Cited by 400Cancer Cells and MetastasisMechanisms of cancer metastasisBreast Cancer Treatment Studies

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Lung metastasis genes couple breast tumor size and metastatic spread

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Minn, Andy J., Gupta, Gaorav P., Padua, David, Bos, Paula, Nguyen, Don X., Nuyten, Dimitry, Kreike, Bas, Zhang, Yi, Wang, Yixin, Ishwaran, Hemant, Foekens, John A., van de Vijver, Marc, Massagué, Joan·2007·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.0701138104PMC PMC1871856

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Abstract

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.

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Tanabe, A., Ndzinu, J., & Sahara, H. (2025) · Cancer Treatment and Research Communications · doi:10.1016/j.ctarc.2025.101046
Additional file 10 of Cellular dormancy in minimal residual disease following targeted therapy
Ruth, J. R., Pant, D. K., Pan, T.-C., Seidel, H. E., Baksh, S. C., Keister, B. A., Singh, R., Sterner, C. J., Bakewell, S. J., Moody, S. E., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14737017
Additional file 7 of Cellular dormancy in minimal residual disease following targeted therapy
Ruth, J. R., Pant, D. K., Pan, T.-C., Seidel, H. E., Baksh, S. C., Keister, B. A., Singh, R., Sterner, C. J., Bakewell, S. J., Moody, S. E., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14737041
Additional file 6 of Cellular dormancy in minimal residual disease following targeted therapy
Ruth, J. R., Pant, D. K., Pan, T.-C., Seidel, H. E., Baksh, S. C., Keister, B. A., Singh, R., Sterner, C. J., Bakewell, S. J., Moody, S. E., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14737038
Additional file 1 of Cellular dormancy in minimal residual disease following targeted therapy
Ruth, J. R., Pant, D. K., Pan, T.-C., Seidel, H. E., Baksh, S. C., Keister, B. A., Singh, R., Sterner, C. J., Bakewell, S. J., Moody, S. E., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14737023
Additional file 5 of Cellular dormancy in minimal residual disease following targeted therapy
Ruth, J. R., Pant, D. K., Pan, T.-C., Seidel, H. E., Baksh, S. C., Keister, B. A., Singh, R., Sterner, C. J., Bakewell, S. J., Moody, S. E., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14737035
Additional file 8 of Cellular dormancy in minimal residual disease following targeted therapy
Ruth, J. R., Pant, D. K., Pan, T.-C., Seidel, H. E., Baksh, S. C., Keister, B. A., Singh, R., Sterner, C. J., Bakewell, S. J., Moody, S. E., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14737044
Additional file 4 of Cellular dormancy in minimal residual disease following targeted therapy
Ruth, J. R., Pant, D. K., Pan, T.-C., Seidel, H. E., Baksh, S. C., Keister, B. A., Singh, R., Sterner, C. J., Bakewell, S. J., Moody, S. E., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14737032
Additional file 3 of Cellular dormancy in minimal residual disease following targeted therapy
Ruth, J. R., Pant, D. K., Pan, T.-C., Seidel, H. E., Baksh, S. C., Keister, B. A., Singh, R., Sterner, C. J., Bakewell, S. J., Moody, S. E., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14737029
Additional file 1 of Transforming growth factor-induced gene TGFBI is correlated with the prognosis and immune infiltrations of breast cancer
Wang, H., Wang, X., & Xu, L. (2024) · Figshare · doi:10.6084/m9.figshare.25036221
Additional file 11 of Cellular dormancy in minimal residual disease following targeted therapy
Ruth, J. R., Pant, D. K., Pan, T.-C., Seidel, H. E., Baksh, S. C., Keister, B. A., Singh, R., Sterner, C. J., Bakewell, S. J., Moody, S. E., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14737020
Additional file 1 of LTBP1 promotes esophageal squamous cell carcinoma progression through epithelial-mesenchymal transition and cancer-associated fibroblasts transformation
Cai, R., Wang, P., Zhao, X., Lu, X., Deng, R., Wang, X., Su, Z., Hong, C., & Lin, J. (2020) · Figshare · doi:10.6084/m9.figshare.12038061
Additional file 9 of Cellular dormancy in minimal residual disease following targeted therapy
Ruth, J. R., Pant, D. K., Pan, T.-C., Seidel, H. E., Baksh, S. C., Keister, B. A., Singh, R., Sterner, C. J., Bakewell, S. J., Moody, S. E., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14737047
Additional file 2 of Cellular dormancy in minimal residual disease following targeted therapy
Ruth, J. R., Pant, D. K., Pan, T.-C., Seidel, H. E., Baksh, S. C., Keister, B. A., Singh, R., Sterner, C. J., Bakewell, S. J., Moody, S. E., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14737026
Robust Association of Breast Cancer Co-morbidity Using Subtype-specific Expressed Genes
Gupta, M., Verma, S., Rao, S., & Kumar, R. (2026) · Current Drug Targets · doi:10.2174/0113894501450605260121095416
Réactivation des gènes embryonnaires twist et snai3 et dissémination précoce des cellules cancéreuses
Bastid, J. (2009) · theses.fr (ABES) · doi:10.70675/1f08a215z4b9cz4886z8897z7926d12b1bff
Caractérisation des altérations moléculaires dans le cancer du sein inflammatoire
Manai, M. (2016) · doi:10.70675/af0aed36z2300z49f5z8dbcz639db7e53fd1
Developing a prediction model to predict the incidence of metastasis in lung cancer patients using artificial intelligence techniques
Gharabaghi, M. A., & Gholamzadeh, M. (2026) · BMC Pulmonary Medicine · doi:10.1186/s12890-026-04530-6
Genes that mediate breast cancer metastasis to the brain
Bos, P., Zhang, X., Nadal, C., Shu, W., Gomis, R., Nguyen, D., Minn, A. J., van de Vijver, M. J., Wl, G., Foekens, J., et al. (2009) · EUR Research Repository (Erasmus University Rotterdam)
Self-citation
Stress Biology in Cancer: Neuroendocrine–Immune Mechanisms Linking Tumor Progression to Translational Interventions
Ma, C., Ma, C., Xing, X., Sun, C., Guan, L., Schiöth, H. B., & Liu, W. (2026) · 癌症：英文版 · doi:10.34133/cancomm.0053
Integrating the molecular subtypes of breast cancer into a novel prognostic model
Haibe‐Kains, B., Desmedt, C., Rothé, F., Piccart, M. J., Bontempi, G., & Sotiriou, C. P. (2009) · Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles)
Computational Methods for Breast Cancer Diagnosis, Prognosis, and Treatment Prediction
Saini, A. K. (2014)
Examining the Functional Consequences of Tumor Endothelial Marker 8 (TEM8) Expression in Human Breast Cancer Cells
Sampson, E. (2014) · Libraries and Cultural Resources (University of Calgary) · doi:10.11575/prism/26027

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: Minn, Andy J.
Gupta, Gaorav P.
Padua, David
Bos, Paula
Nguyen, Don X.
Kreike, Bas
Zhang, Yi
Wang, Yixin
Ishwaran, Hemant
Massagué, Joan
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
DOI: 10.1073/pnas.0701138104
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

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Lung metastasis genes couple breast tumor size and metastatic spread

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