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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Immune cells can attenuate metastasis.
“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 a spontaneous mouse melanoma model, dormancy in micrometastatic lesions is mediated by immunosurveillance.
“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]
Cytostatic CD8+ T cells suppress expansion of disseminated tumour cells in the melanoma model.
“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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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 · see citing works
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 · see citing works
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 · see citing works
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 3,087 · see citing works
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 2,956 · see citing works
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 2,637 · see citing works
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 · see citing works
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 2,448 · see citing works
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 2,256 · see citing works
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 · see citing works
Metastasis Results from Preexisting Variant Cells Within a Malignant Tumor
Fidler, I. J., & Kripke, M. L. (1977) · Science · doi:10.1126/science.887927 · Cited by 1,426 · see citing works
Dissecting the metastatic cascade
Pantel, K., & Brakenhoff, R. H. (2004) · Nature reviews. Cancer · doi:10.1038/nrc1370 · Cited by 1,284 · see citing works
Systemic Spread Is an Early Step in Breast Cancer
Hüsemann, Y., Geigl, J. B., Schubert, F., Musiani, P., Meyer, M., Burghart, E., Forni, G., Eils, R., Fehm, T. N., Riethmüller, G., et al. (2008) · Cancer Cell · doi:10.1016/j.ccr.2007.12.003 · Cited by 1,175 · see citing works
Parallel progression of primary tumours and metastases
Klein, C. A. (2009) · Nature reviews. Cancer · doi:10.1038/nrc2627 · Cited by 1,134 · see citing works
Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment
Harlin, H., Meng, Y., Peterson, A. C., Zha, Y., Tretiakova, M., Slingluff, C., McKee, M., & Gajewski, T. F. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-2281 · Cited by 1,121 · see citing works
Circulating Tumor Cells in Patients with Breast Cancer Dormancy
Meng, S., Tripathy, D., Frenkel, E. P., Shete, S. S., Naftalis, E. Z., Huth, J. F., Beitsch, P. D., Leitch, M., Hoover, S. J., Euhus, D., et al. (2004) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-04-1110 · Cited by 969 · see citing works
A faster circular binary segmentation algorithm for the analysis of array CGH data
Venkatraman, E. S., & Olshen, A. B. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btl646 · Cited by 963 · see citing works
Biological Diversity in Metastatic Neoplasms: Origins and Implications
Fidler, I. J., & Hart, I. R. (1982) · Science · doi:10.1126/science.7112116 · Cited by 926 · see citing works
Braun, S., Pantel, K., Müller, P. E., Janni, W., Hepp, F., Kentenich, C. R. M., Gastroph, S., Wischnik, A., Dimpfl, T., Kindermann, G., et al. (2000) · New England Journal of Medicine · doi:10.1056/nejm200002243420801 · Cited by 923 · see citing works
The roles of IFNγ in protection against tumor development and cancer immunoediting
Ikeda, H., Old, L. J., & Schreiber, R. D. (2002) · Cytokine & Growth Factor Reviews · doi:10.1016/s1359-6101(01)00038-7 · Cited by 899 · see citing works
Cell Growth Arrest and Induction of Cyclin-Dependent Kinase Inhibitor p21WAF1/CIP1 Mediated by STAT1
Chin, Y. E., Kitagawa, M., Su, W.-C., You, Z.-H., Iwamoto, Y., & Fu, X.-Y. (1996) · Science · doi:10.1126/science.272.5262.719 · Cited by 893 · see citing works
Metastasis genes: A progression puzzle
Bernards, R., & Weinberg, R. A. (2002) · Nature · doi:10.1038/418823a · Cited by 801 · see citing works
A microenvironmental model of carcinogenesis
Gatenby, R. A., & Gillies, R. J. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2255 · Cited by 725 · see citing works
Malignant melanoma: genetics and therapeutics in the genomic eraPreprint
Chin, L., Garraway, L. A., & Fisher, D. E. (2006) · Genes & Development · doi:10.1101/gad.1437206 · Cited by 509 · see citing works
Sotiriou, C. P., & Piccart, M. J. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2173 · Cited by 461 · see citing works
Lung metastasis genes couple breast tumor size and metastatic spread
Minn, A. J., Gupta, G. P., Padua, D., Bos, P., Nguyen, D. X., Nuyten, D., Kreike, B., Zhang, Y., Wang, Y., Ishwaran, H., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701138104 · Cited by 400 · see citing works
Braun, S., Kentenich, C. R. M., Janni, W., Hepp, F., Waal, J. D., Willgeroth, F., Sommer, H. L., & Pantel, K. (2000) · Journal of Clinical Oncology · doi:10.1200/jco.2000.18.1.80 · Cited by 394 · see citing works
Cancer Management: A Multidisciplinary Approach
Pazdur, R., Coia, L. R., Hoskins, W. J., & Wagman, L. D. (2007) · Cited by 354 · see citing works
Is cancer a disease of self-seeding?
Norton, L., & Massagué, J. (2006) · Nature Medicine · doi:10.1038/nm0806-875 · Cited by 346 · see citing works
Veronesi, U., Marubini, E., Mariani, L., Valagussa, P., & Zucali, R. (1999) · European Journal of Cancer · doi:10.1016/s0959-8049(99)00133-1 · Cited by 345 · see citing works
Mihm, M. C., Clemente, C. G., & Cascinelli, N. (1996) · PubMed · Cited by 318 · see citing works
Müller-Hermelink, N., Braumüller, H., Pichler, B., Wieder, T., Mailhammer, R., Schaak, K., Ghoreschi, K., Yazdi, A., Haubner, R., Sander, C. A., et al. (2008) · Cancer Cell · doi:10.1016/j.ccr.2008.04.001 · Cited by 302 · see citing works
Schlimok, G., Funke, I., Holzmann, B., Göttlinger, H. G., Schmidt, G., Hauser, H., Swierkot, S., Warnecke, H., Schneider, B., Koprowski, H., et al. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.23.8672 · Cited by 299 · see citing works
Fatal Melanoma Transferred in a Donated Kidney 16 Years after Melanoma Surgery
MacKie, R. M., Reid, R., & Junor, B. J. R. (2003) · New England Journal of Medicine · doi:10.1056/nejm200302063480620 · Cited by 290 · see citing works
An Alternating Least Squares Approach to Inferring Phylogenies from Pairwise Distances
Felsenstein, J. (1997) · Systematic Biology · doi:10.1093/sysbio/46.1.101 · Cited by 289 · 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-citationD, S. M. M., Hoon, D. S. �., Ambrosi, A., Nitti, D., & Rossi, C. R. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-0823 · Cited by 218 · see citing works
Malignant Tumors of the Small Intestine: A Review of 144 Cases
North, J. H., & Pack, M. (2000) · The American Surgeon · doi:10.1177/000313480006600110 · Cited by 183 · see citing works
Cancer micrometastasis and tumour dormancy
Wikman, H., Vessella, R. L., & Pantel, K. (2008) · Apmis · doi:10.1111/j.1600-0463.2008.01033.x · Cited by 175 · see citing works
Piras, F., Colombari, R., Minerba, L., Murtas, D., Floris, C., Maxia, C., Corbu, A., Perra, M. T., & Sirigu, P. (2005) · Cancer · doi:10.1002/cncr.21283 · Cited by 169 · see citing works
Chromosomal Alterations in Ductal Carcinomas In Situ and Their In Situ Recurrences
Waldman, F. M. (2000) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/92.4.313 · Cited by 166 · see citing works
The heterogeneity of the kinetics of response to ipilimumab in metastatic melanoma: patient cases.
Saenger, Y. M., & Wolchok, J. D. (2008) · PubMed Central · Cited by 164 · see citing works
Norton, L. (2005) · The Oncologist · doi:10.1634/theoncologist.10-6-370 · Cited by 162 · see citing works
Primary Malignant Melanoma of the Esophagus
Chalkiadakis, G., Wihlm, J. M., Morand, G., Weill-Bousson, M., & Witz, J. (1985) · The Annals of Thoracic Surgery · doi:10.1016/s0003-4975(10)61963-7 · Cited by 157 · see citing works
Mullins, I. M., Slingluff, C. L., Lee, J. K., Garbee, C. F., Shu, J., Anderson, S. G., Mayer, M. E., Knaus, W. A., & Mullins, D. W. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-2059 · Cited by 150 · see citing works
Bidard, F., Vincent‐Salomon, A., Gomme, S., Nos, C., Rycke, Y. D., Thiery, J. P., Sigal‐Zafrani, B., Mignot, L., Sastre‐Garau, X., Pierga, J., et al. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-4749 · Cited by 142 · see citing works
Donor transmitted malignancies.
Buell, J., Beebe, T. M., Trofe, J., Gross, T. G., Alloway, R. R., Hanaway, M. J., & Woodle, E. S. (2004) · PubMed · Cited by 139 · see citing works
Weir, L., Speers, C. H., Dyachkova, Y., & Olivotto, I. A. (2002) · Journal of Clinical Oncology · doi:10.1200/jco.2002.07.112 · Cited by 138 · see citing works
Dormancy of metastatic melanoma
Ossowski, L., & Aguirre‐Ghiso, J. A. (2009) · Pigment Cell & Melanoma Research · doi:10.1111/j.1755-148x.2009.00647.x · Cited by 132 · see citing works
Dworacki, G., Meidenbauer, N., Kuss, I., Hoffmann, T. K., Gooding, W. E., Lotze, M. T., & Whiteside, T. L. (2001) · PubMed · Cited by 129 · see citing works
Iwamoto, T., Takahashi, M., Ito, M. A., Hamatani, K., Ohbayashi, M., Wajjwalku, W., Isobe, K.-I., & Nakashima, I. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb04878.x · Cited by 129 · see citing works
PhyloDraw: a phylogenetic tree drawing system
Choi, J.-H., Jung, H.-Y., Kim, H.-S., & Cho, H.-G. (2000) · Bioinformatics · doi:10.1093/bioinformatics/16.11.1056 · Cited by 126 · see citing works
Hillen, F., Baeten, C. I. M., van de Winkel, A., Creytens, D., van der Schaft, D. W. J., Winnepenninckx, V. J. L., & Griffioen, A. W. (2007) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-007-0353-9 · Cited by 120 · see citing works
Callejo, S. A., Antecka, E., Blanco, P. L., Edelstein, C., & Burnier, M. N. (2006) · Eye · doi:10.1038/sj.eye.6702322 · Cited by 110 · see citing works
Clonal History of Papillomavirus-Induced Dysplasia in the Female Lower Genital Tract
Vinokurova, S., Wentzensen, N., Einenkel, J., Klaes, R., Ziegert, C., Melsheimer, P., Sartor, H., Horn, L., Höckel, M., & Doeberitz, M. V. K. (2005) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/dji428 · Cited by 109 · see citing works
Do primary small intestinal melanomas exist? Report of a case
Sachs, D. L., Lowe, L., Chang, A. E., Carson, E., & Johnson, T. M. (1999) · Journal of the American Academy of Dermatology · doi:10.1016/s0190-9622(99)70273-2 · Cited by 95 · see citing works
Palmieri, G., Ascierto, P. A., Perrone, F., Satriano, S. M. R., Ottaiano, A., Daponte, A., Napolitano, M., Caracò, C., Mozzillo, N., Melucci, M. T., et al. (2003) · Journal of Clinical Oncology · doi:10.1200/jco.2003.01.128 · Cited by 90 · see citing works
Schuster, R., Bechrakis, N. E., Stroux, A., Busse, A., Schmittel, A. H., Scheibenbogen, C., Thiel, E., Foerster, M. H., & Keilholz, U. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-2329 · Cited by 71 · see citing works
Old, L. J. (2008) · PubMed · Cited by 68 · see citing works
Cell Proliferation Kinetics in the Human Hair Root
Weinstein, G. D., & Mooney, K. M. (1980) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12514601 · Cited by 65 · see citing works
Distinct Role for CD8 T Cells toward Cutaneous Tumors and Visceral Metastases
Lengagne, R., Graff-Dubois, S., Garcette, M., Renia, L., Kato, M., Guillet, J.-G., Engelhard, V. H., Avril, M.-F., Abastado, J.-P., & Prévost-Blondel, A. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.1.130 · Cited by 64 · see citing works
Self-citationUlmer, A., Beutel, J., Süßkind, D., Hilgers, R.-D., Ziemssen, F., Lüke, M., Röcken, M., Rohrbach, M., Fierlbeck, G., Bartz‐Schmidt, K. U., et al. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-0012 · Cited by 62 · see citing works
Primary malignant melanoma of the oesophagus: case report and review of surgical pathology.
Stranks, G. J., Mathai, J., & Rowe-Jones, D. C. (1991) · Gut · doi:10.1136/gut.32.7.828 · Cited by 58 · see citing works
Primary malignant melanoma of the small bowel: a case study.
Kadivar, T. F., Vw, V., & Eu, K. (1992) · PubMed · Cited by 57 · see citing works
Gene expression predictors in breast cancer: Current status, limitations and perspectives
Desmedt, C., Ruíz‐García, E., & André, F. (2008) · European Journal of Cancer · doi:10.1016/j.ejca.2008.09.011 · Cited by 51 · see citing works
Tumor Infiltrating Lymphocytes in Uveal Melanoma: A Link with Clinical Behavior?
Staibano, S., Mascolo, M., Tranfa, F., Salvatore, G., Mignogna, C., Bufo, P., Nugnes, L., Bonavolontà, G., & Rosa, G. D. (2006) · International Journal of Immunopathology and Pharmacology · doi:10.1177/205873920601900117 · Cited by 35 · see citing works
The transmission of donor‐derived malignant melanoma to a renal allograft recipient
Milton, C., Barbara, J. A. J., Cooper, J., Rao, M., Russell, C., & Gr, R. (2006) · Clinical Transplantation · doi:10.1111/j.1399-0012.2006.00514.x · Cited by 34 · see citing works
Optimal genotype determination in highly multiplexed SNP data
Moorhead, M., Hardenbol, P., Siddiqui, F. A., Falkowski, M., Bruckner, C., Ireland, J. S., Jones, H. B., Jain, M., Willis, T. D., & Faham, M. (2005) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5201528 · Cited by 33 · see citing works
A Survival Benefit From Axillary Dissection: Was Halsted Correct?
Morrow, M. (1999) · Annals of Surgical Oncology · doi:10.1007/s10434-999-0017-4 · Cited by 33 · see citing works
Three cases of primary malignant melanoma of the alimentary tract.
Christova, S. L., Meinhard, K., Mihailov, I., & Alexiev, B. A. (1996) · PubMed · Cited by 33 · see citing works
The Anti-proliferative Activity of Interferon-γ on Ovarian Cancer: In Vitro and in Vivo
Wall, L. R., Burke, F., Smyth, J. F., & Balkwill, F. R. (2003) · Gynecologic Oncology · doi:10.1006/gyno.2002.6707 · Cited by 32 · see citing works
Melanoma of the stomach: reality or fiction?
Mačák, J. (1998) · PubMed · Cited by 15 · see citing works
Mapping of Melanoma Modifier Loci in RET Transgenic Mice
Dragani, T. A., Peissel, B., Zanesi, N. A. O., Aloisi, A., Dai, Y., Kato, M., Suzuki, H., & Nakashima, I. (2000) · Japanese Journal of Cancer Research · doi:10.1111/j.1349-7006.2000.tb00897.x · Cited by 14 · see citing works
Self-citationTarantino, L., Nocera, V. G., Perrotta, M., Balsamo, G., Schiano, A., Orabona, P., Sordelli, I., Ripa, C., Parmeggiani, D., & Sperlongano, P. (2007) · Journal of Ultrasound in Medicine · doi:10.7863/jum.2007.26.1.121 · Cited by 9 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [11]11. Bernards R, Weinberg RA. A progression puzzle. Nature. 2002;418(6900):823.
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 · see citing works
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 3,075 · see citing works
T cell exclusion, immune privilege, and the tumor microenvironment
Joyce, J. A., & Fearon, D. T. (2015) · Science · doi:10.1126/science.aaa6204 · Cited by 2,494 · see citing works
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 · see citing works
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 2,095 · see citing works
Metastatic colonization by circulating tumour cells
Massagué, J., & Obenauf, A. C. (2016) · Nature · doi:10.1038/nature17038 · Cited by 2,062 · see citing works
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 1,287 · see citing works
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 · see citing works
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 1,125 · see citing works
Ganesh, K., & Massagué, J. (2021) · Nature Medicine · doi:10.1038/s41591-020-01195-4 · Cited by 1,070 · see citing works
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 · see citing works
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 884 · see citing works
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 · see citing works
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 746 · see citing works
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 745 · see citing works
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 621 · see citing works
Mechanisms Governing Metastatic Dormancy and Reactivation
Giancotti, F. G. (2013) · Cell · doi:10.1016/j.cell.2013.10.029 · Cited by 586 · see citing works
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 581 · see citing works
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 569 · see citing works
Tumor Immunology and Tumor Evolution: Intertwined Histories
Galon, J., & Bruni, D. (2020) · Immunity · doi:10.1016/j.immuni.2019.12.018 · Cited by 541 · see citing works
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 495 · see citing works
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 · see citing works
Neophytou, C. M., Panagi, M., Stylianopoulos, T., & Papageorgis, P. (2021) · Cancers · doi:10.3390/cancers13092053 · Cited by 468 · see citing works
Krall, J. A., Reinhardt, F., Mercury, O. A., Pattabiraman, D., Brooks, M., Dougan, M., Lambert, A. W., Bierie, B., Ploegh, H., Dougan, S., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aan3464 · Cited by 399 · see citing works
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 416 · see citing works
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 408 · see citing works
Metastasis-Initiating Cells and Ecosystems
Massagué, J., & Ganesh, K. (2021) · Cancer Discovery · doi:10.1158/2159-8290.cd-21-0010 · Cited by 372 · see citing works
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 379 · see citing works
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 379 · see citing works
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 369 · see citing works
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 352 · see citing works
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 316 · see citing works
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 318 · see citing works
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 319 · see citing works
Does tumour dormancy offer a therapeutic target?
Goss, P. E., & Chambers, A. F. (2010) · Nature reviews. Cancer · doi:10.1038/nrc2933 · Cited by 302 · see citing works
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 292 · see citing works
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 289 · see citing works
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 · see citing works
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 257 · see citing works
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 248 · see citing works
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 252 · see citing works
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 241 · see citing works
Targeting Breast Cancer Metastasis
Jin, X., & Mu, P. (2015) · Breast Cancer Basic and Clinical Research · doi:10.4137/bcbcr.s25460 · Cited by 239 · see citing works
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 233 · see citing works
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 235 · see citing works
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 · see citing works
Self-citationDamsky, W., Rosenbaum, L. E., & Bosenberg, M. (2010) · Cancers · doi:10.3390/cancers3010126 · Cited by 225 · see citing works
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 225 · see citing works
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 · see citing works
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 220 · see citing works
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 217 · see citing works
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 216 · see citing works
The force awakens: metastatic dormant cancer cells
Park, S., & Nam, J. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-0423-z · Cited by 209 · see citing works
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 · see citing works
The metastatic niche and stromal progression
Sleeman, J. P. (2012) · Cancer and Metastasis Reviews · doi:10.1007/s10555-012-9373-9 · Cited by 205 · see citing works
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 200 · see citing works
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 · see citing works
Gomis, R. R., & Gawrzak, S. (2016) · Molecular Oncology · doi:10.1016/j.molonc.2016.09.009 · Cited by 190 · see citing works
Endo, H., & Inoue, M. (2018) · Cancer Science · doi:10.1111/cas.13917 · Cited by 178 · see citing works
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 179 · see citing works
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 176 · see citing works
Metastatic niche functions and therapeutic opportunities
Celià-Terrassa, T., & Kang, Y. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0145-9 · Cited by 172 · see citing works
Kciuk, M., Gielecińska, A., Budzinska, A., Mojzych, M., & Kontek, R. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073847 · Cited by 170 · see citing works
Melanoma metastasis: new concepts and evolving paradigms
Damsky, W., Theodosakis, N., & Bosenberg, M. (2013) · Oncogene · doi:10.1038/onc.2013.194 · Cited by 163 · see citing works
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 · see citing works
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 161 · see citing works
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 165 · see citing works
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 155 · see citing works
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 151 · see citing works
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 150 · see citing works
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 148 · 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
Alcohol and Cancer: Mechanisms and Therapies
Ratna, A., & Mandrekar, P. (2017) · Biomolecules · doi:10.3390/biom7030061 · Cited by 149 · see citing works
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 150 · see citing works
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 · see citing works
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 142 · see citing works
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 142 · see citing works
Shibue, T., & Weinberg, R. A. (2010) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2010.12.003 · Cited by 138 · see citing works
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 132 · see citing works
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 135 · see citing works
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 · see citing works
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 · see citing works
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 126 · see citing works
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 124 · see citing works
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 · see citing works
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 123 · see citing works
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 117 · see citing works
Opposing Roles for IL-23 and IL-12 in Maintaining Occult Cancer in an Equilibrium State
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 118 · see citing works
Tumor Dormancy and Relapse: From a Natural Byproduct of Evolution to a Disease State
Manjili, M. H. (2017) · Cancer Research · doi:10.1158/0008-5472.can-17-0068 · Cited by 116 · see citing works
Adaptive Stress Responses During Tumor Metastasis and Dormancy
Senft, D., & Ronai, Z. A. (2016) · Trends in cancer · doi:10.1016/j.trecan.2016.06.004 · Cited by 111 · see citing works
Circulating immune cell and microRNA in patients with uveal melanoma developing metastatic disease
Achberger, S., Aldrich, W. A., Tubbs, R., Crabb, J. W., Singh, A. D., & Triozzi, P. L. (2013) · Molecular Immunology · doi:10.1016/j.molimm.2013.11.018 · Cited by 114 · see citing works
Cancer cell dormancy: mechanisms and implications of cancer recurrence and metastasis
Gao, X., Zhang, M., Tang, Y., & Liang, X. (2017) · OncoTargets and Therapy · doi:10.2147/ott.s140854 · Cited by 113 · see citing works
Prospects for new lung cancer treatments that target EMT signaling
Otsuki, Y., Saya, H., & Arima, Y. (2017) · Developmental Dynamics · doi:10.1002/dvdy.24596 · Cited by 112 · see citing works
The EWS/FLI Oncogene Drives Changes in Cellular Morphology, Adhesion, and Migration in Ewing Sarcoma
Chaturvedi, A. P., Hoffman, L. M., Welm, A. L., Lessnick, S. L., & Beckerle, M. C. (2012) · Genes & Cancer · doi:10.1177/1947601912457024 · Cited by 112 · see citing works
ADAM8 expression in invasive breast cancer promotes tumor dissemination and metastasis
Romagnoli, M., Mineva, N. D., Polmear, M. M., Conrad, C., Srinivasan, S. S., Loussouarn, D., Barillé‐Nion, S., Georgakoudi, I., Dagg, Á., McDermott, E. W. M., et al. (2013) · EMBO Molecular Medicine · doi:10.1002/emmm.201303373 · Cited by 110 · see citing works
Regulation of Tumor Cell Dormancy by Tissue Microenvironments and Autophagy
Sosa, M. S., Bragado, P., Debnath, J., & Aguirre‐Ghiso, J. A. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-1445-2_5 · 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
Targeting dormant tumor cells to prevent cancer recurrence
Damen, M. P. F., van Rheenen, J., & Scheele, C. L. G. J. (2020) · FEBS Journal · doi:10.1111/febs.15626 · Cited by 108 · see citing works
Primary tumor-induced immunity eradicates disseminated tumor cells in syngeneic mouse model
Piranlioglu, R., Lee, E., Ouzounova, M., Bollag, R. J., Vinyard, A. H., Arbab, A. S., Marasco, D., Güzel, M., Cowell, J. K., Thangaraju, M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09015-1 · Cited by 107 · see citing works
Early tumor dissemination, but late metastasis: insights into tumor dormancy
Röcken, M. (2010) · Journal of Clinical Investigation · doi:10.1172/jci43424 · Cited by 101 · see citing works
- 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
- Health Sciences › Medicine › Psychiatry and Mental health › 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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