NCRs and DNAM-1 mediate NK cell recognition and lysis of human and mouse melanoma cell lines in vitro and in vivo
Open accessAbstract
NK cells use a variety of receptors to detect abnormal cells, including tumors and their metastases. However, in the case of melanoma, it remains to be determined what specific molecular interactions are involved and whether NK cells control metastatic progression and/or the route of dissemination. Here we show that human melanoma cell lines derived from LN metastases express ligands for natural cytotoxicity receptors (NCRs) and DNAX accessory molecule-1 (DNAM-1), two emerging NK cell receptors key for cancer cell recognition, but not NK group 2 member D (NKG2D). Compared with cell lines derived from metastases taken from other anatomical sites, LN metastases were more susceptible to NK cell lysis and preferentially targeted by adoptively transferred NK cells in a xenogeneic model of cell therapy. In mice, DNAM-1 and NCR ligands were also found on spontaneous melanomas and melanoma cell lines. Interference with DNAM-1 and NCRs by antibody blockade or genetic disruption reduced killing of melanoma cells. Taken together, these results show that DNAM-1 and NCRs are critical for NK cell-mediated innate immunity to melanoma cells and provide a background to design NK cell-based immunotherapeutic strategies against melanoma and possibly other tumors.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
NKp30, NKp46, and DNAM-1 are NK activation receptors involved in the recognition and lysis of different tumors, such as hematological malignancies, melanoma, and ovarian cancer.
“Moreover, NKp30, NKp46, and DNAM-1 are NK activation receptors involved in the recognition and lysis of different tumors, such as hematological malignancies [82], melanoma [83], and ovarian cancer [84].”
From Immunosenescence: a key player in cancer development (2020) · cites this paper as [83]
Cites
Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants
Ruggeri, L., Capanni, M., Urbani, E., Perruccio, K., Shlomchik, W. D., Tosti, A., Posati, S., Rogaia, D., Frassoni, F., Aversa, F., et al. (2002) · Science · doi:10.1126/science.1068440 · Cited by 3,380 · see citing works
Self-citationBiology of Natural Killer Cells
Trinchieri, G. (1989) · Advances in Immunology · doi:10.1016/s0065-2776(08)60664-1 · Cited by 2,902 · see citing works
IFNγ and lymphocytes prevent primary tumour development and shape tumour immunogenicity
Shankaran, V., Ikeda, H., Bruce, A. T., White, J. M., Swanson, P. E., Old, L. J., & Schreiber, R. D. (2001) · Nature · doi:10.1038/35074122 · Cited by 2,896 · see citing works
Lanier, L. L. (2004) · Annual Review of Immunology · doi:10.1146/annurev.immunol.23.021704.115526 · Cited by 2,765 · see citing works
Swann, J. B., & Smyth, M. J. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31405 · Cited by 1,469 · see citing works
Induced recruitment of NK cells to lymph nodes provides IFN-γ for TH1 priming
Martin‐Fontecha, A., Thomsen, L. L., Brett, S. J., Gerard, C. J., Lipp, M., Lanzavecchia, A., & Sallusto, F. (2004) · Nature Immunology · doi:10.1038/ni1138 · Cited by 1,351 · see citing works
Bottino, C., Castriconi, R., Pende, D., Rivera, P., Nanni, M., Carnemolla, B., Cantoni, C., Grassi, J., Marcenaro, S., Reymond, N., et al. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20030788 · Cited by 874 · see citing works
Self-citationBryceson, Y. T., March, M., Ljunggren, H., & Long, E. O. (2005) · Blood · doi:10.1182/blood-2005-04-1351 · Cited by 863 · see citing works
Fehniger, T. A., Cooper, M. A., Nuovo, G. J., Cella, M., Facchetti, F., Colonna, M., & Caligiuri, M. A. (2003) · Blood · doi:10.1182/blood-2002-09-2876 · Cited by 850 · see citing works
New aspects of natural-killer-cell surveillance and therapy of cancer
Smyth, M. J., Hayakawa, Y., Takeda, K., & Yagita∥, H. (2002) · Nature reviews. Cancer · doi:10.1038/nrc928 · Cited by 750 · see citing works
HUMAN T CELL RESPONSES AGAINST MELANOMA
Boon, T., Coulie, P. G., den Eynde, B. J. V., & van der Bruggen, P. (2005) · Annual Review of Immunology · doi:10.1146/annurev.immunol.24.021605.090733 · Cited by 651 · see citing works
Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1
Gazit, R., Gruda, R., Elboim, M., Arnon, T. I., Katz, G., Achdout, H., Hanna, J. H., Qimron, U., Landau, G., Greenbaum, E., et al. (2006) · Nature Immunology · doi:10.1038/ni1322 · Cited by 549 · see citing works
In vivo natural killer cell activities revealed by natural killer cell-deficient mice
Kim, S., Iizuka, K., Aguila, H. L., Weissman, I. L., & Yokoyama, W. M. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.050588297 · Cited by 419 · see citing works
A Human CD34(+) Subset Resides in Lymph Nodes and Differentiates into CD56brightNatural Killer Cells
Freud, A. G., Becknell, B., Roychowdhury, S., Mao, H. C., Ferketich, A. K., Nuovo, G. J., Hughes, T. L., Marburger, T. B., Sung, J., Baiocchi, R. A., et al. (2005) · Immunity · doi:10.1016/j.immuni.2005.01.013 · Cited by 399 · see citing works
Gilfillan, S., Chan, C. J., Cella, M., Haynes, N. M., Rapaport, A. S., Boles, K. S., Andrews, D. M., Smyth, M. J., & Colonna, M. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20081752 · Cited by 361 · see citing works
El-Sherbiny, Y. M., Meade, J. L., Holmes, T. D., McGonagle, D. G., Mackie, S. L., Morgan, A. W., Cook, G., Feyler, S., Richards, S. J., Davies, F. E., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-4230 · Cited by 320 · see citing works
The role of natural killer cells in innate resistance to infection
Bancroft, G. J. (1993) · Current Opinion in Immunology · doi:10.1016/0952-7915(93)90030-v · Cited by 320 · see citing works
The Anti-Tumor Activity of IL-12: Mechanisms of Innate Immunity That Are Model and Dose Dependent
Smyth, M. J., Taniguchi, M., & Street, S. E. A. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.165.5.2665 · Cited by 303 · see citing works
The genetics of malignant melanoma: lessons from mouse and man
Chin, L. (2003) · Nature reviews. Cancer · doi:10.1038/nrc1145 · 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
Self-citationNatural Killer Cell-Mediated Killing of Freshly Isolated Neuroblastoma Cells
Castriconi, R., Dondero, A., Corrias, M. V., Lanino, E., Pende, D., Moretta, L., Bottino, C., & Moretta, A. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-2682 · Cited by 257 · see citing works
Self-citationCarlsten, M., Björkström, N. K., Norell, H., Bryceson, Y., van Hall, T., Baumann, B. C., Hanson, M., Schedvins, K., Kiessling, R., Ljunggren, H.-G., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-2264 · Cited by 234 · see citing works
Transgenic mouse model for skin malignant melanoma
Kato, M., Takahashi, M., Akhand, A. A., Liu, W., Dai, Y. M., Shimizu, S., Iwamoto, T., Suzuki, H., & Nakashima, I. (1998) · Oncogene · doi:10.1038/sj.onc.1202077 · Cited by 220 · see citing works
Self-citationNatural killer cell activation in mice and men: different triggers for similar weapons?
Colucci, F., Santo, J. P. D., & Leibson, P. J. (2002) · Nature Immunology · doi:10.1038/ni0902-807 · Cited by 206 · see citing works
Self-citationNowbakht, P., Ionescu, M.-C. S., Rohner, A., Kalberer, C. P., Rossy, E., Mori, L., Cosman, D. J., Libero, G. D., & Wodnar‐Filipowicz, A. (2005) · Blood · doi:10.1182/blood-2004-07-2585 · Cited by 194 · see citing works
Igarashi, T., Wynberg, J., Srinivasan, R., Becknell, B., McCoy, J. P., Takahashi, Y., Suffredini, D. A., Linehan, W. M., Caligiuri, M. A., & Childs, R. W. (2004) · Blood · doi:10.1182/blood-2003-12-4438 · Cited by 192 · see citing works
Lopez, M., Aoubala, M., Jordier, F., Isnardon, D., Gomez, S., & Dubreuil, P. C. (1998) · Blood · doi:10.1182/blood.v92.12.4602 · Cited by 165 · see citing works
Enhanced In Vivo Growth of Lymphoma Tumors in the Absence of the NK-Activating Receptor NKp46/NCR1
Halfteck, G. G., Elboim, M., Gur, C., Achdout, H., Ghadially, H., & Mandelboim, O. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0801878 · Cited by 162 · 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
Self-citationRepp, A. C., Mayhew, E. S., Apte, S., & Niederkorn, J. Y. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.165.2.710 · Cited by 142 · see citing works
Characterization of uveal melanoma cell lines that grow as xenografts in rabbit eyes.
Kan‐Mitchell, J., Mitchell, M. S., Rao, N. P., & Liggett, P. E. (1989) · PubMed · Cited by 132 · see citing works
HLA expression in uveal melanoma: there is no rule without some exception
Jager, M. J., Hurks, H. M. H., Levitskaya, J., & Kiessling, R. W. (2002) · Human Immunology · doi:10.1016/s0198-8859(02)00389-0 · Cited by 122 · see citing works
Ink4a/arf deficiency promotes ultraviolet radiation-induced melanomagenesis.
Recio, J. A., Noonan, F. P., Takayama, H., Anver, M. R., Duray, P. H., Rush, W. L., Lindner, G., Fabo, E. C. D., DePinho, R. A., & Merlino, G. T. (2002) · PubMed · Cited by 91 · see citing works
Chansac, B. L. M., Moretta, A., Vergnon, I., Opolon, P., Lécluse, Y., Grunenwald, D. H., Kubin, M. Z., Soria, J., Chouaı̈b, S., & Mami‐Chouaib, F. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.9.5790 · Cited by 81 · see citing works
Pathways to Melanoma Development: Lessons from the Mouse
Walker, G. J., & Hayward, N. K. (2002) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.2002.00217.x · Cited by 73 · see citing works
Spontaneous Vitiligo in an Animal Model for Human Melanoma
Lengagne, R., Gal, F. L., Garcette, M., Fiette, L., Avé, P., Kato, M., Briand, J., Massot, C., Nakashima, I., Rénia, L., et al. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-2828 · Cited by 57 · see citing works
Self-citationEstablishment of cell lines of uveal melanoma. Methodology and characteristics.
Albert, D. M., Ruzzo, M., McLaughlin, M. A., Robinson, N., Craft, J. L., & EPSTEIN, J. (1984) · PubMed · Cited by 55 · see citing works
Expression of Ligands to NKp46 in Benign and Malignant Melanocytes
Cagnano, E., Hershkovitz, O., Zilka, A., Bar-Ilan, A., Golder, A., Sion‐Vardy, N., Bogdanov‐Berezovsky, A., Mandelboim, O., Benharroch, D., & Porgador, A. (2007) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5701111 · Cited by 51 · see citing works
Paschen, A., Arens, N., Sucker, A., Greulich‐Bode, K. M., Fonsatti, E., Gloghini, A., Striegel, S., Schwinn, N., Carbone, A., Hildenbrand, R., et al. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-2174 · Cited by 36 · see citing works
Self-citationNon-fastidious, melanoma-specific CD8 + cytotoxic T lymphocytes from choroidal melanoma patients
Huang, X. Q., Mitchell, M. S., Liggett, P. E., Murphree, A. L., & Kan‐Mitchell, J. (1994) · Cancer Immunology Immunotherapy · doi:10.1007/bf01517210 · Cited by 26 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Controlling Natural Killer Cell Responses: Integration of Signals for Activation and Inhibition
Long, E. O., Kim, H. S., Liu, D., Peterson, M., & Rajagopalan, S. (2013) · Annual Review of Immunology · doi:10.1146/annurev-immunol-020711-075005 · Cited by 1,209 · see citing works
NK cells and cancer: you can teach innate cells new tricks
Morvan, M. G., & Lanier, L. L. (2015) · Nature reviews. Cancer · doi:10.1038/nrc.2015.5 · Cited by 1,159 · see citing works
Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition)
Cossarizza, A., Chang, H., Radbruch, A., Acs, A., Adam, D., Adam‐Klages, S., Agace, W. W., Aghaeepour, N., Akdiş, M., Allez, M., et al. (2019) · European Journal of Immunology · doi:10.1002/eji.201970107 · Cited by 982 · see citing works
Chauvin, J.-M., & Zarour, H. M. (2020) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2020-000957 · Cited by 808 · see citing works
Control of Metastasis by NK Cells
López‐Soto, A., Gonzalez, S. R., Smyth, M. J., & Galluzzi, L. (2017) · Cancer Cell · doi:10.1016/j.ccell.2017.06.009 · Cited by 730 · see citing works
Mamessier, É., Sylvain, A., Thibult, M., Houvenaeghel, G. F., Jacquemier, J. D., Castellano, R., Gonçalvès, A., André, P., Romagné, F., Thibault, G., et al. (2011) · Journal of Clinical Investigation · doi:10.1172/jci45816 · Cited by 682 · see citing works
Innate Immune Recognition of Cancer
Woo, S., Corrales, L. P., & Gajewski, T. F. (2015) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032414-112043 · Cited by 569 · see citing works
Guidelines for the use of flow cytometry and cell sorting in immunological studies *
Cossarizza, A., Chang, H., Radbruch, A., Akdiş, M., Andrä, I., Annunziato, F., Bächer, P., Barnaba, V., Battistini, L., Bauer, W. M., et al. (2017) · European Journal of Immunology · doi:10.1002/eji.201646632 · Cited by 572 · see citing works
Immunosenescence: a key player in cancer development
Lian, J., Yue, Y., Yu, W., & Zhang, Y. (2020) · Journal of Hematology & Oncology · doi:10.1186/s13045-020-00986-z · Cited by 510 · see citing works
Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition)
Cossarizza, A., Chang, H., Radbruch, A., Abrignani, S., Addo, R., Akdis, M., Andrä, I., Andreata, F., Annunziato, F., Arranz, E., et al. (2021) · European Journal of Immunology · doi:10.1002/eji.202170126 · Cited by 531 · 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
Effect of tumor cells and tumor microenvironment on NK‐cell function
Vitale, M., Cantoni, C., Pietra, G., Mingari, M. C., & Moretta, L. (2014) · European Journal of Immunology · doi:10.1002/eji.201344272 · Cited by 410 · see citing works
Recognition of Tumors by the Innate Immune System and Natural Killer Cells
Marcus, A., Gowen, B. G., Thompson, T. W., Iannello, A., Ardolino, M., Deng, W., Wang, L., Shifrin, N. T., & Raulet, D. H. (2014) · Advances in immunology · doi:10.1016/b978-0-12-800267-4.00003-1 · Cited by 394 · see citing works
Reprogramming of T Cells to Natural Killer–Like Cells upon <i>Bcl11b</i> Deletion
Li, P., Burke, S., Wang, J., Chen, X., Ortiz, M., Lee, S.-C., Lu, D., Campos, L., Goulding, D., Ng, B. L., et al. (2010) · Science · doi:10.1126/science.1188063 · Cited by 374 · see citing works
Self-citationThe Natural Cytotoxicity Receptors in Health and Disease
Barrow, A. D., Martin, C. J., & Colonna, M. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00909 · Cited by 370 · see citing works
Unraveling the crosstalk between melanoma and immune cells in the tumor microenvironment
Marzagalli, M., Ebelt, N. D., & Manuel, E. R. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.08.002 · Cited by 345 · see citing works
Cortez, V. S., Ulland, T. K., Cervantes‐Barragán, L., Bando, J. K., Robinette, M. L., Wang, Q., White, A. J., Gilfillan, S., Cella, M., & Colonna, M. (2017) · Nature Immunology · doi:10.1038/ni.3809 · Cited by 335 · see citing works
Melanoma-associated fibroblasts modulate NK cell phenotype and antitumor cytotoxicity
Balsamo, M., Scordamaglia, F., Pietra, G., Manzini, C., Cantoni, C., Boitano, M., Queirolo, P., Vermi, W., Facchetti, F., Moretta, A., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906481106 · Cited by 327 · see citing works
Pietra, G., Manzini, C., Rivara, S., Vitale, M., Cantoni, C., Petretto, A., Balsamo, M., Conte, R., Benelli, R., Minghelli, S., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-2544 · Cited by 321 · see citing works
Activating natural cytotoxicity receptors of natural killer cells in cancer and infection
Koch, J., Steinle, A., Watzl, C., & Mandelboim, O. (2013) · Trends in Immunology · doi:10.1016/j.it.2013.01.003 · Cited by 314 · see citing works
Balsamo, M., Manzini, C., Pietra, G., Raggi, F., Blengio, F., Mingari, M. C., Varesio, L., Moretta, L., Bosco, M. C., & Vitale, M. (2013) · European Journal of Immunology · doi:10.1002/eji.201343448 · Cited by 284 · see citing works
Sun, X., Wu, Y., Gao, W., Enjyoji, K., Csizmadia, E., Müller, C. E., Murakami, T., & Robson, S. C. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.05.007 · Cited by 279 · see citing works
Immune system and melanoma biology: a balance between immunosurveillance and immune escape
Passarelli, A. M., Mannavola, F., Stucci, L. S., Tucci, M., & Silvestris, F. (2017) · Oncotarget · doi:10.18632/oncotarget.22190 · Cited by 271 · see citing works
Tallerico, R., Todaro, M., Franco, S. D., Maccalli, C., Garofalo, C., Sottile, R., Palmieri, C., Tirinato, L., Pangigadde, P., Rocca, R. L., et al. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1201542 · Cited by 251 · see citing works
Self-citationSuppression 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
Correia, D. V., Fogli, M., Hudspeth, K. L., da Silva, M. G., Mavilio, D., & Silva‐Santos, B. (2011) · Blood · doi:10.1182/blood-2011-02-339135 · Cited by 236 · see citing works
Molecular pathways: targeting CD96 and TIGIT for cancer immunotherapy
Blake, S. J., Dougall, W. C., Miles, J. J., Teng, M. W. L., & Smyth, M. J. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-0933 · Cited by 223 · see citing works
A novel Ncr1-Cre mouse reveals the essential role of STAT5 for NK-cell survival and development
Eckelhart, E., Warsch, W., Zebedin, E., Simma, O., Stoiber, D., Kolbe, T., Rülicke, T., Mueller, M., Casanova, E., & Sexl, V. (2010) · Blood · doi:10.1182/blood-2010-06-291633 · Cited by 217 · see citing works
Glasner, A., Levi, A., Enk, J., Isaacson, B., Viukov, S. V., Orlanski, S., Scope, A., Neuman, T., Enk, C. D., Hanna, J. H., et al. (2018) · Immunity · doi:10.1016/j.immuni.2017.12.007 · Cited by 221 · 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
Molecular mechanisms of natural killer cell activation in response to cellular stress
Chan, C. J., Smyth, M. J., & Martinet, L. (2013) · Cell Death and Differentiation · doi:10.1038/cdd.2013.26 · Cited by 210 · see citing works
Samanta, D., & Almo, S. C. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1763-4 · Cited by 209 · see citing works
Wennerberg, E., Kremer, V., Childs, R. W., & Lundqvist, A. (2014) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-014-1629-5 · Cited by 191 · see citing works
Spanholtz, J., Tordoir, M., Eissens, D., Preijers, F. W. M. B., van der Meer, A., Joosten, I., Schaap, N. P., de Witte, T. M., & Dolstra, H. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009221 · Cited by 188 · see citing works
Cytokine regulation of natural killer cell effector functions
Zwirner, N. W., & Domaica, C. I. (2010) · BioFactors · doi:10.1002/biof.107 · Cited by 182 · see citing works
Coles, S., Wang, E. C. Y., Man, S., Hills, R. K., Burnett, A. K., Tonks, A., & Darley, R. L. (2011) · Leukemia · doi:10.1038/leu.2011.1 · Cited by 181 · see citing works
Chan, C. J., Andrews, D. M., McLaughlin, N. M., Yagita∥, H., Gilfillan, S., Colonna, M., & Smyth, M. J. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0903225 · Cited by 181 · see citing works
Recognition and Prevention of Tumor Metastasis by the NK Receptor NKp46/NCR1
Glasner, A., Ghadially, H., Gur, C., Stanietsky, N., Tsukerman, P., Enk, J., & Mandelboim, O. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1102461 · Cited by 176 · see citing works
NKp46-Mediated Killing of Human and Mouse Hepatic Stellate Cells Attenuates Liver Fibrosis
Gur, C., Doron, S., Kfir-Erenfeld, S., Horwitz, E., Abu-tair, L., Safadi, R., & Mandelboim, O. (2012) · Gut · doi:10.1136/gutjnl-2011-301400 · Cited by 173 · see citing works
Braun, M., Aguilera, A. R., Sundarrajan, A., Corvino, D., Stannard, K. A., Krumeich, S., Das, I., Lima, L. G., Guzman, L. G. M., Li, K., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.09.010 · Cited by 171 · see citing works
Hudspeth, K. L., Silva‐Santos, B., & Mavilio, D. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00069 · Cited by 163 · see citing works
Human immunodeficiency-causing mutation defines CD16 in spontaneous NK cell cytotoxicity
Grier, J. T., Forbes, L. R., Monaco-Shawver, L., Oshinsky, J., Atkinson, T. P., Moody, C., Pandey, R., Campbell, K. S., & Orange, J. S. (2012) · Journal of Clinical Investigation · doi:10.1172/jci64837 · Cited by 160 · see citing works
Fukui, A., Funamizu, A., Yokota, M., Yamada, K., Nakamua, R., Fukuhara, R., Kimura, H., & Mizunuma, H. (2011) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2011.04.006 · Cited by 159 · see citing works
Nachmani, D., Lankry, D., Wolf, D. G., & Mandelboim, O. (2010) · Nature Immunology · doi:10.1038/ni.1916 · Cited by 158 · see citing works
Bugide, S., Green, M. R., & Wajapeyee, N. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1802691115 · Cited by 158 · see citing works
Berrou, J., Fougeray, S., Venot, M., Chardiny, V., Gautier, J., Dulphy, N., Toubert, A., & Péraldi, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062418 · Cited by 157 · see citing works
IL15 Stimulation with TIGIT Blockade Reverses CD155-mediated NK-Cell Dysfunction in Melanoma
Chauvin, J.-M., Ka, M. B., Pagliano, O., Menna, C., Ding, Q., Deblasio, R. N., Sander, C., Hou, J., Li, X.-Y., Ferrone, S., et al. (2020) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-20-0575 · Cited by 156 · see citing works
Self-citationImmunosurveillance and therapy of multiple myeloma are CD226 dependent
Guillerey, C., de Andrade, L. F., Vučković, S., Miles, K. M., Ngiow, S. F., Yong, M. C. R., Teng, M. W. L., Colonna, M., Ritchie, D. S., Chesi, M., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci77181 · Cited by 151 · see citing works
The Tumor Microenvironment: A Pitch for Multiple Players
Schiavoni, G., Gabriele, L., & Mattei, F. (2013) · Frontiers in Oncology · doi:10.3389/fonc.2013.00090 · Cited by 147 · see citing works
Ali, T. H., Pisanti, S., Ciaglia, E., Mortarini, R., Anichini, A., Garofalo, C., Tallerico, R., Santinami, M., Gulletta, E., Ietto, C., et al. (2014) · Nature Communications · doi:10.1038/ncomms6639 · Cited by 145 · see citing works
Self-citationMikulak, J., Oriolo, F., Bruni, E., Roberto, A., Colombo, F., VILLA, A. M., Bosticardo, M., Bortolomai, I., Presti, E. L., Meraviglia, S., et al. (2019) · JCI Insight · doi:10.1172/jci.insight.125884 · Cited by 141 · see citing works
DNAM‐1 control of natural killer cells functions through nectin and nectin‐like proteins
de Andrade, L. F., Smyth, M. J., & Martinet, L. (2013) · Immunology and Cell Biology · doi:10.1038/icb.2013.95 · Cited by 142 · see citing works
DNAM-1 Expression Marks an Alternative Program of NK Cell Maturation
Martinet, L., de Andrade, L. F., Guillerey, C., Lee, J. S., Liu, J., Souza-Fonseca-Guimarães, F., Hutchinson, D. S., Kolesnik, T. B., Nicholson, S. E., Huntington, N. D., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.03.006 · Cited by 142 · see citing works
Mamessier, É., Sylvain, A., Bertucci, F., Castellano, R., Finetti, P., Houvenaeghel, G. F., Charafe‐Jauffret, E., Birnbaum, D., Moretta, A., & Olive, D. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-0792 · Cited by 140 · see citing works
Sánchez-Correa, B., Morgado, S., Gayoso, I., Bergua, J., Casado, J. G., Arcos, M. J., Bengochea, M. L., Durán, E., Solana, R., & Tarazona, R. (2011) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-011-1050-2 · Cited by 139 · see citing works
DNAM-1 controls NK cell activation via an ITT-like motif
Zhang, Z., Wu, N., Lü, Y., Davidson, D., Colonna, M., & Veillette, A. (2015) · The Journal of Experimental Medicine · doi:10.1084/jem.20150792 · Cited by 140 · see citing works
TIGIT/CD226 Axis Regulates Anti-Tumor Immunity
Yeo, J., Ko, M., Lee, D.-H., Park, Y., & Jin, H. (2021) · Pharmaceuticals · doi:10.3390/ph14030200 · Cited by 135 · see citing works
Targeting myeloid-derived suppressor cells to enhance natural killer cell-based immunotherapy
Joshi, S., & Sharabi, A. B. (2022) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2022.108114 · Cited by 140 · see citing works
Krämer, B., Körner, C., Kebschull, M., Glässner, A., Eisenhardt, M., Nischalke, H. D., Alexander, M., Sauerbruch, T., Spengler, U., & Nattermann, J. (2012) · Hepatology · doi:10.1002/hep.25804 · Cited by 129 · see citing works
NK cells gain higher IFN ‐γ competence during terminal differentiation
Luetke-Eversloh, M. V., Cicek, B. B., Siracusa, F., Thom, J. T., Hamann, A., Frischbutter, S., Baumgrass, R., Chang, H., Thiel, A., Dong, J., et al. (2014) · European Journal of Immunology · doi:10.1002/eji.201344072 · Cited by 122 · see citing works
Loss of STAT3 in murine NK cells enhances NK cell–dependent tumor surveillance
Gotthardt, D., Putz, E. M., Straka, E., Kudweis, P., Biaggio, M., Poli, V., Strobl, B., Müller, M. M., & Sexl, V. (2014) · Blood · doi:10.1182/blood-2014-03-564450 · Cited by 122 · see citing works
Chan, C. J., Andrews, D. M., & Smyth, M. J. (2012) · Current Opinion in Immunology · doi:10.1016/j.coi.2012.01.009 · Cited by 117 · see citing works
Leukocyte driven-decidual angiogenesis in early pregnancy
Lima, P. D. A., Zhang, J., Dunk, C., Lye, S. J., & Croy, B. A. (2014) · Cellular and Molecular Immunology · doi:10.1038/cmi.2014.63 · Cited by 116 · see citing works
CD155: A Multi-Functional Molecule in Tumor Progression
Molfetta, R., Zitti, B., Lecce, M., Milito, N. D., Stabile, H., Fionda, C., Cippitelli, M., Gismondi, A., Santoni, A., & Paolini, R. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21030922 · Cited by 113 · see citing works
Increased Soluble CD155 in the Serum of Cancer Patients
Iguchi‐Manaka, A., Okumura, G., Kojima, H., Cho, Y., Hirochika, R., Bando, H., Sato, T., Yoshikawa, H., Hara, H., Shibuya, A., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0152982 · Cited by 113 · see citing works
Self-citationCD155 immunoregulation as a target for natural killer cell immunotherapy in glioblastoma
Lupo, K. B., & Matosevic, S. (2020) · Journal of Hematology & Oncology · doi:10.1186/s13045-020-00913-2 · Cited by 108 · see citing works
Balsamo, M., Vermi, W., Parodi, M., Pietra, G., Manzini, C., Queirolo, P., Lonardi, S., Augugliaro, R., Moretta, A., Facchetti, F., et al. (2012) · European Journal of Immunology · doi:10.1002/eji.201142179 · Cited by 110 · see citing works
Tumor cell recognition by γδ T lymphocytes
Correia, D. V., Lopes, A. C., & Silva‐Santos, B. (2013) · OncoImmunology · doi:10.4161/onci.22892 · Cited by 109 · see citing works
New views on natural killer cell-based immunotherapy for melanoma treatment
Burke, S., Lakshmikanth, T., Colucci, F., & Carbone, E. (2010) · Trends in Immunology · doi:10.1016/j.it.2010.06.003 · Cited by 107 · see citing works
Self-citationBossard, C., Bezieau, S., Matysiak‐Budnik, T., Volteau, C., LABOISSE, C. L., Jotereau, F., & Mosnier, J. (2011) · International Journal of Cancer · doi:10.1002/ijc.26453 · Cited by 109 · see citing works
The Immune Microenvironment and Cancer MetastasisPreprint
El-Kenawi, A., Hänggi, K., & Ruffell, B. (2019) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a037424 · Cited by 107 · see citing works
Lehner, M., Götz, G., Proff, J., Schaft, N., Dörrie, J., Full, F., Ensser, A., Muller, Y. A., Cerwenka, A., Abken, H., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031210 · Cited by 107 · see citing works
Satoh‐Takayama, N., Dumoutier, L., Lesjean‐Pottier, S., Ribeiro, V. S. G., Mandelboim, O., Renauld, J., Vosshenrich, C. A. J., & Santo, J. P. D. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0901935 · Cited by 106 · see citing works
Natural Killer Cells: Tumor Surveillance and Signaling
Guzman, L. G. M., Keating, N., & Nicholson, S. E. (2020) · Cancers · doi:10.3390/cancers12040952 · Cited by 109 · see citing works
Chiang, E. Y., de Almeida, P. E., Nagata, D. D. A., Bowles, K. H., Du, X., Chitre, A. S., Banta, K. L., Kwon, Y. C., McKenzie, B. S., Mittman, S., et al. (2020) · European Journal of Immunology · doi:10.1002/eji.201948405 · Cited by 103 · see citing works
CD226: An Emerging Role in Immunologic Diseases
Huang, Z., Qi, G., Miller, J. S., & Zheng, S. G. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00564 · Cited by 103 · see citing works
Coordinated Expression of DNAM-1 and LFA-1 in Educated NK Cells
Enqvist, M., Ask, E. H., Forslund, E., Carlsten, M., Abrahamsen, G., Béziat, V., Andersson, S., Schaffer, M., Spurkland, A., Bryceson, Y. T., et al. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1401972 · Cited by 100 · see citing works
Changes of NK Cells in Preeclampsia
Fukui, A., Yokota, M., Funamizu, A., Nakamua, R., Fukuhara, R., Yamada, K., Kimura, H., Fukuyama, A., Kamoi, M., Tanaka, K., et al. (2012) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2012.01120.x · Cited by 97 · see citing works
Vitenshtein, A., Charpak-Amikam, Y., Yamin, R., Bauman, Y., Isaacson, B., Stein, N., Berhani, O., Dassa, L., Gamliel, M., Gur, C., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.09.008 · Cited by 96 · see citing works
Elboim, M., Gazit, R., Gur, C., Ghadially, H., Betser-Cohen, G., & Mandelboim, O. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0901644 · Cited by 96 · see citing works
Buddingh, E. P., Schilham, M. W., Ruslan, S. E. N., Berghuis, D., Szuhai, K., Suurmond, J., Taminiau, A. H. M., Gelderblom, H. A. J., Egeler, R. M., Serra, M., et al. (2011) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-010-0965-3 · Cited by 95 · see citing works
The Function of NK Cells in Tumor Metastasis and NK Cell-Based Immunotherapy
Yu, Y. (2023) · Cancers · doi:10.3390/cancers15082323 · Cited by 92 · see citing works
Guo, H., Cruz‐Munoz, M., Wu, N., Robbins, M. D. H., & Veillette, A. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.01107-14 · Cited by 88 · see citing works
Advantages and clinical applications of natural killer cells in cancer immunotherapy
Ames, E., & Murphy, W. J. (2013) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-013-1469-8 · Cited by 88 · see citing works
Super natural killer cells that target metastases in the tumor draining lymph nodes
Chandrasekaran, S., Chan, M. F., Li, J., & King, M. R. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.11.001 · Cited by 87 · see citing works
Endothelial cells express NKG2D ligands and desensitize antitumor NK responses
Thompson, T. W., Kim, A. B., Li, P. J., Wang, J., Jackson, B. T., Huang, K. T. H., Zhang, L., & Raulet, D. H. (2017) · eLife · doi:10.7554/elife.30881 · Cited by 85 · see citing works
How to improve the immunogenicity of chemotherapy and radiotherapy
Ma, Y., Conforti, R., Aymeric, L., Locher, C., Kepp, O., Kroemer, G., & Zitvogel, L. (2011) · Cancer and Metastasis Reviews · doi:10.1007/s10555-011-9283-2 · Cited by 82 · see citing works
Cantoni, C., Huergo-Zapico, L., Parodi, M., Pedrazzi, M., Mingari, M. C., Moretta, A., Sparatore, B., Gonzalez, S. R., Olive, D., Bottino, C., et al. (2016) · Journal of Immunology Research · doi:10.1155/2016/4684268 · Cited by 82 · see citing works
Sun, S., Feng, Y., Xu, D., Zheng, H., & Li, M. (2022) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2022.188700 · Cited by 77 · see citing works
Investigation of NK cell function and their modulation in different malignancies
Konjević, G. M., Jurišić, V., Jović, V., Vuletić, A. M., Martinović, K. M., Radenković, S., & Spužić, I. (2012) · Immunologic Research · doi:10.1007/s12026-012-8285-7 · Cited by 77 · see citing works
He, S., Yin, T., Li, D., Gao, X., Wan, Y., Ma, X., Ye, T., Guo, F., Sun, J., Lin, Z., et al. (2013) · Journal of Translational Medicine · doi:10.1186/1479-5876-11-186 · Cited by 75 · see citing works
Paul, S., Kulkarni, N., Shilpi, & Lal, G. (2016) · OncoImmunology · doi:10.1080/2162402x.2016.1235106 · Cited by 75 · see citing works
Newtonian cell interactions shape natural killer cell education
Goodridge, J. P., Önfelt, B., & Malmberg, K. (2015) · Immunological Reviews · doi:10.1111/imr.12325 · Cited by 74 · see citing works
The Host Defense Peptide Cathelicidin Is Required for NK Cell-Mediated Suppression of Tumor Growth
Büchau, A. S., Morizane, S., Trowbridge, J., Schauber, J., Kotol, P., Bui, J. D., & Gallo, R. L. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0902110 · Cited by 73 · see citing works
mTORC1 and mTORC2 differentially promote natural killer cell development
Yang, C., Tsaih, S., Lemke, A., Flister, M. J., Thakar, M. S., & Malarkannan, S. (2018) · eLife · doi:10.7554/elife.35619 · Cited by 73 · see citing works
López-Cobo, S., Pieper, N., Campos-Silva, C., García-Cuesta, E. M., Reyburn, H. T., Paschen, A., & Valés-Gómez, M. (2018) · OncoImmunology · doi:10.1080/2162402x.2017.1392426 · Cited by 71 · see citing works
Self-citationTriki, H., Charfi, S., Bouzidi, L., Kridis, W. B., Daoud, J., Chaabane, K., Sellami‐Boudawara, T., Rebaï, A., & Cherif, B. (2019) · Life Sciences · doi:10.1016/j.lfs.2019.116543 · Cited by 72 · see citing works
Voskens, C., Watanabe, R., Rollins, S., Campana, D., Hasumi, K., & Mann, D. L. (2010) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/1756-9966-29-134 · Cited by 70 · see citing works
Tallerico, R., Cristiani, C. M., Staaf, E., Garofalo, C., Sottile, R., Capone, M., de Coaña, Y. P., Madonna, G., Palella, E., Wolodarski, M., et al. (2016) · OncoImmunology · doi:10.1080/2162402x.2016.1261242 · Cited by 68 · see citing works
Self-citation
- Authors
- Lakshmikanth, T., Burke, S., Ali, T. H., Kimpfler, S., Ursini, F., Ruggeri, L., Capanni, M., Umansky, V., Paschen, A., Sucker, A., Pende, D., Groh, V., Biassoni, R., Höglund, P., Kato, M., Shibuya, K., Schadendorf, D., Anichini, A., Ferrone, S., Velardi, A., Kärre, K., Shibuya, A., Carbone, E., & Colucci, F.
- Affiliations
- Magna Graecia University (IT)
- Babraham Institute (GB)
- Heidelberg University (DE)
- University of Perugia (IT)
- Ospedale Policlinico San Martino (IT)
- Fred Hutch Cancer Center (US)
- Istituto Giannina Gaslini (IT)
- Karolinska Institutet (SE)
- Chubu University (JP)
- University of Tsukuba (JP)
- Fondazione IRCCS Istituto Nazionale dei Tumori (IT)
- University of Pittsburgh (US)
- ORCID
- Lakshmikanth, Tadepally
- Burke, Shannon
- Ali, Talib Hassan
- Ursini, Francesco
- Ruggeri, Loredana
- Umansky, Viktor
- Paschen, Annette
- Sucker, Antje
- Pende, Daniela
- Biassoni, Roberto
- Höglund, Petter
- Kato, Masashi
- Shibuya, Kazuko
- Schadendorf, Dirk
- Anichini, Andrea
- Ferrone, Soldano
- Velardi, Andrea
- Kärre, Klas
- Shibuya, Akira
- Carbone, Ennio
- Colucci, Francesco
- Venue
- Journal of Clinical Investigation
- Published
- 2009-05-01
- Volume
- 119
- Issue
- 5
- Pages
- 1251-1263
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC2673866
- OpenAlex
- W2143731593
- Cited by
- 347
- References
- 40
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 10 · 2023: 14 · 2022: 14 · 2021: 24 · 2020: 29 · 2019: 31 · 2018: 15 · 2017: 24 · 2016: 26 · 2015: 26 · 2014: 27 · 2013: 23 · 2012: 25
- FWCI
- 10.21
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion)
- Archivio Istituzionale della Ricerca - Università degli Studi della Campania "Luigi Vanvitelli" (submittedVersion)
- Institutional Research Information System University of Ferrara (University of Ferrara) (submittedVersion)
- Funders
- Cancerfonden
- Karolinska Institutet
- Vetenskapsrådet
- Associazione Italiana per la Ricerca sul Cancro
- Medical Research Council
- Biotechnology and Biological Sciences Research Council (BBS/E/B/00001212, BBS/E/B/0000C212)
- National Cancer Institute (R01CA110249)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune Cell Function and Interaction
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Keywords
- natural killer cells, natural cytotoxicity receptors, DNAM-1, melanoma, lymph node metastasis, NK cell-mediated lysis, NK cell receptors, NKG2D, innate immunity, NK cell therapy, antibody blocking, adoptive NK cell transfer, tumor recognition
- MeSH terms
- T Lineage-Specific Activation Antigen 1, Animals, Antibodies, Antigens, Differentiation, T-Lymphocyte, Antigens, Ly, Cytotoxicity Tests, Immunologic, Cytotoxicity, Immunologic, DNA-Binding Proteins, Humans, Killer Cells, Natural, Ligands, Lymphatic Metastasis, Melanoma, Melanoma, Experimental, Mice, Inbred Strains, Mice, Transgenic, Lymphocyte Function-Associated Antigen-1, Immunotherapy, Adoptive, Mice, SCID, Mice, Inbred NOD, Mice, Knockout, Xenograft Model Antitumor Assays, Cell Line, Tumor, Mice, Interleukin Receptor Common gamma Subunit, Natural Killer T-Cells, Natural Cytotoxicity Triggering Receptor 1, Receptors, Natural Cytotoxicity Triggering
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review