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The DEK oncogene promotes cellular proliferation through paracrine Wnt signaling in Ron receptor-positive breast cancers

Oncogene volume 34, pages 2325–2336 (2015)Cite this article

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Abstract

Disease progression and recurrence are major barriers to survival for breast cancer patients. Understanding the etiology of recurrent or metastatic breast cancer and underlying mechanisms is critical for the development of new treatments and improved survival. Here, we report that two commonly overexpressed breast cancer oncogenes, Ron (Recepteur d’Origine Nantaise) and DEK, cooperate to promote advanced disease through multipronged effects on β-catenin signaling. The Ron receptor is commonly activated in breast cancers, and Ron overexpression in human disease stimulates β-catenin nuclear translocation and is an independent predictor of metastatic dissemination. Dek is a chromatin-associated oncogene whose expression has been linked to cancer through multiple mechanisms, including β-catenin activity. We demonstrate here that Dek is a downstream target of Ron receptor activation in murine and human models. The absence of Dek in the MMTV-Ron mouse model led to a significant delay in tumor development, characterized by decreased cell proliferation, diminished metastasis and fewer cells expressing mammary cancer stem cell markers. Dek complementation of cell lines established from this model was sufficient to promote cellular growth and invasion. Mechanistically, Dek expression stimulated the production and secretion of Wnt ligands to sustain an autocrine/paracrine canonical β-catenin signaling loop. Finally, we show that Dek overexpression promotes tumorigenic phenotypes in immortalized human mammary epithelial MCF10A cells and, in the context of Ron receptor activation, correlates with disease recurrence and metastasis in patients. Overall, our studies demonstrate that DEK overexpression, due in part to Ron receptor activation, drives breast cancer progression through the induction of Wnt/β-catenin signaling.

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Acknowledgements

We acknowledge James Lessard and Gerard Grosveld for reagents, Kathryn Wikenheiser-Brokamp for technical assistance and the Research Flow Cytometry Core at Cincinnati Children’s, supported by NIH AR-47363. LMPV is supported by the Ride Cincinnati Foundation for Breast Cancer Research in honor of Marlene Harris and Public Health Service Grants F32CA139931, T32HL091805 and K12HD051953. Funding also was provided by Public Health Services Grants R01CA116316 (SIW), R01HL875109 (JAC), T32ES007250 (AKA), T32CA117846-07 (PKW) and T32CA11784 (SEW and NMB), Department of Defense Grant W81XWH-12-1-0194 (SIW and SEW) and the Veteran’s Administration Grant BX000803 (SEW). JS-W is supported by the Government of the Spanish Junta de Andalucia.

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Authors and Affiliations

  1. Division of Oncology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA

    L M Privette Vinnedge, N A Pease, A K Adams & S I Wells

  2. Department of Cancer Biology, University of Cincinnati College of Medicine, Cincinnati, OH, USA

    N M Benight, M A Nashu & S E Waltz

  3. Department of Pathology and Laboratory Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA

    P K Wagh

  4. Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA

    J Serrano-Lopez & J A Cancelas

  5. IMIBIC/UCO/University Hospital Reina Sofia, Cordoba, Spain

    J Serrano-Lopez

  6. Hoxworth Blood Center, University of Cincinnati College of Medicine, Cincinnati, OH, USA

    J A Cancelas

  7. Department of Research, Cincinnati Veterans Affairs Medical Center, Cincinnati, OH, USA

    S E Waltz

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  1. L M Privette Vinnedge
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Privette Vinnedge, L., Benight, N., Wagh, P. et al. The DEK oncogene promotes cellular proliferation through paracrine Wnt signaling in Ron receptor-positive breast cancers. Oncogene 34, 2325–2336 (2015). https://doi.org/10.1038/onc.2014.173

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