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Dynamic interactions between the extracellular matrix and estrogen activity in progression of ER+ breast cancer

Oncogene volume 38, pages 6913–6925 (2019)Cite this article

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Abstract

Metastatic, antiestrogen resistant estrogen receptor α positive (ER+) breast cancer is the leading cause of breast cancer deaths in USA women. While studies have demonstrated the importance of the stromal tumor microenvironment in cancer progression and therapeutic responses, effects on the responses of ER+ cancers to estrogen and antiestrogens are poorly understood, particularly in the complex in vivo environment. In this study, we used an estrogen responsive syngeneic mouse model to interrogate how a COL1A1-enriched fibrotic ECM modulates integrated hormonal responses in cancer progression. We orthotopically transplanted the ER+ TC11 cell line into wild-type (WT) or collagen-dense (Col1a1tm1Jae/+, mCol1a1) syngeneic FVB/N female mice. Once tumors were established, recipients were supplemented with 17β-estradiol (E2), tamoxifen, or left untreated. Although the dense/stiff environment in mCol1a1 recipients did not alter the rate of E2-induced proliferation of the primary tumor, it fostered the agonist activity of tamoxifen to increase proliferation and AP-1 activity. Manipulation of estrogen activity did not alter the incidence of lung lesions in either WT or mCol1a1 hosts. However, the mCol1a1 environment enabled tamoxifen-stimulated growth of pulmonary metastases and further fueled estrogen-driven growth. Moreover, E2 remodeled peritumoral ECM architecture in WT animals, modifying alignment of collagen fibers and altering synthesis of ECM components associated with increased alignment and stiffness, and increasing FN1 and POSTN expression in the pulmonary metastatic niche. These studies demonstrate dynamic interactions between ECM properties and estrogen activity in progression of ER+ breast cancer, and support the need for therapeutics that target both ER and the tumor microenvironment.

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Acknowledgements

We would like to thank Kyle Wegner for assistance with picrosirius red staining and image processing, and Ashley Weichmann in the UW Carbone Cancer Center Small Animal Imaging Facility for assistance with the tail vein injections. We are grateful to Dr Elaine Alarid for helpful discussions.

Funding

This work was supported by the National Institutes of Health [R01 CA157675 (LAS) and R01 CA179556 (LAS, SMP), T32 HD041921 and R25 GM083252 (FJ), and P30CA014520 (University of Wisconsin Carbone Cancer Center)], and funds from the UWCCC Breast Disease Oriented Team.

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  1. These authors contributed equally: Fatou Jallow, Kathleen A. O’Leary

Authors and Affiliations

  1. Department of Comparative Biosciences, University of Wisconsin-Madison, Madison, WI, USA

    Fatou Jallow, Kathleen A. O’Leary, Debra E. Rugowski & Linda A. Schuler

  2. Endocrinology-Reproductive Physiology Program, University of Wisconsin-Madison, Madison, WI, USA

    Fatou Jallow

  3. Department of Cell and Regenerative Biology, University of Wisconsin-Madison, Madison, WI, USA

    Jorge F. Guerrero & Suzanne M. Ponik

  4. University of Wisconsin Carbone Cancer Center, University of Wisconsin-Madison, Madison, WI, USA

    Suzanne M. Ponik & Linda A. Schuler

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Jallow, F., O’Leary, K.A., Rugowski, D.E. et al. Dynamic interactions between the extracellular matrix and estrogen activity in progression of ER+ breast cancer. Oncogene 38, 6913–6925 (2019). https://doi.org/10.1038/s41388-019-0941-0

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