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Estrogen switches pure mucinous breast cancer to invasive lobular carcinoma with mucinous features

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Abstract

Mucinous breast cancer (MBC) is mainly a disease of postmenopausal women. Pure MBC is rare and augurs a good prognosis. In contrast, MBC mixed with other histological subtypes of invasive disease loses the more favorable prognosis. Because of the relative rarity of pure MBC, little is known about its cell and tumor biology and relationship to invasive disease of other subtypes. We have now developed a human breast cancer cell line called BCK4, in which we can control the behavior of MBC. BCK4 cells were derived from a patient whose poorly differentiated primary tumor was treated with chemotherapy, radiation and tamoxifen. Malignant cells from a recurrent pleural effusion were xenografted in mammary glands of a nude mouse. Cells from the solid tumor xenograft were propagated in culture to generate the BCK4 cell line. Multiple marker and chromosome analyses demonstrate that BCK4 cells are human, near diploid and luminal, expressing functional estrogen, androgen, and progesterone receptors. When xenografted back into immunocompromised cycling mice, BCK4 cells grow into small pure MBC. However, if mice are supplemented with continuous estradiol, tumors switch to invasive lobular carcinoma (ILC) with mucinous features (mixed MBC), and growth is markedly accelerated. Tamoxifen prevents the expansion of this more invasive component. The unexpected ability of estrogens to convert pure MBC into mixed MBC with ILC may explain the rarity of the pure disease in premenopausal women. These studies show that MBC can be derived from lobular precursors and that BCK4 cells are new, unique models to study the phenotypic plasticity, hormonal regulation, optimal therapeutic interventions, and metastatic patterns of MBC.

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Abbreviations

MBC:

Mucinous breast cancer

PR:

Progesterone receptor

ER:

Estrogen receptor

AR:

Androgen receptor

GR:

Glucocorticoid receptor

ILC:

Invasive lobular carcinoma

IDC:

Invasive ductal carcinoma

IDC NOS:

Invasive ductal carcinoma not otherwise specified

MBCPure :

Pure mucinous breast cancer

MBCMixed :

Mixed mucinous breast cancer

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Acknowledgments

These studies were supported by The Avon Foundation for Women (BMJ, KBH), NIH NCI CA026869, the National Foundation for Cancer Research, and the Breast Cancer Research Foundation (KBH). We are grateful to the University of Colorado Cancer Center Sequencing and Cytogenetics Core laboratories for technical support, to Dr. Hany Abdel-Hafiz for providing PCR primers for pS2 and CathD, and we thank Robert W. Burke for helpful discussions. All authors edited and approved the final manuscript.

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Division of Endocrinology, Department of Medicine, University of Colorado, Anschutz Medical Campus, Mail Stop 8106, Aurora, CO, 80045, USA

    Purevsuren Jambal, Melanie M. Badtke, Grace E. Sollender, Kathryn B. Horwitz & Britta M. Jacobsen

  2. Division of Medical Oncology, Department of Medicine, University of Colorado, Anschutz Medical Campus, Mail Stop 8117, Aurora, CO, 80045, USA

    Virginia F. Borges

  3. Department of Pathology, University of Colorado, Anschutz Medical Campus, Aurora, CO, 80045, USA

    Miriam D. Post & Kathryn B. Horwitz

  4. Department of Obstetrics and Gynecology, University of Colorado, Anschutz Medical Campus, Aurora, CO, 80045, USA

    Monique A. Spillman

  5. Department of Genetics, University of North Carolina, Chapel Hill, NC, 27599, USA

    J. Chuck Harrell

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  1. Purevsuren Jambal
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Correspondence to Britta M. Jacobsen.

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Jambal, P., Badtke, M.M., Harrell, J.C. et al. Estrogen switches pure mucinous breast cancer to invasive lobular carcinoma with mucinous features. Breast Cancer Res Treat 137, 431–448 (2013). https://doi.org/10.1007/s10549-012-2377-x

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