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Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth, in a mouse model of melanoma
Open accessAbstract
Although metastasis is the leading cause of cancer-related death, it is not clear why some patients with localized cancer develop metastatic disease after complete resection of their primary tumor. Such relapses have been attributed to tumor cells that disseminate early and remain dormant for prolonged periods of time; however, little is known about the control of these disseminated tumor cells. Here, we have used a spontaneous mouse model of melanoma to investigate tumor cell dissemination and immune control of metastatic outgrowth. Tumor cells were found to disseminate throughout the body early in development of the primary tumor, even before it became clinically detectable. The disseminated tumor cells remained dormant for varying periods of time depending on the tissue, resulting in staggered metastatic outgrowth. Dormancy in the lung was associated with reduced proliferation of the disseminated tumor cells relative to the primary tumor. This was mediated, at least in part, by cytostatic CD8+ T cells, since depletion of these cells resulted in faster outgrowth of visceral metastases. Our findings predict that immune responses favoring dormancy of disseminated tumor cells, which we propose to be the seed of subsequent macroscopic metastases, are essential for prolonging the survival of early stage cancer patients and suggest that therapeutic strategies designed to reinforce such immune responses may produce marked benefits in these patients.
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“On one hand, there is evidence that immune cells have the capability to attenuate metastasis[54–59], which provides insight into how to restore or enhance their ability to combat cancer.”
From Microfluidics: A New Tool for Modeling Cancer–Immune Interactions (2016) · cites this paper as [55]
In the citing paper
“studies in a spontaneous mouse melanoma model suggest that dormancy in micrometastatic lesions is mediated by immunosurveillance 131,132”
From Inside and out: the activities of senescence in cancer (2014) · cites this paper as [132]
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“cytostatic CD8 + T cells suppress the expansion of the disseminated tumour cells 132”
From Inside and out: the activities of senescence in cancer (2014) · cites this paper as [132]
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Citations
Cites
A genetic model for colorectal tumorigenesis
Fearon, E. R., & Vogelstein, B. (1990) · Cell · doi:10.1016/0092-8674(90)90186-i · Cited by 12,132
Jemal, A., Siegel, R. L., Ward, E., Hao, Y., Xu, J., Murray, T., & Thun, M. J. (2008) · CA A Cancer Journal for Clinicians · doi:10.3322/ca.2007.0010 · Cited by 10,184
Gene expression profiling predicts clinical outcome of breast cancer
van 't Veer, L. J., Dai, H., van de Vijver, M. J., He, Y. D., Hart, A. A. M., Mao, M., Peterse, H. L., van der Kooy, K., Marton, M. J., Witteveen, A. T., et al. (2002) · Nature · doi:10.1038/415530a · Cited by 9,536
The Three Es of Cancer Immunoediting
Dunn, G. P., Old, L. J., & Schreiber, R. D. (2004) · Annual Review of Immunology · doi:10.1146/annurev.immunol.22.012703.104803 · Cited by 3,235
Cancer immunotherapy: moving beyond current vaccines
Rosenberg, S. A., Yang, J. C.-H., & Restifo, N. P. (2004) · Nature Medicine · doi:10.1038/nm1100 · Cited by 2,980
Metastasis: from dissemination to organ-specific colonization
Nguyen, D. X., Bos, P. D., & Massagué, J. (2009) · Nature reviews. Cancer · doi:10.1038/nrc2622 · Cited by 2,716
Allard, W. J., Matera, J., Miller, M. C., Repollet, M., Connelly, M. C., Rao, C., Tibbe, A. G. J., Uhr, J. W., & Terstappen, L. W. M. M. (2004) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-04-0378 · Cited by 2,542
A molecular signature of metastasis in primary solid tumors
Ramaswamy, S., Ross, K. N., Lander, E. S., & Golub, T. R. (2002) · Nature Genetics · doi:10.1038/ng1060 · Cited by 2,469
Circular binary segmentation for the analysis of array-based DNA copy number data
Olshen, A. B., Venkatraman, E. S., Lucito, R., & Wigler, M. H. (2004) · Biostatistics · doi:10.1093/biostatistics/kxh008 · Cited by 2,304
Adaptive immunity maintains occult cancer in an equilibrium state
Koebel, C. M., Vermi, W., Swann, J. B., Zerafa, N., Rodig, S. J., Old, L. J., Smyth, M. J., & Schreiber, R. D. (2007) · Nature · doi:10.1038/nature06309 · Cited by 1,438
Flagged first, then by citations
Research works printed but not linked: 6
- Macak, 1998, Pathologica., 90, 388
- Christova, 1996, Gen Diagn Pathol., 142, 63
- Kadivar, 1992, Am Surg., 58, 418
- Buell, 2004, Ann Transplant., 9, 53
- Dworacki, 2001, Clin Cancer Res., 7, 947s
- Old, 2008, Cancer Immun., 8, 1
Cited by
Sorted by citations
Cancer Immunoediting: Integrating Immunity’s Roles in Cancer Suppression and Promotion
Schreiber, R. D., Old, L. J., & Smyth, M. J. (2011) · Science · doi:10.1126/science.1203486 · Cited by 6,474
Emerging Biological Principles of Metastasis
Lambert, A. W., Pattabiraman, D. R., & Weinberg, R. A. (2017) · Cell · doi:10.1016/j.cell.2016.11.037 · Cited by 3,191
T cell exclusion, immune privilege, and the tumor microenvironment
Joyce, J. A., & Fearon, D. T. (2015) · Science · doi:10.1126/science.aaa6204 · Cited by 2,539
Feig, C., Jones, J. O., Kraman, M., Wells, R. J. B., Deonarine, A., Chan, D. S., Connell, C. M., Roberts, E. W., Zhao, Q., Caballero, O. L., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1320318110 · Cited by 2,100
Natural Innate and Adaptive Immunity to Cancer
Vesely, M. D., Kershaw, M. H., Schreiber, R. D., & Smyth, M. J. (2011) · Annual Review of Immunology · doi:10.1146/annurev-immunol-031210-101324 · Cited by 2,225
Metastatic colonization by circulating tumour cells
Massagué, J., & Obenauf, A. C. (2016) · Nature · doi:10.1038/nature17038 · Cited by 2,062
Characteristics and Significance of the Pre-metastatic Niche
Liu, Y., & Cao, X. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.09.011 · Cited by 1,314
Immune cell promotion of metastasis
Kitamura, T., Qian, B.-Z., & Pollard, J. W. (2015) · Nature Reviews Immunology · doi:10.1038/nri3789 · Cited by 1,158
Mechanisms of disseminated cancer cell dormancy: an awakening field
Sosa, M. S., Bragado, P., & Aguirre‐Ghiso, J. A. (2014) · Nature reviews. Cancer · doi:10.1038/nrc3793 · Cited by 1,184
Ganesh, K., & Massagué, J. (2021) · Nature Medicine · doi:10.1038/s41591-020-01195-4 · Cited by 1,123
Cancer stem cells as key drivers of tumour progression
Ayob, A. Z., & Ramasamy, T. S. (2018) · Journal of Biomedical Science · doi:10.1186/s12929-018-0426-4 · Cited by 910
Initial steps of metastasis: Cell invasion and endothelial transmigration
van Zijl, F., Krupitza, G., & Mikulits, W. (2011) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2011.05.002 · Cited by 927
Metastatic Latency and Immune Evasion through Autocrine Inhibition of WNT
Malladi, S., Macalinao, D. G., Jin, X., He, L., Basnet, H., Zou, Y., de Stanchina, E., & Massagué, J. (2016) · Cell · doi:10.1016/j.cell.2016.02.025 · Cited by 791
Tumor metastasis: moving new biological insights into the clinic
Wan, L., Pantel, K., & Kang, Y. (2013) · Nature Medicine · doi:10.1038/nm.3391 · Cited by 763
Early dissemination seeds metastasis in breast cancer
Hosseini, H., Obradović, M. M. S., Hoffmann, M., Harper, K. L., Sosa, M. S., Werner‐Klein, M., Nanduri, L. K., Werno, C., Ehrl, C., Maneck, M., et al. (2016) · Nature · doi:10.1038/nature20785 · Cited by 762
The lingering mysteries of metastatic recurrence in breast cancer
Riggio, A. I., Varley, K. E., & Welm, A. L. (2020) · British Journal of Cancer · doi:10.1038/s41416-020-01161-4 · Cited by 656
Mechanisms Governing Metastatic Dormancy and Reactivation
Giancotti, F. G. (2013) · Cell · doi:10.1016/j.cell.2013.10.029 · Cited by 586
The dormant cancer cell life cycle
Phan, T. G., & Croucher, P. I. (2020) · Nature reviews. Cancer · doi:10.1038/s41568-020-0263-0 · Cited by 588
Mechanism of early dissemination and metastasis in Her2+ mammary cancer
Harper, K. L., Sosa, M. S., Entenberg, D. R., Hosseini, H., Cheung, J. F., Nobre, A. R., Avivar‐Valderas, A., Nagi, C., Girnius, N., Davis, R. J., et al. (2016) · Nature · doi:10.1038/nature20609 · Cited by 578
Tumor Immunology and Tumor Evolution: Intertwined Histories
Galon, J., & Bruni, D. (2020) · Immunity · doi:10.1016/j.immuni.2019.12.018 · Cited by 564
Gender Differences in Cancer Susceptibility: An Inadequately Addressed Issue
Dorak, M. T., & Karpuzoglu, E. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00268 · Cited by 505
Inside and out: the activities of senescence in cancer
Pérez-Mancera, P. A., Young, A. R. J., & Narita, M. (2014) · Nature Reviews Cancer · doi:10.1038/nrc3773 · Cited by 462
Neophytou, C. M., Panagi, M., Stylianopoulos, T., & Papageorgis, P. (2021) · Cancers · doi:10.3390/cancers13092053 · Cited by 489
Krall, J. A., Reinhardt, F., Mercury, O. A., Pattabiraman, D. R., Brooks, M. W., Dougan, M. L., Lambert, A. W., Bierie, B., Ploegh, H. L., Dougan, S. K., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aan3464 · Cited by 452
Macrophages orchestrate breast cancer early dissemination and metastasis
Linde, N., Casanova-Acebes, M., Sosa, M. S., Mortha, A., Rahman, A. H., Farias, E., Harper, K. L., Tardio, E., Reyes-Torres, I., Jones, J. G., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-02481-5 · Cited by 426
Palmieri, E. M., Menga, A., Martín‐Pérez, R., Quinto, A., Riera‐Domingo, C., Tullio, G. D., Hooper, D. C., Lamers, W. H., Ghesquière, B., McVicar, D. W., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.07.054 · Cited by 417
Metastasis-Initiating Cells and Ecosystems
Massagué, J., & Ganesh, K. (2021) · Cancer Discovery · doi:10.1158/2159-8290.cd-21-0010 · Cited by 372
Combination immunotherapy: a road map
Ott, P. A., Hodi, F. S., Kaufman, H. L., Wigginton, J. M., & Wolchok, J. D. (2017) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-017-0218-5 · Cited by 389
Cancer progression and the invisible phase of metastatic colonization
Klein, C. A. (2020) · Nature reviews. Cancer · doi:10.1038/s41568-020-00300-6 · Cited by 387
Toh, B., Wang, X., Keeble, J., Sim, W. J., Khoo, K., Wong, W. C., Kato, M., Prévost‐Blondel, A., Thiery, J. P., & Abastado, J. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001162 · Cited by 386
Self-citationStrategies for the discovery and development of therapies for metastatic breast cancer
Eckhardt, B. L., Francis, P. A., Parker, B. S., & Anderson, R. L. (2012) · Nature Reviews Drug Discovery · doi:10.1038/nrd2372 · Cited by 353
Melanoma plasticity and phenotypic diversity: therapeutic barriers and opportunitiesPreprint
Rambow, F., Marine, J., & Goding, C. R. (2019) · Genes & Development · doi:10.1101/gad.329771.119 · Cited by 348
Differentiation and Regulation of TH Cells: A Balancing Act for Cancer Immunotherapy
Basu, A. B., Ramamoorthi, G., Albert, G. K., Gallen, C., Beyer, A., Snyder, C., Koski, G. K., Disis, M. L., Czerniecki, B. J., & Kodumudi, K. N. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.669474 · Cited by 329
The evolution of tumour phylogenetics: principles and practice
Schwartz, R. S., & Schäffer, A. A. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2016.170 · Cited by 329
Does tumour dormancy offer a therapeutic target?
Goss, P. E., & Chambers, A. F. (2010) · Nature reviews. Cancer · doi:10.1038/nrc2933 · Cited by 310
The immune system in cancer metastasis: friend or foe?
Janssen, L. M. E., Ramsay, E. E., Logsdon, C. D., & Overwijk, W. W. (2017) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-017-0283-9 · Cited by 298
Therapy resistance mediated by cancer stem cells
Steinbichler, T. B., Dudás, J., Skvortsov, S., Ganswindt, U., Riechelmann, H., & Skvortsova, I. (2018) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2018.11.006 · Cited by 298
Pommier, A., Anaparthy, N., Memos, N. K., Kelley, Z. L., Gouronnec, A., Yan, R., Auffray, C., Albrengues, J., Egeblad, M., Iacobuzio–Donahue, C. A., et al. (2018) · Science · doi:10.1126/science.aao4908 · Cited by 269
Determinants of metastatic competency in colorectal cancer
Tauriello, D. V. F., Calon, A., Lonardo, E., & Batlle, E. (2017) · Molecular Oncology · doi:10.1002/1878-0261.12018 · Cited by 262
Hong, M. L. W., Puaux, A., Huang, C. W., Loumagne, L., Tow, C., Mackay, C. R., Kato, M., Prévost‐Blondel, A., Avril, M., Nardin, A., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-1466 · Cited by 262
Self-citationSTING inhibits the reactivation of dormant metastasis in lung adenocarcinoma
Hu, J. Y., Rivera, F. J. S., Wang, Z., Johnson, G. N., Ho, Y.-J., Ganesh, K., Umeda, S., Gan, S., Mujal, A. M., Delconte, R. B., et al. (2023) · Nature · doi:10.1038/s41586-023-05880-5 · Cited by 261
Inflammation and immune surveillance in cancer
Chow, M. T., Möller, A., & Smyth, M. J. (2011) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2011.12.004 · Cited by 253
Targeting Breast Cancer Metastasis
Jin, X., & Mu, P. (2015) · Breast Cancer Basic and Clinical Research · doi:10.4137/bcbcr.s25460 · Cited by 250
Sosa, M. S., Avivar‐Valderas, A., Bragado, P., Wen, H., & Aguirre‐Ghiso, J. A. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-2574 · Cited by 243
The current paradigm and challenges ahead for the dormancy of disseminated tumor cells
Risson, E., Nobre, A. R., Maguer‐Satta, V., & Aguirre‐Ghiso, J. A. (2020) · Nature Cancer · doi:10.1038/s43018-020-0088-5 · Cited by 248
The transcription factor IRF1 dictates the IL-21-dependent anticancer functions of TH9 cells
Végran, F., Berger, H., Boidot, R., Mignot, G., Bruchard, M., Dosset, M., Chalmin, F., Rébé, C., Dérangère, V., Ryffel, B., et al. (2014) · Nature Immunology · doi:10.1038/ni.2925 · Cited by 228
Self-citationDamsky, W., Rosenbaum, L. E., & Bosenberg, M. (2010) · Cancers · doi:10.3390/cancers3010126 · Cited by 233
Optimization and Evaluation of a Novel Size Based Circulating Tumor Cell Isolation System
Xu, L., Mao, X., Imrali, A., Syed, F., Mutsvangwa, K., Berney, D. M., Cathcart, P. J., Hines, J. E. W., Shamash, J., & Lu, Y. (2015) · PLoS ONE · doi:10.1371/journal.pone.0138032 · Cited by 232
Microfluidics: A New Tool for Modeling Cancer–Immune Interactions
Boussommier-Calleja, A., Li, R., Chen, M. B., Wong, S. C., & Kamm, R. D. (2016) · Trends in Cancer · doi:10.1016/j.trecan.2015.12.003 · Cited by 224
Linking the future of anticancer metal-complexes to the therapy of tumour metastases
Bergamo, A., & Sava, G. (2015) · Chemical Society Reviews · doi:10.1039/c5cs00134j · Cited by 225
Immune Microenvironment in Tumor Progression: Characteristics and Challenges for Therapy
Chew, V., Toh, H. C., & Abastado, J. (2012) · Journal of Oncology · doi:10.1155/2012/608406 · Cited by 224
Self-citationStem-like exhausted and memory CD8+ T cells in cancer
Gebhardt, T., Park, S. L., & Parish, I. A. (2023) · Nature reviews. Cancer · doi:10.1038/s41568-023-00615-0 · Cited by 234
The force awakens: metastatic dormant cancer cells
Park, S., & Nam, J. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-0423-z · Cited by 218
Framework models of tumor dormancy from patient-derived observations
Klein, C. A. (2010) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2010.10.011 · Cited by 207
The metastatic niche and stromal progression
Sleeman, J. P. (2012) · Cancer and Metastasis Reviews · doi:10.1007/s10555-012-9373-9 · Cited by 214
Tran, D. D., Corsa, C. A. S., Biswas, H., Aft, R., & Longmore, G. D. (2011) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-11-0371 · Cited by 197
Kerjaschki, D., Bagó-Horváth, Z., Rudas, M., Sexl, V., Schneckenleithner, C., Wolbank, S., Bond, G., Krieger, S., Kalt, R., Hantusch, B., et al. (2011) · Journal of Clinical Investigation · doi:10.1172/jci44751 · Cited by 190
Gomis, R. R., & Gawrzak, S. (2016) · Molecular Oncology · doi:10.1016/j.molonc.2016.09.009 · Cited by 202
Endo, H., & Inoue, M. (2018) · Cancer Science · doi:10.1111/cas.13917 · Cited by 183
Dormant tumour cells, their niches and the influence of immunity
Goddard, E. T., Božić, I., Riddell, S. R., & Ghajar, C. M. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0214-0 · Cited by 180
Myeloid‐derived suppressor cells: Important contributors to tumor progression and metastasis
Safarzadeh, E., Orangi, M., Mohammadi, H., Babaie, F., & Baradaran, B. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.26075 · Cited by 177
Metastatic niche functions and therapeutic opportunities
Celià-Terrassa, T., & Kang, Y. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0145-9 · Cited by 174
Kciuk, M., Gielecińska, A., Budzinska, A., Mojzych, M., & Kontek, R. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073847 · Cited by 170
Melanoma metastasis: new concepts and evolving paradigms
Damsky, W., Theodosakis, N., & Bosenberg, M. (2013) · Oncogene · doi:10.1038/onc.2013.194 · Cited by 174
Lin, W., Chang, Y.-W., Hong, M.-X., Hsu, T.-C., Lee, K.-C., Lin, C., & Lee, J.-L. (2020) · Oncogene · doi:10.1038/s41388-020-01566-8 · Cited by 164
Self-citationBone metastasis and the metastatic niche
Ren, G., Esposito, M., & Kang, Y. (2015) · Journal of Molecular Medicine · doi:10.1007/s00109-015-1329-4 · Cited by 167
Type I Interferons and Natural Killer Cell Regulation in Cancer
Müller, L., Aigner, P., & Stoiber, D. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00304 · Cited by 173
Resident memory CD8+ T cells in regional lymph nodes mediate immunity to metastatic melanoma
Molodtsov, A. K., Khatwani, N., Vella, J. L., Lewis, K. A., Zhao, Y., Han, J., Sullivan, D. E., Searles, T. G., Preiss, N. K., Shabaneh, T. B., et al. (2021) · Immunity · doi:10.1016/j.immuni.2021.08.019 · Cited by 157
Building the niche: The role of the S100 proteins in metastatic growth
Lukanidin, E. M., & Sleeman, J. P. (2012) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2012.02.006 · Cited by 152
Do all roads lead to Rome? Routes to metastasis development
Sleeman, J. P., Nazarenko, I. A., & Thiele, W. (2011) · International Journal of Cancer · doi:10.1002/ijc.26027 · Cited by 153
Recent Progress in Isolation and Detection of Extracellular Vesicles for Cancer Diagnostics
Wang, W., Luo, J., & Wang, S. (2018) · Advanced Healthcare Materials · doi:10.1002/adhm.201800484 · Cited by 151
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
Alcohol and Cancer: Mechanisms and Therapies
Ratna, A., & Mandrekar, P. (2017) · Biomolecules · doi:10.3390/biom7030061 · Cited by 155
New insights into the correlations between circulating tumor cells and target organ metastasis
Zhan, Q., Liu, B., Situ, X., Luo, Y., Fu, T., Wang, Y., Xie, Z., Ren, L., Zhu, Y. J., He, W., et al. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01725-9 · Cited by 156
Interferons in cancer immunoediting: sculpting metastasis and immunotherapy response
von Locquenghien, M., Rozalén, C., & Celià-Terrassa, T. (2021) · Journal of Clinical Investigation · doi:10.1172/jci143296 · Cited by 144
Immune regulation of metastasis: mechanistic insights and therapeutic opportunities
Blomberg, O. S., Spagnuolo, L., & de Visser, K. E. (2018) · Disease Models & Mechanisms · doi:10.1242/dmm.036236 · Cited by 145
Emerging roles of intratumor microbiota in cancer metastasis
Fu, A., Yao, B., Dong, T., & Cai, S. (2022) · Trends in Cell Biology · doi:10.1016/j.tcb.2022.11.007 · Cited by 146
Shibue, T., & Weinberg, R. A. (2010) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2010.12.003 · Cited by 138
Aytés, À., Mitrofanova, A., Kinkade, C. W., Lefèbvre, C., Lei, M., Phelan, V., Lekaye, C., Koutcher, J. A., Cardiff, R. D., Califano, A., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1303558110 · Cited by 135
Tenascin-C Protects Cancer Stem–like Cells from Immune Surveillance by Arresting T-cell Activation
Jachetti, E., Caputo, S., Mazzoleni, S., Brambillasca, C. S., Parigi, S. M., Grioni, M., Piras, I. S., Restuccia, U., Calcinotto, A., Freschi, M., et al. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-2346 · Cited by 146
Hix, L. M., Karavitis, J., Khan, M. W., Shi, Y. H., Khazaie, K., & Zhang, M. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.441402 · Cited by 134
Targeting tumor–stromal interactions in bone metastasis
Esposito, M., & Kang, Y. (2013) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.10.006 · Cited by 129
Cytotoxic lymphocytes target characteristic biophysical vulnerabilities in cancer
Tello‐Lafoz, M., Srpan, K., Sanchez, E. E., Hu, J. Y., Remšík, J., Romin, Y., Calò, A., Hoen, D. R., Bhanot, U. K., Morris, L. G. T., et al. (2021) · Immunity · doi:10.1016/j.immuni.2021.02.020 · Cited by 129
Baklaushev, V. P., Kilpeläinen, A., Petkov, S., Abakumov, M. A., Grinenko, N. F., Yusubalieva, G. M., Latanova, A. A., Gubskiy, I. L., Zabozlaev, F., Starodubova, E. S., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-07851-z · Cited by 132
Harter, P. N., Bernatz, S., Scholz, A., Zeiner, P. S., Zinke, J., Kiyose, M., Blasel, S., Beschorner, R., Senft, C., Bender, B., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.5696 · Cited by 125
Cancer metastasis: Molecular mechanisms and clinical perspectives
Khan, S. U., Fatima, K., Malik, F. A., Kalkavan, H., & Wani, A. (2023) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2023.108522 · Cited by 127
IFN-γ-dependent NK cell activation is essential to metastasis suppression by engineered Salmonella
Lin, Q., Li, R., Jia, X., Li, R., Yu, B., Hu, J., Luo, X., Badea, S. R., Chen, X., Fu, G., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22755-3 · Cited by 118
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Teng, M. W. L., Vesely, M. D., Duret, H., McLaughlin, N. M., Towne, J. E., Schreiber, R. D., & Smyth, M. J. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-1337 · Cited by 127
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Metadata
- Authors
- Eyles, J., Puaux, A.-L., Wang, X., Toh, B., Prakash, C., Hong, M., Tan, T. G., Zheng, L., Ong, L. C., Jin, Y., Kato, M., Prévost-Blondel, A., Chow, P., Yang, H., & Abastado, J.-P.
- Affiliations
- Agency for Science, Technology and Research (SG)
- Singapore Immunology Network (SG)
- SingHealth (SG)
- Chubu University (JP)
- National University of Singapore (SG)
- Corresponding author
- Abastado, Jean-Pierre
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2010-06-01
- Volume
- 120
- Issue
- 6
- Pages
- 2030-2039
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC2877955
- OpenAlex
- W2063725270
- Cited by
- 506
- References
- 74
- Citations by year
- 2026: 14 · 2025: 18 · 2024: 28 · 2023: 25 · 2022: 31 · 2021: 43 · 2020: 49 · 2019: 29 · 2018: 33 · 2017: 35 · 2016: 36 · 2015: 35 · 2014: 19 · 2013: 36 · 2012: 33
- FWCI
- 17.52
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- National University of Singapore (submittedVersion)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Stress, Anesthesia, and Immune Response
- Keywords
- melanoma, disseminated tumor cells, tumor dormancy, metastasis, immune surveillance, CD8+ T cells, metastatic outgrowth, lung metastasis, visceral metastases
- MeSH terms
- Animals, Humans, Melanoma, Mice, Transgenic, T-Lymphocytes, Monitoring, Immunologic, Cellular Structures, Mice
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