Genes that mediate breast cancer metastasis to the brain
Open accessAbstract
The molecular basis for breast cancer metastasis to the brain is largely unknown. Brain relapse typically occurs years after the removal of a breast tumour, suggesting that disseminated cancer cells must acquire specialized functions to take over this organ. Here we show that breast cancer metastasis to the brain involves mediators of extravasation through non-fenestrated capillaries, complemented by specific enhancers of blood-brain barrier crossing and brain colonization. We isolated cells that preferentially infiltrate the brain from patients with advanced disease. Gene expression analysis of these cells and of clinical samples, coupled with functional analysis, identified the cyclooxygenase COX2 (also known as PTGS2), the epidermal growth factor receptor (EGFR) ligand HBEGF, and the alpha2,6-sialyltransferase ST6GALNAC5 as mediators of cancer cell passage through the blood-brain barrier. EGFR ligands and COX2 were previously linked to breast cancer infiltration of the lungs, but not the bones or liver, suggesting a sharing of these mediators in cerebral and pulmonary metastases. In contrast, ST6GALNAC5 specifically mediates brain metastasis. Normally restricted to the brain, the expression of ST6GALNAC5 in breast cancer cells enhances their adhesion to brain endothelial cells and their passage through the blood-brain barrier. This co-option of a brain sialyltransferase highlights the role of cell-surface glycosylation in organ-specific metastatic interactions.
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Both TLR4 and RAGE are expressed in breast cancer cells.
“Both TLR4 and RAGE are expressed in breast cancer cells (Bos et al., 2009; Hsieh et al., 2003).”
From A CXCL1 Paracrine Network Links Cancer Chemoresistance and Metastasis (2012) · cites this paper as Bos et al., 2009
To cross the BBB, tumor cells bind endothelial cells and disrupt their tight junctions, and melanoma cells adhere to and disturb the interaction of brain endothelial cells through a disruption of tight and adherence junction proteins such as Claudin 5 and ZO-1.
“To cross the BBB, tumor cells bind endothelial cells and disrupt their tight junctions”
From Living on the Edge of the CNS: Meninges Cell Diversity in Health and Disease (2021) · cites this paper as Bos et al., 2009
Breast cancer cells express ST6GALNAC5, which is normally exclusively expressed in the brain, allowing for increased adhesion to brain endothelial cells to pass through the BBB, and acute lymphoblastic leukemia cells access the CNS via vascular channels that exist between bone marrow located in the vertebral and calvarium bone and the meninges.
“breast cancer cells express ST6GALNAC5, which is normally exclusively expressed in the brain, allowing for increased adhesion to brain endothelial cells to pass through the BBB”
From Living on the Edge of the CNS: Meninges Cell Diversity in Health and Disease (2021) · cites this paper as Bos et al., 2009
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The CCL2-CCR2 astrocyte-cancer cell axis in tumor extravasation at the brain
Hajal, C., Shin, Y., Li, L., Serrano, J. C., Jacks, T., & Kamm, R. D. (2021) · Science Advances · doi:10.1126/sciadv.abg8139 · Cited by 69 · see citing works
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Identification of synergistic drug combinations using breast cancer patient-derived xenografts
Turner, T. H., Alzubi, M. A., & Harrell, J. C. (2020) · Scientific Reports · doi:10.1038/s41598-020-58438-0 · Cited by 50 · see citing works
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Patient-derived models of brain metastases recapitulate human disseminated disease
Faria, C. C., Cascão, R., Custódia, C., Paisana, E., Carvalho, T., Pereira, P., Roque, R., Pimentel, J., Miguéns, J., Cortes-Ciriano, I., et al. (2022) · Cell Reports Medicine · doi:10.1016/j.xcrm.2022.100623 · Cited by 15 · see citing works
- Authors
- 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., & Massagué, J.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- University of Chicago (US)
- Erasmus MC (NL)
- Corresponding author
- Massagué, Joan
- Venue
- Nature
- Published
- 2009-05-06
- Volume
- 459
- Issue
- 7249
- Pages
- 1005-1009
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2698953
- OpenAlex
- W2057151160
- Cited by
- 1,863
- References
- 35
- Citations by year
- 2026: 58 · 2025: 78 · 2024: 73 · 2023: 149 · 2022: 98 · 2021: 134 · 2020: 122 · 2019: 118 · 2018: 100 · 2017: 130 · 2016: 115 · 2015: 118 · 2014: 104 · 2013: 140 · 2012: 125
- FWCI
- 90.88
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Pure Amsterdam UMC (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- Robert J. Kleberg, Jr. and Helen C. Kleberg Foundation
- National Institutes of Health
- National Cancer Institute (U54CA126518, P30CA008748)
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Brain Metastases and Treatment
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mechanisms of cancer metastasis
- Keywords
- breast cancer brain metastasis, blood-brain barrier penetration, alpha-2,6-sialyltransferase, cyclooxygenase-2, HB-EGF, EGFR ligands, cell surface glycosylation, organ-specific metastasis, lung metastasis
- MeSH terms
- Animals, Blood-Brain Barrier, Brain, Brain Neoplasms, Breast Neoplasms, Humans, Neoplasm Metastasis, Organ Specificity, Sialyltransferases, Gene Expression Regulation, Neoplastic, Gene Expression Profiling, Intercellular Signaling Peptides and Proteins, Cell Line, Tumor, Mice, Cyclooxygenase 2, ErbB Receptors, Heparin-binding EGF-like Growth Factor
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