3D collagen alignment limits protrusions to enhance breast cancer cell persistence
Open accessAbstract
Patients with mammographically dense breast tissue have a greatly increased risk of developing breast cancer. Dense breast tissue contains more stromal collagen, which contributes to increased matrix stiffness and alters normal cellular responses. Stromal collagen within and surrounding mammary tumors is frequently aligned and reoriented perpendicular to the tumor boundary. We have shown that aligned collagen predicts poor outcome in breast cancer patients, and postulate this is because it facilitates invasion by providing tracks on which cells migrate out of the tumor. However, the mechanisms by which alignment may promote migration are not understood. Here, we investigated the contribution of matrix stiffness and alignment to cell migration speed and persistence. Mechanical measurements of the stiffness of collagen matrices with varying density and alignment were compared with the results of a 3D microchannel alignment assay to quantify cell migration. We further interpreted the experimental results using a computational model of cell migration. We find that collagen alignment confers an increase in stiffness, but does not increase the speed of migrating cells. Instead, alignment enhances the efficiency of migration by increasing directional persistence and restricting protrusions along aligned fibers, resulting in a greater distance traveled. These results suggest that matrix topography, rather than stiffness, is the dominant feature by which an aligned matrix can enhance invasion through 3D collagen matrices.
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Alignment directs tumor invasion in hydrogels containing anisotropic structures generated by mechanical strain or by adding collagen-free tracks.
“it was recently demonstrated that alignment directs tumor invasion in hydrogels containing anisotropic structures”
From Cancer-on-chip models for metastasis: importance of the tumor microenvironment (2024) · cites this paper as [30]
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- Authors
- Riching, K. M., Cox, B. L., Salick, M. R., Pehlke, C., Riching, A. S., Ponik, S. M., Bass, B. R., Crone, W. C., Jiang, Y., Weaver, A. M., Eliceiri, K. W., & Keely, P. J.
- Affiliations
- University of Wisconsin–Madison (US)
- Georgia State University (US)
- Vanderbilt University Medical Center (US)
- Corresponding author
- Keely, Patricia J.
- ORCID
- Venue
- Biophysical Journal
- Publisher
- Elsevier BV
- Published
- 2014-12
- Volume
- 107
- Issue
- 11
- Pages
- 2546-2558
- ISSN
- 0006-3495 (ISSN-L)
- PMC
- PMC4255204
- OpenAlex
- W2082208320
- Cited by
- 446
- References
- 75
- Citations by year
- 2026: 15 · 2025: 39 · 2024: 33 · 2023: 34 · 2022: 47 · 2021: 55 · 2020: 59 · 2019: 40 · 2018: 39 · 2017: 39 · 2016: 32 · 2015: 13
- FWCI
- 13.94
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biophysical Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Archive @ GSU (submittedVersion, cc-by)
- Counseling And Psychological Services Dissertations (Georgia State University) (submittedVersion, cc-by)
- Funders
- National Cancer Institute (R01CA142833, R01CA114462, U01CA143069, P30CA014520)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Keywords
- collagen fiber alignment, breast cancer, cell migration, directional persistence, extracellular matrix stiffness, extracellular matrix topography, tumor invasion, dense breasts, 3D collagen matrix, cell protrusions
- MeSH terms
- Breast Neoplasms, Cell Movement, Collagen, Extracellular Matrix, Female, Gels, Humans, Models, Biological, Cell Line, Tumor
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 ›
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