Lung metastasis genes couple breast tumor size and metastatic spread
Open accessAbstract
The association between large tumor size and metastatic risk in a majority of clinical cancers has led to questions as to whether these observations are causally related or whether one is simply a marker for the other. This is partly due to an uncertainty about how metastasis-promoting gene expression changes can arise in primary tumors. We investigated this question through the analysis of a previously defined “lung metastasis gene-expression signature” (LMS) that mediates experimental breast cancer metastasis selectively to the lung and is expressed by primary human breast cancer with a high risk for developing lung metastasis. Experimentally, we demonstrate that the LMS promotes primary tumor growth that enriches for LMS + cells, and it allows for intravasation after reaching a critical tumor size. Clinically, this corresponds to LMS + tumors being larger at diagnosis compared with LMS − tumors and to a marked rise in the incidence of metastasis after LMS + tumors reach 2 cm. Patients with LMS-expressing primary tumors selectively fail in the lung compared with the bone or other visceral sites and have a worse overall survival. The mechanistic linkage between metastasis gene expression, accelerated tumor growth, and likelihood of metastatic recurrence provided by the LMS may help to explain observations of prognostic gene signatures in primary cancer and how tumor growth can both lead to metastasis and be a marker for cells destined to metastasize.
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?
CXCL1 expression is associated with lung relapse in breast tumors, including tumors not exposed to prior chemotherapy, and increases aggressiveness of circulating breast tumor cells.
“CXCL1 emerged among a set of genes whose expression is associated with lung relapse in breast tumors, including tumors that had not been exposed to prior chemotherapy (Minn et al., 2007; Minn et al., 2005), and as a gene that increases the aggressiveness of circulating breast tumor cells (Kim et al., 2009).”
From A CXCL1 Paracrine Network Links Cancer Chemoresistance and Metastasis (2012) · cites this paper as Minn et al., 2007
Cites
In silico prediction of protein-protein interactions in human macrophages
Souiai, O., Guerfali, F. Z., Miled, S. B., Brun, C., & Benkahla, A. (2014) · BMC Research Notes · doi:10.1186/1756-0500-7-157 · Cited by 10,785 · see citing works
Significance analysis of microarrays applied to the ionizing radiation response
Tusher, V. G., Tibshirani, R., & Chu, G. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091062498 · Cited by 10,568 · 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
A Gene-Expression Signature as a Predictor of Survival in Breast Cancer
van de Vijver, M. J., He, Y. D., Veer, L. V. ‘., Dai, H. A., Hart, A. A. M., Voskuil, D. W., Schreiber, G. J., Peterse, J. L., Roberts, C., Marton, M. J., et al. (2002) · New England Journal of Medicine · doi:10.1056/nejmoa021967 · Cited by 6,411 · see citing works
A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer.
Paik, S., Shak, S., Tang, G., Kim, C., Baker, J., Cronin, M., Baehner, F., Walker, M. G., Watson, D., Park, T., et al. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa041588 · Cited by 6,009 · see citing works
Repeated observation of breast tumor subtypes in independent gene expression data sets
Sørlie, T., Tibshirani, R. J., Parker, J. S., Hastie, T. J., Marron, J. S., Nobel, A. B., Deng, S., Johnsen, H., Pesich, R., Geisler, S. B., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0932692100 · Cited by 5,428 · see citing works
TM4: a free, open-source system for microarray data management and analysis
Saeed, A. I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M., et al. (2003) · BioTechniques · doi:10.2144/03342mt01 · Cited by 4,837 · see citing works
The pathogenesis of cancer metastasis: the ‘seed and soil’ hypothesis revisited
Fidler, I. J. (2003) · Nature Reviews Cancer · doi:10.1038/nrc1098 · Cited by 4,686 · see citing works
Dissemination and growth of cancer cells in metastatic sites
Chambers, A. F., Groom, A. C., & MacDonald, I. C. (2002) · Nature reviews. Cancer · doi:10.1038/nrc865 · Cited by 3,920 · see citing works
Genes that mediate breast cancer metastasis to lung
Minn, A. J., Gupta, G. P., Siegel, P. M., Bos, P. D., Shu, W., Giri, D. D., Viale, A., Olshen, A. B., Gerald, W. L., & Massagué, J. (2005) · Nature · doi:10.1038/nature03799 · Cited by 2,922 · see citing works
Self-citationGene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer
Wang, Y., Klijn, J. G. M., Zhang, Y., Sieuwerts, A. M., Look, M. P., Yang, F., Talantov, D., Timmermans, M. A. M., Gelder, M. E. M., Yu, J. X., et al. (2005) · The Lancet · doi:10.1016/s0140-6736(05)17947-1 · Cited by 2,848 · see citing works
Self-citationA multigenic program mediating breast cancer metastasis to bone
Kang, Y., Siegel, P. M., Shu, W., Drobnjak, M., Käkönen, S.-M., Cordon‐Cardo, C., Guise, T. A., & Massagué, J. (2003) · Cancer Cell · doi:10.1016/s1535-6108(03)00132-6 · Cited by 2,562 · see citing works
Self-citationA 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
Oncogenic pathway signatures in human cancers as a guide to targeted therapies
Bild, A., Yao, G., Chang, J. T., Wang, Q., Potti, A., Chasse, D. A. D., Joshi, M.-B., Harpole, D. H., Lancaster, J. M., Berchuck, A., et al. (2005) · Nature · doi:10.1038/nature04296 · Cited by 2,032 · see citing works
[9] TM4 Microarray Software Suite
Saeed, A. I., BHAGABATI, N. K., Braisted, J. C., Liang, W. P., Sharov, V., Howe, E., Li, J., Thiagarajan, M., White, J., & Quackenbush, J. F. (2006) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(06)11009-5 · Cited by 1,982 · see citing works
The molecular portraits of breast tumors are conserved across microarray platforms
Hu, Z., Fan, C., Oh, D. S., Marron, J. S., He, X., Qaqish, B. F., Livasy, C., Carey, L., Reynolds, E. R., Dressler, L. G., et al. (2006) · BMC Genomics · doi:10.1186/1471-2164-7-96 · Cited by 1,492 · see citing works
Concordance among Gene-Expression–Based Predictors for Breast Cancer
Fan, C., Oh, D. S., Wessels, L. F. A., Weigelt, B., Nuyten, D. S. A., Nobel, A. B., Veer, L. J. V., & Perou, C. M. (2006) · New England Journal of Medicine · doi:10.1056/nejmoa052933 · Cited by 1,338 · see citing works
Self-citationChang, H. Y., Nuyten, D. S. A., Sneddon, J. B., Hastie, T., Tibshirani, R., Sørlie, T., Dai, H., He, Y. D., van't Veer, L. J., Bartelink, H., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409462102 · Cited by 981 · see citing works
Self-citationMetastasis genes: A progression puzzle
Bernards, R., & Weinberg, R. A. (2002) · Nature · doi:10.1038/418823a · Cited by 801 · see citing works
Mediators of vascular remodelling co-opted for sequential steps in lung metastasis
Gupta, G. P., Nguyen, D. X., Chiang, A. C., Bos, P. D., Kim, J. Y., Nadal, C., Gomis, R. R., Manova-Todorova, K. O., & Massagué, J. (2007) · Nature · doi:10.1038/nature05760 · Cited by 728 · see citing works
Self-citationIs breast cancer survival improving?
Giordano, S. H., Buzdar, A. U., Smith, T. L., Kau, S., Yang, Y., & Hortobágyi, G. N. (2003) · Cancer · doi:10.1002/cncr.11859 · Cited by 541 · see citing works
Koscielny, S., Tubiana, M., Lê, M. G., Valleron, A., Mouriesse, H., Contesso, G., & Sarrazin, D. (1984) · British Journal of Cancer · doi:10.1038/bjc.1984.112 · Cited by 356 · see citing works
Genes Associated With Breast Cancer Metastatic to Bone
Smid, M., Wang, Y., Klijn, J. G. M., Sieuwerts, A. M., Zhang, Y., Atkins, D., Martens, J. W. M., & Foekens, J. A. (2006) · Journal of Clinical Oncology · doi:10.1200/jco.2005.03.8802 · Cited by 315 · see citing works
Self-citationGenetic regulators of large-scale transcriptional signatures in cancer
Adler, A. S., Lin, M., Horlings, H. M., Nuyten, D. S. A., van de Vijver, M. J., & Chang, H. Y. (2006) · Nature Genetics · doi:10.1038/ng1752 · Cited by 231 · see citing works
Self-citationPittman, J. L., Huang, E. S., Dressman, H. K., Horng, C., Cheng, S. H., Tsou, M.-H., Chen, C.-M., Bild, A., Iversen, E. S., Huang, A. T., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401736101 · Cited by 222 · see citing works
Sorting Out Breast-Cancer Gene Signatures
Massagué, J. (2007) · New England Journal of Medicine · doi:10.1056/nejme068292 · Cited by 127 · see citing works
Self-citationClinical Progression of Breast Cancer Malignant Behavior: What to Expect and When to Expect it
Heimann, R., & Hellmän, S. (2000) · Journal of Clinical Oncology · doi:10.1200/jco.2000.18.3.591 · Cited by 107 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Györffy, B., Lanczky, A., Eklund, A. C., Denkert, C., Budczies, J., Li, Q., & Szallasi, Z. (2010) · Breast Cancer Research and Treatment · doi:10.1007/s10549-009-0674-9 · Cited by 4,169 · see citing works
Microenvironmental regulation of metastasis
Joyce, J. A., & Pollard, J. W. (2009) · Nature Reviews Cancer · doi:10.1038/nrc2618 · Cited by 3,684 · 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
Self-citationCirculating Tumor Cell Clusters Are Oligoclonal Precursors of Breast Cancer Metastasis
Aceto, N., Bardia, A., Miyamoto, D. T., Collier, M. D., Wittner, B. S., Spencer, J. A., Yu, M., Pely, A., Engstrom, A., Zhu, H., et al. (2014) · Cell · doi:10.1016/j.cell.2014.07.013 · Cited by 2,438 · see citing works
Metastatic Behavior of Breast Cancer Subtypes
Kennecke, H., Yerushalmi, R., Woods, R., Cheang, M. C. U., Voduc, D., Speers, C. H., Nielsen, T. O., & Gelmon, K. (2010) · Journal of Clinical Oncology · doi:10.1200/jco.2009.25.9820 · Cited by 2,262 · see citing works
Genes that mediate breast cancer metastasis to the brain
Bos, P. D., Zhang, X. H.-F., Nadal, C., Shu, W., Gomis, R. R., Nguyen, D. X., Minn, A. J., van de Vijver, M. J., Gerald, W. L., Foekens, J. A., et al. (2009) · Nature · doi:10.1038/nature08021 · Cited by 1,863 · see citing works
Self-citationThe Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells
Cordenonsi, M., Zanconato, F., Azzolin, L., Forcato, M., Rosato, A., Frasson, C., Inui, M., Montagner, M., Parenti, A. R., Poletti, A., et al. (2011) · Cell · doi:10.1016/j.cell.2011.09.048 · Cited by 1,381 · see citing works
Tumor Self-Seeding by Circulating Cancer Cells
Kim, M.-Y., Oskarsson, T., Acharyya, S., Nguyen, D. X., Zhang, X. H.-F., Norton, L., & Massagué, J. (2009) · Cell · doi:10.1016/j.cell.2009.11.025 · Cited by 1,335 · see citing works
Self-citationThe metastatic niche: adapting the foreign soil
Psaila, B., & Lyden, D. C. (2009) · Nature reviews. Cancer · doi:10.1038/nrc2621 · Cited by 1,302 · see citing works
A CXCL1 Paracrine Network Links Cancer Chemoresistance and Metastasis
Acharyya, S., Oskarsson, T., Vanharanta, S., Malladi, S., Kim, J., Morris, P. G., Manova-Todorova, K., Leversha, M., Hogg, N., Seshan, V. E., et al. (2012) · Cell · doi:10.1016/j.cell.2012.04.042 · Cited by 1,085 · see citing works
Self-citationChiang, A. C., & Massagué, J. (2008) · New England Journal of Medicine · doi:10.1056/nejmra0805239 · Cited by 1,049 · see citing works
Self-citationTGFβ Primes Breast Tumors for Lung Metastasis Seeding through Angiopoietin-like 4
Padua, D. M., Zhang, X. H.-F., Wang, Q., Nadal, C., Gerald, W. L., Gomis, R. R., & Massagué, J. (2008) · Cell · doi:10.1016/j.cell.2008.01.046 · Cited by 947 · see citing works
Self-citationWeichselbaum, R. R., & Hellmän, S. (2011) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2011.44 · Cited by 947 · see citing works
Subtypes of Breast Cancer Show Preferential Site of Relapse
Smid, M., Wang, Y., Zhang, Y., Sieuwerts, A. M., Yu, J. X., Klijn, J. G. M., Foekens, J. A., & Martens, J. W. M. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-5644 · Cited by 817 · see citing works
Self-citationGenetic determinants of cancer metastasis
Nguyen, D. X., & Massagué, J. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2101 · Cited by 796 · see citing works
Self-citationTriple-negative breast cancer: disease entity or title of convenience?
Carey, L., Winer, E. P., Viale, G., Cameron, D., & Gianni, L. (2010) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2010.154 · Cited by 780 · see citing works
Progress in matrix metalloproteinase research
MURPHY, G., & Nagase, H. (2008) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2008.05.002 · Cited by 755 · see citing works
Charafe-Jauffret, E., Ginestier, C., Iovino, F., Tarpin, C., Diebel, M., Esterni, B., Houvenaeghel, G., Extra, J.-M., Bertucci, F., Jacquemier, J., et al. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-1630 · Cited by 732 · see citing works
Mediators of vascular remodelling co-opted for sequential steps in lung metastasis
Gupta, G. P., Nguyen, D. X., Chiang, A. C., Bos, P. D., Kim, J. Y., Nadal, C., Gomis, R. R., Manova-Todorova, K. O., & Massagué, J. (2007) · Nature · doi:10.1038/nature05760 · Cited by 728 · see citing works
Self-citationBreast cancer: origins and evolution
Polyák, K. (2007) · Journal of Clinical Investigation · doi:10.1172/jci33295 · Cited by 703 · see citing works
A MicroRNA Targeting Dicer for Metastasis Control
Martello, G., Rosato, A., Ferrari, F., Manfrin, A., Cordenonsi, M., Dupont, S., Enzo, E., Guzzardo, V., Rondina, M. B., Spruce, T., et al. (2010) · Cell · doi:10.1016/j.cell.2010.05.017 · Cited by 668 · see citing works
Xiao, Y., Cong, M., Li, J., He, D., Wu, Q., Tian, P., Wang, Y., Yang, S., Liang, C., Liang, Y., et al. (2021) · Cancer Cell · doi:10.1016/j.ccell.2020.12.012 · Cited by 654 · see citing works
Self-citationChen, Q., Zhang, X. H.-F., & Massagué, J. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.08.025 · Cited by 619 · see citing works
Self-citationVanharanta, S., & Massagué, J. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.09.007 · Cited by 563 · see citing works
Self-citationEyles, J., Puaux, A.-L., Wang, X., Toh, B., Prakash, C., Hong, M., Tan, T. G., Zheng, L., Ong, L. C., Jin, Y., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci42002 · Cited by 506 · see citing works
Rody, A., Holtrich, U., Pusztai, L., Liedtke, C., Gaetje, R., Ruckhaeberle, E., Solbach, C., Hanker, L., Ahr, A., Metzler, D., et al. (2009) · Breast Cancer Research · doi:10.1186/bcr2234 · Cited by 460 · see citing works
A SUMOylation-Dependent Transcriptional Subprogram Is Required for Myc-Driven Tumorigenesis
Kessler, J. D., Kahle, K. T., Sun, T., Meerbrey, K. L., Schlabach, M. R., Schmitt, E. M., Skinner, S. O., Xu, Q., Li, M. Z., Hartman, Z. C., et al. (2011) · Science · doi:10.1126/science.1212728 · Cited by 433 · see citing works
GOBO: Gene Expression-Based Outcome for Breast Cancer Online
Ringnér, M., Fredlund, E., Häkkinen, J., Borg, Å., & Staaf, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017911 · Cited by 421 · see citing works
Lou, E., Fujisawa, S., Morozov, A., Barlas, A., Romin, Y., Dogan, Y., Gholami, S., Moreira, A. L., Manova-Todorova, K., & Moore, M. A. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033093 · Cited by 420 · see citing works
Organotropism: new insights into molecular mechanisms of breast cancer metastasis
Chen, W., Hoffmann, A. D., Liu, H., & Liu, X. (2018) · npj Precision Oncology · doi:10.1038/s41698-018-0047-0 · Cited by 388 · see citing works
Extracellular matrix signatures of human mammary carcinoma identify novel metastasis promoters
Naba, A., Clauser, K. R., Lamar, J. M., Carr, S. A., & Hynes, R. O. (2014) · eLife · doi:10.7554/elife.01308 · Cited by 377 · see citing works
Breast cancer subtypes predict the preferential site of distant metastases: a SEER based study
Wu, Q., Li, J., Zhu, S., Wu, J., Chen, C., Liu, Q., Wei, W., Zhang, Y., & Sun, S. (2017) · Oncotarget · doi:10.18632/oncotarget.15856 · Cited by 357 · see citing works
Self-citationAnchorage-independent cell growth signature identifies tumors with metastatic potential
Mori, S., Chang, J. T., Andrechek, E. R., Matsumura, N., Baba, T., Yao, G., Kim, J., Gatza, M. L., Murphy, S. K., & Nevins, J. R. (2009) · Oncogene · doi:10.1038/onc.2009.139 · Cited by 346 · see citing works
A Three-Gene Model to Robustly Identify Breast Cancer Molecular Subtypes
Haibe‐Kains, B., Desmedt, C., Loi, S., Culhane, A. C., Bontempi, G., Quackenbush, J. F., & Sotiriou, C. P. (2012) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djr545 · Cited by 313 · see citing works
Clinical implications of cancer self-seeding
Comen, E. A., Norton, L., & Massagué, J. (2011) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2011.64 · Cited by 314 · see citing works
Self-citationDifferential effects on lung and bone metastasis of breast cancer by Wnt signalling inhibitor DKK1
Zhuang, X., Zhang, H., Li, X., Li, X., Cong, M., Peng, F., Yu, J., Zhang, X., Yang, Q., & Hu, G. (2017) · Nature Cell Biology · doi:10.1038/ncb3613 · Cited by 309 · see citing works
Transient regulatory T cell ablation deters oncogene-driven breast cancer and enhances radiotherapy
Bos, P. D., Plitas, G., Rudra, D., Lee, S. Y., & Rudensky, A. Y. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20130762 · Cited by 295 · see citing works
Self-citationPassing the Vascular Barrier: Endothelial Signaling Processes Controlling Extravasation
Wettschureck, N., Strilić, B., & Offermanns, S. (2019) · Physiological Reviews · doi:10.1152/physrev.00037.2018 · Cited by 282 · see citing works
Huang, R.-L., Teo, Z., Chong, H. C., Zhu, P., Tan, M., Tan, C. K., Lam, C. R. I., Sng, M. K., Leong, D. T., Tan, S., et al. (2011) · Blood · doi:10.1182/blood-2011-01-328716 · Cited by 284 · see citing works
Breast Cancer Subtypes Predispose the Site of Distant Metastases
Soni, A., Ren, Z., Hameed, O., Chanda, D., Morgan, C. J., Siegal, G. P., & Wei, S. (2015) · American Journal of Clinical Pathology · doi:10.1309/ajcpyo5fsv3upexs · Cited by 267 · see citing works
Breast Cancer Methylomes Establish an Epigenomic Foundation for Metastasis
Fang, F., Turcan, Ş., Rimner, A., Kaufman, A., Giri, D. D., Morris, L. G. T., Shen, R., Seshan, V., Mo, Q., Heguy, A., et al. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3001875 · Cited by 267 · see citing works
Self-citationHammerl, D., Martens, J. W. M., Timmermans, M., Smid, M., Trapman-Jansen, A. M., Foekens, R., Isaeva, O. I., Voorwerk, L., Balcioglu, H. E., Wijers, R., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25962-0 · Cited by 262 · see citing works
Wnt signaling in triple negative breast cancer is associated with metastasis
Dey, N., Barwick, B. G., Moreno, C. S., Ordanic-Kodani, M., Chen, Z., Oprea-Ilies, G. M., Tang, W., Catzavelos, C., Kerstann, K. F., Sledge, G. W., et al. (2013) · BMC Cancer · doi:10.1186/1471-2407-13-537 · Cited by 256 · see citing works
ID genes mediate tumor reinitiation during breast cancer lung metastasis
Gupta, G. P., Perk, J., Acharyya, S., de Candia, P., Mittal, V., Manova-Todorova, K., Gerald, W. L., Brogi, E., Benezra, R., & Massagué, J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709185104 · Cited by 242 · see citing works
Self-citationA Six-Gene Signature Predicts Survival of Patients with Localized Pancreatic Ductal Adenocarcinoma
Stratford, J. K., Bentrem, D. J., Anderson, J. M., Fan, C., Volmar, K. A., Marron, J. S., Routh, E. D., Caskey, L. S., Samuel, J. C., Der, C. J., et al. (2010) · PLoS Medicine · doi:10.1371/journal.pmed.1000307 · Cited by 243 · see citing works
Genomic analysis identifies unique signatures predictive of brain, lung, and liver relapse
Harrell, J. C., Prat, A., Parker, J. S., Fan, C., He, X., Carey, L., Anders, C. K., Ewend, M. G., & Perou, C. M. (2011) · Breast Cancer Research and Treatment · doi:10.1007/s10549-011-1619-7 · Cited by 228 · see citing works
Olmeda, D., Moreno‐Bueno, G., Flores, J. M., Fabra, À., Portillo, F., & Cano, A. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-2318 · Cited by 226 · see citing works
SIRT7 antagonizes TGF-β signaling and inhibits breast cancer metastasis
Tang, X., Shi, L., Xie, N., Liu, Z., Qian, M., Meng, F., Xu, Q.-Y., Zhou, M., Cao, X., Zhu, W., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00396-9 · Cited by 224 · see citing works
Jiang, Y., Qiu, Y. L., Minn, A. J., & Zhang, N. R. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1522203113 · Cited by 221 · see citing works
Self-citationYe, H., Zhou, Q., Zheng, S., Li, G., Lin, Q., Wei, L., Fu, Z., Zhang, B., Liu, Y., Li, Z., et al. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0486-0 · Cited by 217 · see citing works
The molecular profile of luminal B breast cancer
Creighton, C. J. (2012) · Biologics · doi:10.2147/btt.s29923 · Cited by 213 · see citing works
Yau, C. S. F., Esserman, L. J., Moore, D. H., Waldman, F., Sninsky, J. J., & Benz, C. C. (2010) · Breast Cancer Research · doi:10.1186/bcr2753 · Cited by 210 · see citing works
Signalling pathway for RKIP and Let‐7 regulates and predicts metastatic breast cancer
Yun, J., Frankenberger, C. A., Kuo, W.-L., Boelens, M. C., Eves, E. M., Cheng, N., Liang, H., Li, W., Ishwaran, H., Minn, A. J., et al. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.312 · Cited by 207 · see citing works
Self-citationEmerging Roles of Angiopoietin-like 4 in Human Cancer
Tan, M., Teo, Z., Sng, M. K., Zhu, P., & Tan, N. S. (2012) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-11-0519 · Cited by 197 · see citing works
Diverse matrix metalloproteinase functions regulate cancer amoeboid migration
Orgaz, J. L., Pandya, P., Dalmeida, R., Karagiannis, P., Sánchez‐Laorden, B. L., Virós, A., Albrengues, J., Nestle, F. O., Ridley, A. J., Gaggioli, C., et al. (2014) · Nature Communications · doi:10.1038/ncomms5255 · Cited by 193 · see citing works
An Integrated Genomic Screen Identifies LDHB as an Essential Gene for Triple-Negative Breast Cancer
McCleland, M. L., Adler, A. S., Shang, Y., Hunsaker, T., Truong, T., Peterson, D., Torres, E., Li, L., Haley, B., Stéphan, J.-P., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-1098 · Cited by 192 · see citing works
Cheng, Q., Chang, J. T., Geradts, J., Neckers, L. Μ., Haystead, T., Spector, N. L., & Lyerly, H. K. (2012) · Breast Cancer Research · doi:10.1186/bcr3168 · Cited by 185 · see citing works
Circulating Tumor Cell Phenotyping via High‐Throughput Acoustic Separation
Wu, M., Huang, P., Zhang, R., Mao, Z., Chen, C., Kemeny, G., Li, P., Lee, A. V., Gyanchandani, R., Armstrong, A. J., et al. (2018) · Small · doi:10.1002/smll.201801131 · Cited by 176 · see citing works
A Six-Gene Signature Predicting Breast Cancer Lung Metastasis
Landemaine, T., Jackson, A. M., Bellahcène, A., Rucci, N., Sin, S., Martín, B., Sierra, À., Boudinet, A., Guinebretière, J., Ricevuto, E., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0436 · Cited by 169 · see citing works
Minireview: Basal-Like Breast Cancer: From Molecular Profiles to Targeted Therapies
Toft, D. J., & Cryns, V. L. (2010) · Molecular Endocrinology · doi:10.1210/me.2010-0164 · Cited by 160 · see citing works
Cancer-associated fibroblast-derived Gremlin 1 promotes breast cancer progression
Ren, J., Smid, M., Iaria, J., Salvatori, D. C. F., van Dam, H., Zhu, H., Martens, J. W. M., & ten Dijke, P. (2019) · Breast Cancer Research · doi:10.1186/s13058-019-1194-0 · Cited by 160 · see citing works
Sims, A. H., Smethurst, G. J., Hey, Y., Okoniewski, M. J., Pepper, S. D. V., Howell, A., Miller, C. J., & Clarke, R. B. (2008) · BMC Medical Genomics · doi:10.1186/1755-8794-1-42 · Cited by 159 · see citing works
Wu, C., Andzinski, L., Kasnitz, N., Kröger, A., Klawonn, F., Lienenklaus, S., Weiß, S., & Jabłońska, J. (2015) · International Journal of Cancer · doi:10.1002/ijc.29444 · Cited by 150 · see citing works
Notch promotes recurrence of dormant tumor cells following HER2/neu-targeted therapy
Abravanel, D. L., Belka, G. K., Pan, T.-C., Pant, D. K., Collins, M. A., Sterner, C. J., & Chodosh, L. A. (2015) · Journal of Clinical Investigation · doi:10.1172/jci74883 · Cited by 147 · see citing works
Peng, J., Bera, R., Chiou, C., Yu, M., Chen, T., Chen, C., Wang, T.-H., Chiang, W., Chai, S., Wei, Y., et al. (2017) · Hepatology · doi:10.1002/hep.29678 · Cited by 147 · see citing works
Mammary tumor growth and pulmonary metastasis are enhanced in a hyperlipidemic mouse model
Alikhani, N., Ferguson, R. D., Novosyadlyy, R., Gallagher, E. J., Scheinman, E. J., Yakar, S., & LeRoith, D. (2013) · Oncogene · doi:10.1038/onc.2012.113 · Cited by 146 · see citing works
Thyroid Hormone Receptor β1 Acts as a Potent Suppressor of Tumor Invasiveness and Metastasis
Martínez-Iglesias, O. A., Garcı́a-Silva, S., Tenbaum, S. P., Regadera, J., Larcher, F., Paramio, J. M., Vennström, B., & Aranda, A. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-2198 · Cited by 143 · see citing works
Fayard, B., Bianchi, F., Dey, J. H., Moreno, E., Djaffer, S., Hynes, N. E., & Monard, D. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-4573 · Cited by 142 · see citing works
Mandal, C. C., Ghosh-Choudhury, N., Yoneda, T., Choudhury, G. G., & Ghosh-Choudhury, N. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.193714 · Cited by 138 · see citing works
Breast cancer stem cells: tools and models to rely on
Charafe‐Jauffret, E., Ginestier, C., & Birnbaum, D. (2009) · BMC Cancer · doi:10.1186/1471-2407-9-202 · Cited by 131 · see citing works
Breast cancer metastasis: Putative therapeutic role of vascular cell adhesion molecule-1
Sharma, R., Sharma, R., Khaket, T. P., Dutta, C., Chakraborty, B., & Mukherjee, T. K. (2017) · Cellular Oncology · doi:10.1007/s13402-017-0324-x · Cited by 132 · see citing works
The Fragile X Protein binds mRNAs involved in cancer progression and modulates metastasis formation
Lucà, R., Averna, M., Zalfa, F., Vecchi, M., Bianchi, F., Fata, G. L., Nonno, F. D., Nardacci, R., Bianchi, M., Nuciforo, P. G., et al. (2013) · EMBO Molecular Medicine · doi:10.1002/emmm.201302847 · Cited by 131 · see citing works
Hepatic Resection or Ablation for Isolated Breast Cancer Liver Metastasis
Sadot, E., Lee, S. Y., Sofocleous, C. T., Solomon, S. B., Gönen, M., Kingham, T. P., Allen, P. J., DeMatteo, R. P., Jarnagin, W. R., Hudis, C. A., et al. (2015) · Annals of Surgery · doi:10.1097/sla.0000000000001371 · Cited by 131 · see citing works
Arg/Abl2 promotes invasion and attenuates proliferation of breast cancer in vivo
Gil-Henn, H., Patsialou, A., Wang, Y., Warren, M. S., Condeelis, J. S., & Koleske, A. J. (2012) · Oncogene · doi:10.1038/onc.2012.284 · Cited by 126 · see citing works
Self-citationBreast cancer metastases are molecularly distinct from their primary tumors
Vecchi, M., Confalonieri, S., Nuciforo, P. G., Viganò, M., Capra, M. C., Bianchi, M., Nicosia, D., Bianchi, F., Galimberti, V. E., Viale, G., et al. (2007) · Oncogene · doi:10.1038/sj.onc.1210858 · Cited by 125 · see citing works
Transforming growth factor-β signaling: emerging stem cell target in metastatic breast cancer?
Tan, A. R., Alexe, G., & Reiß, M. (2008) · Breast Cancer Research and Treatment · doi:10.1007/s10549-008-0184-1 · Cited by 124 · see citing works
Role of Cannabinoid Receptor CB2 in HER2 Pro-oncogenic Signaling in Breast Cancer
Pérez-Gómez, E., Andradas, C., Blasco-Benito, S., Caffarel, M. M., García-Taboada, E., Villa‐Morales, M., Moreno, E., Hamann, S., Martín-Villar, E., Flores, J. M., et al. (2015) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djv077 · Cited by 121 · see citing works
Role of the CXCR4/CXCL12 signaling axis in breast cancer metastasis to the brain
Hinton, C. V., Avraham, S., & Avraham, H. K. (2008) · Clinical & Experimental Metastasis · doi:10.1007/s10585-008-9210-2 · Cited by 119 · see citing works
Relationships between LDH-A, Lactate, and Metastases in 4T1 Breast Tumors
Rizwan, A., Serganova, I. S., Khanin, R., Karabeber, H., Ni, X., Thakur, S. B., Zakian, K. L., Blasberg, R. G., & Koutcher, J. A. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-3300 · Cited by 118 · see citing works
LDH-A regulates the tumor microenvironment via HIF-signaling and modulates the immune response
Serganova, I. S., Cohen, I., Vemuri, K., Shindo, M., Maeda, M., Mane, M. M., Moroz, E., Khanin, R., Satagopan, J. M., Koutcher, J. A., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0203965 · Cited by 118 · see citing works
Histone Demethylase RBP2 Is Critical for Breast Cancer Progression and Metastasis
Cao, J. P., Liu, Z. Z., Cheung, W. K. C., Zhao, M., Chen, S. Y., Chan, S. W., Booth, C. J., Nguyen, D. X., & Yan, Q. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.02.004 · Cited by 115 · see citing works
Self-citationInsua‐Rodríguez, J., Pein, M., Hongu, T., Meier, J., Descot, A., Lowy, C., Braekeleer, E. D., Sinn, H., Spaich, S., Sütterlin, M., et al. (2018) · EMBO Molecular Medicine · doi:10.15252/emmm.201809003 · Cited by 111 · see citing works
New and Paradoxical Roles of Matrix Metalloproteinases in the Tumor Microenvironment
Noël, A., Gutiérrez‐Fernández, A., Sounni, N. E., Behrendt, N., Maquoi, E., Lund, I. K., Cal, S., Høyer‐Hansen, G., & López-Otı́n, C. (2012) · Frontiers in Pharmacology · doi:10.3389/fphar.2012.00140 · Cited by 110 · see citing works
Understanding the role of stromal fibroblasts in cancer progression
Tripathi, M., Billet, S., & Bhowmick, N. A. (2012) · Cell Adhesion & Migration · doi:10.4161/cam.20419 · Cited by 108 · see citing works
Stresing, V., Baltziskueta, E., Rubio, N., Blanco, J., de Arriba, M., Valls, J., Janier, M. F., Clézardin, P., Pamplona, R. S., Nieva, C., et al. (2012) · Oncogene · doi:10.1038/onc.2012.93 · Cited by 107 · see citing works
Song, K.-H., Park, M. S., Nandu, T. S., Gadad, S. S., Kim, S.-C., & Kim, M. (2016) · Nature Communications · doi:10.1038/ncomms13796 · Cited by 106 · see citing works
Thyroid receptor: roles in cancer
Aranda, A., Martínez-Iglesias, O. A., Ruiz-Llorente, L., García-Carpizo, V., & Zambrano, A. (2009) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2009.03.011 · Cited by 103 · see citing works
Ruckhäberle, E., Karn, T., Rody, A., Hanker, L., Gätje, R., Metzler, D., Holtrich, U., & Kaufmann, M. (2009) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-008-0536-6 · Cited by 102 · see citing works
RKIP and HMGA2 regulate breast tumor survival and metastasis through lysyl oxidase and syndecan-2
Sun, M., Gomes, S. C. V., Chen, P. B., Frankenberger, C. A., Sankarasharma, D., Chung, C. H., Chada, K. K., & Rosner, M. R. (2013) · Oncogene · doi:10.1038/onc.2013.328 · Cited by 100 · see citing works
A novel gene expression signature for bone metastasis in breast carcinomas
Savci-Heijink, C. D., Halfwerk, H., Köster, J., & van de Vijver, M. J. (2016) · Breast Cancer Research and Treatment · doi:10.1007/s10549-016-3741-z · Cited by 98 · see citing works
Cytokine Regulation of Metastasis and Tumorigenicity
Yao, M., Brummer, G., Acevedo, D. S., & Cheng, N. (2016) · Advances in cancer research · doi:10.1016/bs.acr.2016.05.005 · Cited by 96 · see citing works
Cross-study validation for the assessment of prediction algorithms
Bernau, C., Riester, M., Boulesteix, A., Parmigiani, G., Huttenhower, C., Waldron, L., & Trippa, L. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu279 · Cited by 95 · see citing works
Role of the Focal Adhesion Protein Kindlin-1 in Breast Cancer Growth and Lung Metastasis
Sin, S., Bonin, F., Petit, V., Meseure, D., Lallemand, F., Bièche, I., Bellahcène, A., Castronovo, V., Wever, O. D., Gespach, C. P., et al. (2011) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djr290 · Cited by 91 · see citing works
Cancer biology as revealed by the research autopsy
Iacobuzio–Donahue, C. A., Michael, C., Baez, P., Kappagantula, R. L., Hooper, J. E., & Hollman, T. J. (2019) · Nature reviews. Cancer · doi:10.1038/s41568-019-0199-4 · Cited by 89 · see citing works
Ömürlü, İ. K., Türe, M., & Tokatlı, F. (2008) · Expert Systems with Applications · doi:10.1016/j.eswa.2008.10.023 · Cited by 87 · see citing works
Fan, L., Lei, H., Zhang, S., Peng, Y., Fu, C., Shu, G., & Yin, G. (2020) · Theranostics · doi:10.7150/thno.43198 · Cited by 86 · see citing works
Hypothyroidism Enhances Tumor Invasiveness and Metastasis Development
Martínez-Iglesias, O. A., Garcı́a-Silva, S., Regadera, J., & Aranda, A. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006428 · Cited by 86 · see citing works
Activation of Notch Signaling in a Xenograft Model of Brain Metastasis
Nam, D., Jeon, H.-M., Kim, S., Kim, M., Lee, Y.-J., Lee, M. S., Kim, H., Joo, K. M., Lee, D., Price, J. E., et al. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-4039 · Cited by 86 · see citing works
Ceramide Kinase Promotes Tumor Cell Survival and Mammary Tumor Recurrence
Payne, A. W., Pant, D. K., Pan, T.-C., & Chodosh, L. A. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-1292 · Cited by 85 · see citing works
Albini, A., Mirisola, V., & Pfeffer, U. (2007) · Cancer and Metastasis Reviews · doi:10.1007/s10555-007-9111-x · Cited by 82 · see citing works
- Authors
- Minn, A. J., Gupta, G. P., Padua, D., Bos, P., Nguyen, D. X., Nuyten, D., Kreike, B., Zhang, Y., Wang, Y., Ishwaran, H., Foekens, J. A., van de Vijver, M., & Massagué, J.
- Affiliations
- University of Chicago (US)
- Memorial Sloan Kettering Cancer Center (US)
- The Netherlands Cancer Institute (NL)
- Johnson & Johnson (United States) (US)
- Cleveland Clinic (US)
- Erasmus MC (NL)
- **Department of Diagnostic Oncology, The Netherlands Cancer Institute, 1066 CX, Amsterdam, The Netherlands;
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2007-04-17
- Volume
- 104
- Issue
- 16
- Pages
- 6740-6745
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC1871856
- OpenAlex
- W2021880490
- Cited by
- 400
- References
- 27
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 3 · 2023: 25 · 2022: 10 · 2021: 32 · 2020: 16 · 2019: 12 · 2018: 19 · 2017: 16 · 2016: 22 · 2015: 22 · 2014: 29 · 2013: 24 · 2012: 28
- FWCI
- 14.46
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- Funders
- U.S. Public Health Service (P01-94060)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mechanisms of cancer metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Breast Cancer Treatment Studies
- Keywords
- breast cancer, lung metastasis, tumor size, primary tumor growth, intravasation, prognostic gene signature, distant recurrence, overall survival, tumor microenvironment
- MeSH terms
- Animals, Breast Neoplasms, Female, Humans, Lung Neoplasms, Mammary Neoplasms, Experimental, Gene Expression Regulation, Neoplastic, Cell Line, Tumor, Mice
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
