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Mammary glands exhibit molecular laterality and undergo left–right asymmetric ductal epithelial growth in MMTV-cNeu mice*

Oncogene volume 34, pages 2003–2010 (2015)Cite this article

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Abstract

Significant left–right (L–R) differences in tumor incidence and disease outcome occur for cancers of paired organs, including the breasts; however, the basis for this laterality is unknown. Here, we show that despite their morphologic symmetry, left versus right mammary glands in wild-type mice have baseline differences in gene expression that are L–R independently regulated during pubertal development, including genes that regulate luminal progenitor cell renewal, luminal cell differentiation, mammary tumorigenesis, tamoxifen sensitivity and chemotherapeutic resistance. In MMTV-cNeuTg/Tg mice, which model HER2/Neu-amplified breast cancer, baseline L–R differences in mammary gene expression are amplified, sustained or inverted in a gene-specific manner and the mammary ductal epithelium undergoes L–R asymmetric growth and patterning. Comparative genomic analysis of mouse L–R mammary gene expression profiles with gene expression profiles of human breast tumors revealed significant linkage between right-sided gene expression and decreased breast cancer patient survival. Collectively, these findings are the first to demonstrate that mammary glands are lateralized organs, and, moreover, that mammary glands have L–R differential susceptibility to HER2/Neu oncogene-mediated effects on ductal epithelial growth and differentiation. We propose that intrinsic molecular laterality may have a role in L–R asymmetric breast tumor incidence and, furthermore, that interplay between the L–R molecular landscape and oncogene activity may contribute to the differential disease progression and patient outcome that are associated with tumor situs.

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Acknowledgements

We thank Dr Scott Argraves, Dr Jeremey Barth and Mr Victor Fresco of the MUSC Proteogenomics Facility for performing the DNA microarray and Dr Caroline Alexander and Dr Elizabeth Yeh for helpful discussion. This work was supported by National Institutes of Health K02HL086737 (AFR), R21HD068993 (AFR) and conducted in facilities supported, in part, by Cancer Center Support Grant P30CA138313 to the Hollings Cancer Center, MUSC.

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Authors and Affiliations

  1. Department of Regenerative Medicine and Cell Biology and Hollings Cancer Center, Medical University of South Carolina, Charleston, SC, USA

    J P Robichaux & A F Ramsdell

  2. Department of Biochemistry and Biomedical Sciences, Centre for Functional Genomics, McMaster University, Hamilton, ON, Canada,

    R M Hallett & J A Hassell

  3. Department of Cell Biology and Anatomy, School of Medicine, University of South Carolina, Columbia, SC, USA,

    J W Fuseler & A F Ramsdell

  4. Program In Women’s and Gender Studies, College of Arts and Sciences, University of South Carolina, Columbia, SC, USA

    A F Ramsdell

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  1. J P Robichaux
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Robichaux, J., Hallett, R., Fuseler, J. et al. Mammary glands exhibit molecular laterality and undergo left–right asymmetric ductal epithelial growth in MMTV-cNeu mice*. Oncogene 34, 2003–2010 (2015). https://doi.org/10.1038/onc.2014.149

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