 in myeloid cells induces antitumor immunity

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Progression of Lung Cancer Is Associated with Increased Dysfunction of T Cells Defined by Coexpression of Multiple Inhibitory Receptors

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VISTA is an acidic pH-selective ligand for PSGL-1

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Tim-3 finds its place in the cancer immunotherapy landscape

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Characterization of the lymphocyte activation gene 3-encoded protein. A new ligand for human leukocyte antigen class II antigens.

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Bat3 promotes T cell responses and autoimmunity by repressing Tim-3-mediated cell death and exhaustion

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Cutting Edge: Molecular Analysis of the Negative Regulatory Function of Lymphocyte Activation Gene-3

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TIM-3 regulates CD103+ dendritic cell function and response to chemotherapy in breast cancer

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Restriction of PD-1 function by cis -PD-L1/CD80 interactions is required for optimal T cell responses

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The promising immune checkpoint LAG-3: from tumor microenvironment to cancer immunotherapy

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LSECtin Expressed on Melanoma Cells Promotes Tumor Progression by Inhibiting Antitumor T-cell Responses

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PD-L1:CD80 Cis-Heterodimer Triggers the Co-stimulatory Receptor CD28 While Repressing the Inhibitory PD-1 and CTLA-4 Pathways

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Immune-checkpoint proteins VISTA and PD-1 nonredundantly regulate murine T-cell responses

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Phase I/Ib Clinical Trial of Sabatolimab, an Anti‐TIM‐3 Antibody, Alone and in Combination with Spartalizumab, an Anti‐PD‐1 Antibody, in Advanced Solid Tumors

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Combination anti–CTLA-4 plus anti–PD-1 checkpoint blockade utilizes cellular mechanisms partially distinct from monotherapies

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Recruitment of Grb2 and SHIP1 by the ITT-like motif of TIGIT suppresses granule polarization and cytotoxicity of NK cells

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CTLA-4 in Regulatory T Cells for Cancer Immunotherapy

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VSIG ‐3 as a ligand of VISTA inhibits human T‐cell function

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Expression and functional significance of an additional ligand for CTLA-4.

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Control of signaling-mediated clearance of apoptotic cells by the tumor suppressor p53

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CD226 opposes TIGIT to disrupt Tregs in melanoma

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A highly conserved tyrosine of Tim‐3 is phosphorylated upon stimulation by its ligand galectin‐9

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Disruption of the immune-checkpoint VISTA gene imparts a proinflammatory phenotype with predisposition to the development of autoimmunity

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Immunogenomic Landscape of Hematological Malignancies

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Immune-Checkpoint Protein VISTA Regulates Antitumor Immunity by Controlling Myeloid Cell–Mediated Inflammation and Immunosuppression

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Tim-3 Expression Defines Regulatory T Cells in Human Tumors

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PD-L1 Binds to B7-1 Only In Cis on the Same Cell Surface

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CA-170 – A Potent Small-Molecule PD-L1 Inhibitor or Not?

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Constitutive Clathrin-mediated Endocytosis of CTLA-4 Persists during T Cell Activation

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Decreased Galectin-9 and Increased Tim-3 Expression Are Related to Poor Prognosis in Gastric Cancer

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Apoptosis of tumor infiltrating effector TIM-3+CD8+ T cells in colon cancer

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PD-1 derived CA-170 is an oral immune checkpoint inhibitor that exhibits preclinical anti-tumor efficacy

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Hallmarks of Resistance to Immune-Checkpoint Inhibitors

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PD-1H (VISTA)–mediated suppression of autoimmunity in systemic and cutaneous lupus erythematosus

Han, X. N., Vesely, M. D., Yang, W., Sanmamed, M. F., Badri, T., Alawa, J., López‐Giráldez, F., Gaule, P., Lee, S. W., Zhang, J., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aax1159 · Cited by 139

Expression of LAG-3 is coincident with the impaired effector function of HBV-specific CD8+ T cell in HCC patients

Li, F., Zhang, Y., Jin, G., Yao, L., & Wu, D. (2012) · Immunology Letters · doi:10.1016/j.imlet.2012.12.004 · Cited by 138

T Cell Ig and Mucin Domain–Containing Protein 3 Is Recruited to the Immune Synapse, Disrupts Stable Synapse Formation, and Associates with Receptor Phosphatases

Clayton, K. L., Haaland, M. S., Douglas-Vail, M. B., Mujib, S., Chew, G. M., Ndhlovu, L. C., & Ostrowski, M. A. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1302663 · Cited by 134

The structure, expression, and multifaceted role of immune-checkpoint protein VISTA as a critical regulator of anti-tumor immunity, autoimmunity, and inflammation

Xu, W., Hiếu, T., Malarkannan, S., & Wang, L. L. (2018) · Cellular and Molecular Immunology · doi:10.1038/cmi.2017.148 · Cited by 132

Targeting PD-1 and Tim-3 Pathways to Reverse CD8 T-Cell Exhaustion and Enhance Ex Vivo T-Cell Responses to Autologous Dendritic/Tumor Vaccines

Liu, J., Zhang, S., Hu, Y., Yang, Z., Li, J. P., Liu, X., Deng, L., Wang, Y., Zhang, X., Jiang, T., et al. (2016) · Journal of Immunotherapy · doi:10.1097/cji.0000000000000122 · Cited by 127

Molecular Pathways and Mechanisms of LAG3 in Cancer Therapy

Andrews, L. P., Cillo, A. R., Karapetyan, L., Kirkwood, J. M., Workman, C. J., & Vignali, D. A. A. (2022) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-21-2390 · Cited by 122

Structure and Functional Binding Epitope of V-domain Ig Suppressor of T Cell Activation

Mehta, N., Maddineni, S., Mathews, I. I., Sperberg, R. A. P., Huang, P., & Cochran, J. R. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.07.073 · Cited by 121

VISTA expression on tumor-infiltrating inflammatory cells in primary cutaneous melanoma correlates with poor disease-specific survival

Kuklinski, L. F., Yan, S., Li, Z., Fisher, J. L., Cheng, C., Noelle, R. J., Angeles, C. V., Turk, M. J., & Ernstoff, M. S. (2018) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-018-2169-1 · Cited by 120

A single-cell atlas of diffuse large B cell lymphoma

Ye, X., Wang, L., Nie, M., Wang, Y., Dong, S., Ren, W., Li, G., Li, Z., Wu, K., & Pan‐Hammarström, Q. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110713 · Cited by 116

V-domain Ig-containing suppressor of T-cell activation (VISTA), a potentially targetable immune checkpoint molecule, is highly expressed in epithelioid malignant pleural mesothelioma

Muller, S., Lai, W. V., Adusumilli, P. S., Desmeules, P., Frosina, D., Jungbluth, A. A., Ni, A., Eguchi, T., Travis, W. D., Ladanyi, M., et al. (2019) · Modern Pathology · doi:10.1038/s41379-019-0364-z · Cited by 108

Ligand-Receptor Interactions of Galectin-9 and VISTA Suppress Human T Lymphocyte Cytotoxic Activity

Yasinska, I. M., Meyer, N. H., Schlichtner, S., Hussain, R., Siligardi, G., Casely‐Hayford, M. A., Fiedler, W., Wellbrock, J., Desmet, C., Calzolai, L., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.580557 · Cited by 108

Expression of Tim-3 drives phenotypic and functional changes in Treg cells in secondary lymphoid organs and the tumor microenvironment

Banerjee, H., Nieves-Rosado, H. M., Kulkarni, A., Murter, B., McGrath, K. V., Chandran, U. R., Chang, A., Szymczak-Workman, A. L., Vujanovic, L. N., Delgoffe, G. M., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109699 · Cited by 108

Clinical landscape of LAG-3-targeted therapy

Chocarro, L., Blanco, E., Arasanz, H., Fernández, L., Bocanegra, A., Echaide, M., Garnica, M., Ramos, P., Fernández-Hinojal, G., Vera, R., et al. (2022) · Immuno-Oncology Technology · doi:10.1016/j.iotech.2022.100079 · Cited by 107

Tim-3 promotes tumor-promoting M2 macrophage polarization by binding to STAT1 and suppressing the STAT1-miR-155 signaling axis

Jiang, X., Zhou, T., Xiao, Y., Yu, J., Dou, S., Chen, G., Wang, R., He, X., Hou, C., Wang, W., et al. (2016) · OncoImmunology · doi:10.1080/2162402x.2016.1211219 · Cited by 106

Antigen-Independent Induction of Tim-3 Expression on Human T Cells by the Common γ-Chain Cytokines IL-2, IL-7, IL-15, and IL-21 Is Associated with Proliferation and Is Dependent on the Phosphoinositide 3-Kinase Pathway

Mujib, S., Jones, R. B., Lo, C. C., Aidarus, N., Clayton, K., Sakhdari, A., Benko, E., Kovacs, C. M., & Ostrowski, M. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1102609 · Cited by 105

PD-1 and LAG-3 Dominate Checkpoint Receptor–Mediated T-cell Inhibition in Renal Cell Carcinoma

Zelba, H., Bedke, J., Hennenlotter, J., Mostböck, S., Zettl, M., Zichner, T., Chandran, A., Stenzl, A., Rammensee, H., & Gouttefangeas, C. (2019) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-19-0146 · Cited by 105

A first-in-human study of the anti-LAG-3 antibody favezelimab plus pembrolizumab in previously treated, advanced microsatellite stable colorectal cancer

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MicroRNA Profile of Circulating CD4-positive Regulatory T Cells in Human Adults and Impact of Differentially Expressed MicroRNAs on Expression of Two Genes Essential to Their Function

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Regulation of expression of the human lymphocyte activation gene-3 ( LAG-3 ) molecule, a ligand for MHC class II

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Single-cell characterization of anti–LAG-3 and anti–PD-1 combination treatment in patients with melanoma

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PD-1 agonism by anti-CD80 inhibits T cell activation and alleviates autoimmunity

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LAG3: a novel immune checkpoint expressed by multiple lymphocyte subsets in diffuse large B-cell lymphoma

Keane, C., Law, S. C., Gould, C., Birch, S. E., Sabdia, M. B., de Long, L. M., Thillaiyampalam, G., Abro, E. U., Tobin, J. W. D., Tan, X., et al. (2020) · Blood Advances · doi:10.1182/bloodadvances.2019001390 · Cited by 101

Eftilagimod alpha, a soluble lymphocyte activation gene-3 (LAG-3) protein plus pembrolizumab in patients with metastatic melanoma

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LAG-3 expression on peripheral blood cells identifies patients with poorer outcomes after immune checkpoint blockade

Shen, R., Postow, M. A., Adamow, M. J., Arora, A., Hannum, M., Maher, C. A., Wong, P., Curran, M. A., Hollmann, T. J., Jia, L., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abf5107 · Cited by 100

Immune-checkpoint protein VISTA critically regulates the IL-23/IL-17 inflammatory axis

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Regulation of Surface and Intracellular Expression of CTLA‐4 on Human Peripheral T Cells

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TIGIT blockade repolarizes AML-associated TIGIT + M2 macrophages to an M1 phenotype and increases CD47-mediated phagocytosis

Brauneck, F., Fischer, B., Witt, M., Muschhammer, J., Oelrich, J., Avelar, P., Tsoka, S., Bullinger, L., Seubert, E., Smit, D. J., et al. (2022) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2022-004794 · Cited by 91

TIGIT and PD1 Co-blockade Restores ex vivo Functions of Human Tumor-Infiltrating CD8+ T Cells in Hepatocellular Carcinoma

Ge, Z., Zhou, G., Carrascosa, L. C., Gausvik, E., Boor, P. P. C., Noordam, L., Doukas, M., Polak, W. G., Terkivatan, T., Pan, Q., et al. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2021.03.003 · Cited by 90

Resistance to PD1 blockade in the absence of metalloprotease-mediated LAG3 shedding

Andrews, L. P., Somasundaram, A., Moskovitz, J. M., Szymczak-Workman, A. L., Liu, C., Cillo, A. R., Huang, L., Normolle, D. P., Moynihan, K. D., Taniuchi, I., et al. (2020) · Science Immunology · doi:10.1126/sciimmunol.abc2728 · Cited by 87

Increased coexpression of PD-L1 and TIM3/TIGIT is associated with poor overall survival of patients with esophageal squamous cell carcinoma

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Complimentary mechanisms of dual checkpoint blockade expand unique T-cell repertoires and activate adaptive anti-tumor immunity in triple-negative breast tumors

Crosby, E. J., Wei, J.-P., Yang, X. Y., Lei, G., Wang, T., Liu, C.-X., Agarwal, P., Korman, A. J., Morse, M. A., Gouin, K. H., et al. (2017) · OncoImmunology · doi:10.1080/2162402x.2017.1421891 · Cited by 81

Clinically approved combination immunotherapy: Current status, limitations, and future perspective

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Phase 1 trial of TIM-3 inhibitor cobolimab monotherapy and in combination with PD-1 inhibitors nivolumab or dostarlimab (AMBER).

Falchook, G. S., Ribas, A., Davar, D., et al. (2022) · Journal of Clinical Oncology · doi:10.1200/jco.2022.40.16_suppl.2504 · Cited by 73

Functional characterization of PD1+TIM3+ tumor-infiltrating T cells in DLBCL and effects of PD1 or TIM3 blockade

Roussel, M., Le, K.-S., Granier, C., Gutierrez, F. L., Foucher, E. D., Gallou, S. L., Pangault, C., Xerri, L., Launay, V., Lamy, T., et al. (2021) · Blood Advances · doi:10.1182/bloodadvances.2020003080 · Cited by 72

PD-L1 blockade engages tumor-infiltrating lymphocytes to co-express targetable activating and inhibitory receptors

Beyrend, G., van der Gracht, E. T. I., Yilmaz, A. N., van Duikeren, S., Camps, M. G. M., Höllt, T., Vilanova, A., van Unen, V., Koning, F., de Miranda, N. F. C. C., et al. (2019) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-019-0700-3 · Cited by 70

Prognostic implication of TIM-3 in clear cell renal cell carcinoma

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Rationally targeted anti-VISTA antibody that blockades the C-C’ loop region can reverse VISTA immune suppression and remodel the immune microenvironment to potently inhibit tumor growth in an Fc independent manner

Thakkar, D., Paliwal, S., Dharmadhikari, B., Guan, S., Liu, L., Kar, S., Tulsian, N. K., Gruber, J. J., DiMascio, L. N., Paszkiewicz, K. H., et al. (2022) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2021-003382 · Cited by 67

Expression regulation of co-inhibitory molecules on human natural killer cells in response to cytokine stimulations

Sun, H., Sun, C., & Xiao, W. (2013) · Cytokine · doi:10.1016/j.cyto.2013.09.016 · Cited by 65

Immunoregulation of Dendritic Cells by the Receptor T cell Ig and Mucin Protein-3 via Bruton’s Tyrosine Kinase and c-Src

Maurya, N., Gujar, R., Gupta, M., Yadav, V., Verma, S., & Sen, P. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1400395 · Cited by 62

Prognostic Value of T Cell Immunoglobulin Mucin-3 in Prostate Cancer

Piao, Y.-R., Piao, L., Zhu, L., Jin, Z., & Dong, X.-Z. (2013) · Asian Pacific Journal of Cancer Prevention · doi:10.7314/apjcp.2013.14.6.3897 · Cited by 62

VISTA: A Promising Target for Cancer Immunotherapy?

Tagliamento, M., Agostinetto, E., Borea, R., Brandão, M., Poggio, F. B., Addeo, A., & Lambertini, M. (2021) · ImmunoTargets and Therapy · doi:10.2147/itt.s260429 · Cited by 62

Structural insight into T cell coinhibition by PD-1H (VISTA)

Slater, B., Han, X. N., Chen, L., & Xiong, Y. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1908711117 · Cited by 60

A pan-cancer analysis revealing the role of TIGIT in tumor microenvironment

Wen, J., Mao, X., Cheng, Q., Liu, Z., & Liu, F. (2021) · Scientific Reports · doi:10.1038/s41598-021-01933-9 · Cited by 59

ARC-7: Randomized phase 2 study of domvanalimab + zimberelimab ± etrumadenant versus zimberelimab in first-line, metastatic, PD-L1-high non-small cell lung cancer (NSCLC).

Johnson, M. L., Fox, W., Lee, Y., et al. (2022) · Journal of Clinical Oncology · doi:10.1200/jco.2022.40.36_suppl.397600 · Cited by 59

The Expression Pattern and Clinical Significance of the Immune Checkpoint Regulator VISTA in Human Breast Cancer

Xie, X., Zhang, J., Zhongyuan, S., Liu, W., Hu, X., Qie, C., Chen, W., Wang, Y., Wang, L. L., Jiang, J., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.563044 · Cited by 57

TIM-3 as a Prognostic Marker and a Potential Immunotherapy Target in Human Malignant Tumors: A Meta-Analysis and Bioinformatics Validation

Zang, K., Hui, L., Wang, M., Huang, Y., Zhu, X., & Yao, B. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.579351 · Cited by 53

AdvanTIG-105: a phase I dose escalation study of the anti-TIGIT monoclonal antibody ociperlimab in combination with tislelizumab in patients with advanced solid tumors

Frentzas, S., Kao, S., Gao, R., Zheng, H. W., Rizwan, A., Budha, N. R., Pedroza, L. D. L. H., Tan, W., & Meniawy, T. M. (2023) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2022-005829 · Cited by 53

VISTA Targeting of T-cell Quiescence and Myeloid Suppression Overcomes Adaptive Resistance

Schaafsma, E., Croteau, W., ElTanbouly, M. A., Nowak, E. C., Smits, N. C., Deng, J., Sarde, A., Webber, C. A., Rabadi, D., Cheng, C., et al. (2022) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-22-0116 · Cited by 52

New emerging targets in cancer immunotherapy: the role of VISTA

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Preclinical development of an mRNA-based multiepitope immunotherapeutic for glioblastoma

Lutz, J., Feist, R. K., Sonntag, T., Peguero-Sánchez, E., Wolter, K., Bick, R., Bauer, J., Walz, J. S., & Heidenreich, R. (2025) · Cancer Immunology, Immunotherapy · doi:10.1007/s00262-025-04178-x · Cited by 9

P3.04-15 IDO and Tim3 Gene Expression is Correlated in NSCLC Patients with Low PDL1 Gene Expression

Szeto, C. W., Parulkar, R., Lee, J., et al. (2018) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2018.08.1722

SY03-4 TIGIT blockade therapy from basic insights to clinics

Zarour, H. M. (2023) · Annals of Oncology · doi:10.1016/j.annonc.2023.09.038

TIGIT and CD 96: new checkpoint receptor targets for cancer immunotherapy

Dougall, W. C., Kurtuluş, S., Smyth, M. J., & Anderson, A. C. (2017) · Immunological Reviews · doi:10.1111/imr.12518 · Cited by 432

γδ T cells as unconventional targets of checkpoint blockade

Widlund, H. R., & Lynch, L. (2024) · Nature Cancer · doi:10.1038/s43018-024-00735-y · Cited by 1

Immune checkpoint expression on peripheral lymphocytes in cervical cancer patients: moving beyond the PD-1/PD-L1 axisPreprint

Ibarra, F. S., lez, A. A. G., Ortiz‐Lazareno, P. C., et al. (2020) · doi:10.22541/au.158878854.41125156