Blockade of checkpoint receptor PVRIG unleashes anti-tumor immunity of NK cells in murine and human solid tumors
Open accessAbstract
Background: Although checkpoint-based immunotherapy has shown exciting results in the treatment of tumors, around 70% of patients have experienced unresponsiveness. PVRIG is a recently identified immune checkpoint receptor and blockade of which could reverse T cell exhaustion to treat murine tumor; however, its therapeutic potential via NK cells in mice and human remains seldom reported. Methods: In this study, we used patient paraffin-embedded colon adenocarcinoma sections, various murine tumor models (MC38 colon cancer, MCA205 fibrosarcoma and LLC lung cancer), and human NK cell- or PBMC-reconstituted xenograft models (SW620 colon cancer) to investigate the effect of PVRIG on tumor progression. Results: We found that PVRIG was highly expressed on tumor-infiltrating NK cells with exhausted phenotype. Furthermore, either PVRIG deficiency, early blockade or late blockade of PVRIG slowed tumor growth and prolonged survival of tumor-bearing mice by inhibiting exhaustion of NK cells as well as CD8+ T cells. Combined blockade of PVRIG and PD-L1 showed better effect in controlling tumor growth than using either one alone. Depletion of NK or/and CD8+ T cells in vivo showed that both cell types contributed to the anti-tumor efficacy of PVRIG blockade. By using Rag1−/− mice, we demonstrated that PVRIG blockade could provide therapeutic effect in the absence of adaptive immunity. Further, blockade of human PVRIG with monoclonal antibody enhanced human NK cell function and inhibited human tumor growth in NK cell- or PBMC-reconstituted xenograft mice. Conclusions: Our results reveal the importance of NK cells and provide novel knowledge for clinical application of PVRIG-targeted drugs in future.
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Other ICIs such as α-LAG-3, α-PVRIG, α-TIGIT, α-Siglec-10 also synergized with α-PD-1/PD-L1 in enhancing TIL function and suppressing tumor growth.
“Besides α-TIM-3, other ICIs such as α-LAG-3, α-PVRIG, α-TIGIT, α- Siglec-10 also synergized with α-PD-1/PD-L1 in enhancing TIL function and suppressing tumor growth [161–164].”
From Combination strategies with PD-1/PD-L1 blockade: current advances and future directions (2022) · cites this paper as [162]
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PD-1 Blockade in Tumors with Mismatch-Repair Deficiency
Le, D. T., Uram, J. N., Wang, H., Bartlett, B. R., Kemberling, H., Eyring, A. D., Skora, A. D., Luber, B. S., Azad, N. S., Laheru, D., et al. (2015) · New England Journal of Medicine · doi:10.1056/nejmoa1500596 · Cited by 9,377 · see citing works
Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer
Borghaei, H., Paz-Ares, L., Horn, L., Spigel, D. R., Steins, M., Ready, N. E., Chow, L. Q., Vokes, E. E., Felip, E., Holgado, E., et al. (2015) · New England Journal of Medicine · doi:10.1056/nejmoa1507643 · Cited by 9,335 · see citing works
Overall Survival with Combined Nivolumab and Ipilimumab in Advanced Melanoma
Wolchok, J. D., Chiarion-Sileni, V., Gonzalez, R., Rutkowski, P., Grob, J.-J., Cowey, C. L., Lao, C. D., Wagstaff, J., Schadendorf, D., Ferrucci, P. F., et al. (2017) · New England Journal of Medicine · doi:10.1056/nejmoa1709684 · Cited by 5,357 · see citing works
Nivolumab for Recurrent Squamous-Cell Carcinoma of the Head and Neck
Ferris, R. L., Blumenschein, G., Fayette, J., Guigay, J., Colevas, A. D., Licitra, L., Harrington, K., Kasper, S., Vokes, E. E., Even, C., et al. (2016) · New England Journal of Medicine · doi:10.1056/nejmoa1602252 · Cited by 5,101 · see citing works
PD-1 Blockade with Nivolumab in Relapsed or Refractory Hodgkin's Lymphoma
Ansell, S. M., Lesokhin, A. M., Borrello, I., Halwani, A. S., Scott, E. C., Gutierrez, M. E., Schuster, S. J., Millenson, M. M., Cattry, D., Freeman, G. J., et al. (2014) · New England Journal of Medicine · doi:10.1056/nejmoa1411087 · Cited by 3,564 · see citing works
Pembrolizumab as Second-Line Therapy for Advanced Urothelial Carcinoma
Bellmunt, J., de Wit, R., Vaughn, D. J., Fradet, Y., Lee, J.-L., Fong, L., Vogelzang, N. J., Climent, M. A., Petrylak, D. P., Choueiri, T. K., et al. (2017) · New England Journal of Medicine · doi:10.1056/nejmoa1613683 · Cited by 3,395 · see citing works
Immune Checkpoint Blockade in Cancer Therapy
Postow, M. A., Callahan, M. K., & Wolchok, J. D. (2015) · Journal of Clinical Oncology · doi:10.1200/jco.2014.59.4358 · Cited by 2,736 · see citing works
Yu, X., Harden, K., Gonzalez, L. C., Francesco, M. R., Chiang, E. Y., Irving, B. A., Tom, I., Ivelja, S., Refino, C. J., Clark, H. F., et al. (2008) · Nature Immunology · doi:10.1038/ni.1674 · Cited by 1,486 · see citing works
Prolonged Survival in Stage III Melanoma with Ipilimumab Adjuvant Therapy
Eggermont, A. M. M., Chiarion‐Sileni, V., Grob, J., Dummer, R., Wolchok, J. D., Schmidt, H., Hamid, O., Robert, C., Ascierto, P. A., Richards, J. M., et al. (2016) · New England Journal of Medicine · doi:10.1056/nejmoa1611299 · Cited by 1,319 · see citing works
PD-1 Blockade with pembrolizumab in advanced Merkel-cell carcinoma
Nghiem, P. T., Bhatia, S., Lipson, E. J., Kudchadkar, R. R., Miller, N. J., Annamalai, L., Berry, S., Chartash, E. K., Daud, A., Fling, S. P., et al. (2016) · New England Journal of Medicine · doi:10.1056/nejmoa1603702 · Cited by 1,258 · see citing works
The Immunoreceptor TIGIT Regulates Antitumor and Antiviral CD8 + T Cell Effector Function
Johnston, R. J., Comps‐Agrar, L., Hackney, J. A., Yu, X., Huseni, M. A., Yang, Y., Park, S., Javinal, V., Chiu, H. H., Irving, B. A., et al. (2014) · Cancer Cell · doi:10.1016/j.ccell.2014.10.018 · Cited by 1,191 · see citing works
Zhang, Q., Bi, J., Zheng, X., Chen, Y., Wang, H., Wu, W., Wang, Z., Wu, Q., Peng, H. C., Wei, H., et al. (2018) · Nature Immunology · doi:10.1038/s41590-018-0132-0 · Cited by 1,122 · see citing works
Self-citationPitt, J. M., Vétizou, M., Daillère, R., Roberti, M. P., Yamazaki, T., Routy, B., Lepage, P., Boneca, I. G., Chamaillard, M., Kroemer, G., et al. (2016) · Immunity · doi:10.1016/j.immuni.2016.06.001 · Cited by 1,040 · see citing works
Hudson, W. H., Gensheimer, J., Hashimoto, M., Wieland, A., Valanparambil, R. M., Li, P., Lin, J.-X., Konieczny, B. T., Im, S. J., Freeman, G. J., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.11.002 · Cited by 656 · see citing works
Human NK cells: surface receptors, inhibitory checkpoints, and translational applications
Sivori, S., Vacca, P., Zotto, G. D., Munari, E., Mingari, M. C., & Moretta, L. (2019) · Cellular and Molecular Immunology · doi:10.1038/s41423-019-0206-4 · Cited by 557 · see citing works
The receptors CD96 and CD226 oppose each other in the regulation of natural killer cell functions
Chan, C. J., Martinet, L., Gilfillan, S., Souza-Fonseca-Guimarães, F., Chow, M. T., Town, L., Ritchie, D. S., Colonna, M., Andrews, D. M., & Smyth, M. J. (2014) · Nature Immunology · doi:10.1038/ni.2850 · Cited by 488 · see citing works
Balancing natural killer cell activation through paired receptors
Martinet, L., & Smyth, M. J. (2015) · Nature reviews. Immunology · doi:10.1038/nri3799 · Cited by 483 · see citing works
TIGIT: A Key Inhibitor of the Cancer Immunity Cycle
Manieri, N. A., Chiang, E. Y., & Grogan, J. L. (2016) · Trends in Immunology · doi:10.1016/j.it.2016.10.002 · Cited by 414 · see citing works
Nectins and nectin‐like molecules: Roles in cell adhesion, migration, and polarization
Takai, Y., Irie, K., Shimizu, K., Sakisaka, T., & Ikeda, W. (2003) · Cancer Science · doi:10.1111/j.1349-7006.2003.tb01499.x · Cited by 375 · see citing works
Bi, J., & Tian, Z. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00760 · Cited by 327 · see citing works
Self-citationSun, H., Huang, Q., Huang, M., Wen, H., Lin, R., Zheng, M., Qu, K., Li, K., Wei, H., Xiao, W., et al. (2018) · Hepatology · doi:10.1002/hep.30347 · Cited by 302 · see citing works
Self-citationKong, Y., Zhu, L., Schell, T. D., Zhang, J., Claxton, D. F., Ehmann, W. C., Rybka, W. B., George, M. R., Zeng, H., & Zheng, H. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-15-2626 · Cited by 300 · see citing works
Accelerated tumor growth in mice deficient in DNAM-1 receptor
Iguchi‐Manaka, A., Kai, H., Yamashita, Y., Shibata, K., Tahara‐Hanaoka, S., Honda, S.-I., Yasui, T., Kikutani, H., Shibuya, K., & Shibuya, A. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20081611 · Cited by 289 · see citing works
Suppression of Metastases Using a New Lymphocyte Checkpoint Target for Cancer Immunotherapy
Blake, S. J., Stannard, K. A., Liu, J., Allen, S. M., Yong, M. C. R., Mittal, D., Aguilera, A. R., Miles, J. J., Lutzky, V. P., de Andrade, L. F., et al. (2016) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-0944 · Cited by 242 · see citing works
Targeting natural killer cells in solid tumors
Habif, G., Crinier, A., André, P., Vivier, É., & Narni-Mancinelli, É. (2019) · Cellular and Molecular Immunology · doi:10.1038/s41423-019-0224-2 · Cited by 242 · see citing works
Identification of CD112R as a novel checkpoint for human T cells
Zhu, Y., Paniccia, A., Schulick, A. C., Chen, W., Koenig, M. R., Byers, J. T., Yao, S., Bevers, S. G., & Edil, B. H. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20150785 · Cited by 210 · see citing works
Sánchez-Correa, B., Valhondo, I., Hassouneh, F., López-Sejas, N., Pera, A., Bergua, J., Arcos, M. J., Bañas, H., Casas-Avilés, I., Durán, E., et al. (2019) · Cancers · doi:10.3390/cancers11060877 · Cited by 210 · see citing works
CD226 opposes TIGIT to disrupt Tregs in melanoma.
Fourcade, J., Sun, Z.-J., Chauvin, J.-M., Ka, M., Davar, D., Pagliano, O., Wang, H., Saada, S., Menna, C., Amin, R., et al. (2018) · JCI Insight · doi:10.1172/jci.insight.121157 · Cited by 180 · see citing works
Minnie, S. A., Kuns, R. D., Gartlan, K. H., Zhang, P., Wilkinson, A., Samson, L. D., Guillerey, C., Engwerda, C. R., MacDonald, K. P. A., Smyth, M. J., et al. (2018) · Blood · doi:10.1182/blood-2018-01-825240 · Cited by 169 · see citing works
Targeting PVR (CD155) and its receptors in anti-tumor therapy
Brlić, P. K., Roviš, T. L., Cinamon, G., Tsukerman, P., Mandelboim, O., & Jonjić, S. (2018) · Cellular and Molecular Immunology · doi:10.1038/s41423-018-0168-y · Cited by 169 · see citing works
Cancer immunologists scoop medicine Nobel prize
Ledford, H. K., Else, H., & Warren, M. (2018) · Nature · doi:10.1038/d41586-018-06751-0 · Cited by 158 · see citing works
Blockade of CD112R and TIGIT signaling sensitizes human natural killer cell functions
Xu, F., Sunderland, A., Zhou, Y., Schulick, R. D., Edil, B. H., & Zhu, Y. (2017) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-017-2031-x · Cited by 152 · see citing works
PVRIG and PVRL2 Are Induced in Cancer and Inhibit CD8+ T-cell Function
Whelan, S., Ophir, E., Kotturi, M. F., Levy, O., Ganguly, S., Leung, L., Vaknin, I., Kumar, S., Dassa, L., Hansen, K., et al. (2019) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-18-0442 · Cited by 149 · see citing works
Tumor rejection by the poliovirus receptor family ligands of the DNAM-1 (CD226) receptor
Tahara‐Hanaoka, S., Shibuya, K., Kai, H., Miyamoto, A., Morikawa, Y., Ohkochi, N., Honda, S.-I., & Shibuya, A. (2005) · Blood · doi:10.1182/blood-2005-04-1684 · Cited by 148 · see citing works
Tumor intrinsic and extrinsic immune functions of CD155
O’Donnell, J. S., Madore, J., Li, X.-Y., & Smyth, M. J. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.11.013 · Cited by 136 · see citing works
CD96 Is an Immune Checkpoint That Regulates CD8+ T-cell Antitumor Function
Mittal, D., Lepletier, A., Madore, J., Aguilera, A. R., Stannard, K. A., Blake, S. J., Whitehall, V., Liu, C., Bettington, M. L., Takeda, K., et al. (2019) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-18-0637 · Cited by 119 · see citing works
Pauken, K. E., & Wherry, E. J. (2014) · Cancer Cell · doi:10.1016/j.ccell.2014.11.016 · Cited by 111 · see citing works
Nectin-2 is a potential target for antibody therapy of breast and ovarian cancers
Oshima, T., Sato, S., Kato, J., Ito, Y., Watanabe, T., Tsuji, I., Hori, A., Kurokawa, T., & Kokubo, T. (2013) · Molecular Cancer · doi:10.1186/1476-4598-12-60 · Cited by 109 · see citing works
Targeting innate sensing in the tumor microenvironment to improve immunotherapy
Liu, Z., Han, C., & Fu, Y. (2019) · Cellular and Molecular Immunology · doi:10.1038/s41423-019-0341-y · Cited by 102 · see citing works
Miao, X., Yang, Z., Li, X., Zou, Q., Yuan, Y., Li, J., Liang, L., Chen, M., & Chen, S. (2013) · PubMed Central · Cited by 79 · see citing works
Mouse PVRIG Has CD8+ T Cell–Specific Coinhibitory Functions and Dampens Antitumor Immunity
Murter, B., Pan, X., Ophir, E., Alteber, Z., Azulay, M., Sen, R., Levy, O., Dassa, L., Vaknin, I., Kfir, T. F., et al. (2019) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-18-0460 · Cited by 55 · see citing works
Therapeutic Targeting of Checkpoint Receptors within the DNAM1 Axis
Alteber, Z., Kotturi, M. F., Whelan, S., Ganguly, S., Weyl, E., Pardoll, D. M., Hunter, J., & Ophir, E. (2021) · Cancer Discovery · doi:10.1158/2159-8290.cd-20-1248 · Cited by 48 · see citing works
Cheng, M., Ma, J., Chen, Y., Zhang, J., Zhao, W., Zhang, J., Wei, H., Ling, B., Sun, R., & Tian, Z. (2011) · Cell Transplantation · doi:10.3727/096368911x580536 · Cited by 47 · see citing works
Self-citationPVRIG is a novel natural killer cell immune checkpoint receptor in acute myeloid leukemia
Li, J., Whelan, S., Kotturi, M. F., Meyran, D., D’Souza, C., Hansen, K., Liang, S. C., Hunter, J., Trapani, J. A., & Neeson, P. J. (2020) · Haematologica · doi:10.3324/haematol.2020.258574 · Cited by 34 · see citing works
Blocking PD-L1 for anti-liver cancer immunity: USP22 represents a critical cotarget
Huang, X., Zhang, X., Bai, X., & Liang, T. (2019) · Cellular and Molecular Immunology · doi:10.1038/s41423-019-0348-4 · Cited by 22 · see citing works
Sullivan, R. J., Rasco, D. W., Lim, E. A., Sharma, M. R., Shepard, D. R., Patnaik, A., Hamilton, E. P., Fleming, G. F., Papadopoulos, K. P., ElNaggar, A. C., et al. (2020) · Cancer Research · doi:10.1158/1538-7445.am2020-ct031 · Cited by 8 · see citing works
(2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-nb2020-028 · Cited by 2 · see citing works
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Self-citationYan, Y., Huang, L., Liu, Y., Yi, M., Chu, Q., Jiao, D., & Wu, K. (2022) · Journal of Hematology & Oncology · doi:10.1186/s13045-022-01322-3 · Cited by 222 · see citing works
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Borgeaud, M., Sandoval, J. L., Obéid, M., Banna, G. L., Michielin, O. A., Addeo, A., & Friedlaender, A. (2023) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2023.102614 · Cited by 147 · see citing works
Overcoming cold tumors: a combination strategy of immune checkpoint inhibitors
Ouyang, P., Wang, L., Wu, J., Tian, Y., Chen, C., Li, D., Yao, Z., Chen, R., Xiang, G., Gong, J., et al. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1344272 · Cited by 118 · see citing works
Targeting TIGIT for cancer immunotherapy: recent advances and future directions
Zhang, P., Liu, X., Gu, Z., Jiang, Z., Zhao, S. Q., Song, Y., & Yu, J. (2024) · Biomarker Research · doi:10.1186/s40364-023-00543-z · Cited by 100 · see citing works
Blockade of novel immune checkpoints and new therapeutic combinations to boost antitumor immunity
Archilla‐Ortega, A., Domuro, C., Martín-Liberal, J., & Muñoz, P. (2022) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-022-02264-x · Cited by 79 · see citing works
Inhibitory Receptors and Immune Checkpoints Regulating Natural Killer Cell Responses to Cancer
Buckle, I., & Guillerey, C. (2021) · Cancers · doi:10.3390/cancers13174263 · Cited by 71 · see citing works
The CD112R/CD112 axis: a breakthrough in cancer immunotherapy
Zeng, T., Cao, Y., Jin, T., Tian, Y., Dai, C., & Xu, F. (2021) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-021-02053-y · Cited by 69 · see citing works
Yin, N., Li, X., Zhang, X., Xue, S., Cao, Y., Niedermann, G., Lu, Y., & Xue, J. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01826-z · Cited by 66 · see citing works
Li, Y., Zhu, L., Tang, Y., Zhuang, X., Feng, W., Boor, P. P. C., Buschow, S. I., Sprengers, D., & Zhou, G. (2024) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2024-009934 · Cited by 62 · see citing works
Self-citationCombined Blockade of TIGIT and CD39 or A2AR Enhances NK-92 Cell-Mediated Cytotoxicity in AML
Brauneck, F., Seubert, E., Wellbrock, J., Wiesch, J. S. Z., Duan, Y., Magnus, T. U., Bokemeyer, C., Koch‐Nolte, F., Menzel, S., & Fiedler, W. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222312919 · Cited by 50 · see citing works
Natural Killer Cell Immune Checkpoints and Their Therapeutic Targeting in Cancer Treatment
Lin, A., Ye, P., Li, Z., Jiang, A., Liu, Z., Cheng, Q., Zhang, J., & Luo, P. (2025) · Research · doi:10.34133/research.0723 · Cited by 44 · see citing works
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Akbulut, Z., Aru, B., Aydın, F., & Demirel, G. Y. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1379622 · Cited by 39 · see citing works
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Wang, J., Ding, K., Wang, Y., Yan, T., Xu, Y., Deng, Z., Lin, W., Zhang, L., Zhu, W., Zhao, R., et al. (2022) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2022/4061713 · Cited by 34 · see citing works
Yu, S., Lin, Y., Li, Y., Chen, S., Zhou, L., Song, H., Yang, C., Zhang, H., Zhou, J., Sun, S.-C., et al. (2023) · Cell · doi:10.1016/j.cell.2023.08.033 · Cited by 34 · see citing works
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Wang, L., Chen, Z., Liu, G., & Pan, Y. (2022) · Genes & Diseases · doi:10.1016/j.gendis.2022.07.009 · Cited by 24 · see citing works
The regulating role of galectin-9 in immune cell populations
Cao, Z., Leng, P., Xu, H., & Li, X. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1462061 · Cited by 20 · see citing works
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Yang, J., Wang, L., Byrnes, J. R., Kirkemo, L. L., Driks, H., Belair, C. D., Aguilar, O. A., Lanier, L. L., Wells, J. A., Fong, L. H., et al. (2024) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-23-0722 · Cited by 12 · see citing works
Yang, C. H., Mandelkow, T., Bady, E., Raedler, J. B., Simon, R., Sauter, G., Lennartz, M., Büscheck, F., Luebke, A. M., Dum, D., et al. (2023) · Modern Pathology · doi:10.1016/j.modpat.2022.100089 · Cited by 12 · see citing works
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Huang, H., Lv, X., Chen, Q., & Dong, L. (2025) · Clinics · doi:10.1016/j.clinsp.2025.100662 · Cited by 6 · see citing works
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Zhang, Z., Zhang, Y., Chen, Y., Cao, G., Zheng, X., Sun, R., Peng, H., Tian, Z., & Sun, H. (2025) · Acta Pharmacologica Sinica · doi:10.1038/s41401-025-01556-0 · Cited by 4 · see citing works
Self-citationCD155 density on target cells drives divergent natural killer cell responses owing to DNAM-1 loss
Saunders, P. M., Oates, C. V. L., Hare, R. K., Burgess, M., Vargas-Pavía, T. A., Worboys, J. D., Davis, D. M., & Brööks, A. G. (2025) · The Journal of Immunology · doi:10.1093/jimmun/vkaf293 · Cited by 4 · see citing works
Xue, H., Zhang, Z., Li, L., Zhu, C., Fei, K., Sha, H., Wu, Z., Lin, X., Wang, F., Zhou, S., et al. (2024) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-024-03671-z · Cited by 4 · see citing works
Self-citationBirnbaum, D. J., Picard, M., Costa, Q. D., Delayre, T., Finetti, P., Cabaud, O., Agavnian, E., de Rauglaudre, B., Denicolaï, E., Bertucci, F., et al. (2023) · Cancers · doi:10.3390/cancers15020447 · Cited by 4 · see citing works
Natural killer cell‐based signature: Prognostic analysis in head and neck squamous cell carcinoma
Guo, Z., Zhao, Y., Xu, M., Zhao, L., & Wang, X. (2024) · The Journal of Gene Medicine · doi:10.1002/jgm.3671 · Cited by 3 · see citing works
Application of spatial omics in gastric cancer
Zhu, E., Xie, Q., Huang, X., & Zhang, Z. (2024) · Pathology - Research and Practice · doi:10.1016/j.prp.2024.155503 · Cited by 3 · see citing works
Brauneck, E., Leonhardt, L.-G., Assemissen, A. M., Wahid, Y., Kruppa, M., Kruppa, N., Krüger, J., Menzel, S., Koch‐Nolte, F., Kylies, J., et al. (2025) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-025-04030-2 · Cited by 2 · see citing works
Li, N., Luo, C., Chen, Y., Cheng, X., Luo, J., Yan, Y., Zhang, Y., Lu, B., He, Z., Song, K., et al. (2025) · Chinese Medical Journal · doi:10.1097/cm9.0000000000003681 · Cited by 1 · see citing works
Self-citationChen, P., Pan, J., Chen, L., & Feng, X. (2025) · Frontiers in Oncology · doi:10.3389/fonc.2025.1670033 · Cited by 1 · see citing works
Jiang, W., & Chen, S. (2026) · Annals of Surgical Oncology · doi:10.1245/s10434-026-19339-0 · Cited by 1 · see citing works
Izuegbuna, O. (2024) · Oncology Advances · doi:10.14218/ona.2024.00013 · Cited by 1 · see citing works
Shen, X., Shang, L., Han, J., Zhang, Y., Niu, W., Liu, H., & Shi, H. N. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e39260 · Cited by 1 · see citing works
Self-citationA GLOBAL CONGRESS DIGEST ON SOLID TUMORS. Report from the ASCO Virtual Congress, 4th –8th June 2021
(2021) · memo - Magazine of European Medical Oncology · doi:10.1007/s12254-021-00754-w
Ma, P., Zhang, R., & Sun, W. (2025) · Scientific Reports · doi:10.1038/s41598-025-89308-2
Archilla‐Ortega, A., Domuro, C., Martín-Liberal, J., & Muñoz, P. (2022) · Figshare · doi:10.6084/m9.figshare.19174069
Zhang, X., Li, S., Luo, S., Liu, X., Ao, Y., Zhong, L., Luo, K., & Hu, Y. (2026) · BMC Pulmonary Medicine · doi:10.1186/s12890-026-04244-9
- Authors
- Li, Y., Zhang, Y., Cao, G., Zheng, X., Sun, C., Wei, H., Tian, Z., Xiao, W., Sun, R., & Sun, H.
- Affiliations
- University of Science and Technology of China (CN)
- Corresponding author
- Sun, Rui
- Sun, Haoyu
- ORCID
- Venue
- Journal of Hematology & Oncology
- Published
- 2021-06-26
- Volume
- 14
- Issue
- 1
- Pages
- 100-100
- ISSN
- 1756-8722 (ISSN-L)
- PMC
- PMC8236157
- OpenAlex
- W3175390778
- Cited by
- 51
- References
- 47
- Citations by year
- 2026: 3 · 2025: 9 · 2024: 17 · 2023: 10 · 2022: 8 · 2021: 4
- FWCI
- 3.63
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Journal of Hematology & Oncology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Key R&D Program of China (2019YFA0508502/3)
- National Natural Science Foundation of China (81788101, 82071766, 81972679, 81821001)
- CAMS Innovation Fund for Medical Sciences (2019-I2M-5-073)
- Chinese Academy of Sciences (XDB29030201)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune Cell Function and Interaction
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- PVRIG, immune checkpoint blockade, natural killer cells, NK cell exhaustion, CD8+ T cell exhaustion, antitumor immunity, PD-L1, colon adenocarcinoma, fibrosarcoma, lung cancer, tumor-infiltrating lymphocytes, tumor growth inhibition
- MeSH terms
- Antineoplastic Agents, Immunological, Immune Checkpoint Inhibitors, Animals, Humans, Immunotherapy, Killer Cells, Natural, Mice, Inbred C57BL, Neoplasms, Receptors, Cell Surface, Cell Line, Tumor, Mice
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