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Coronin 1C promotes triple-negative breast cancer invasiveness through regulation of MT1-MMP traffic and invadopodia function

Oncogene volume 37, pages 6425–6441 (2018)Cite this article

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Abstract

Membrane type 1-matrix metalloproteinase (MT1-MMP), a membrane-tethered protease, is key for matrix breakdown during cancer invasion and metastasis. Assembly of branched actin networks by the Arp2/3 complex is required for MT1-MMP traffic and formation of matrix-degradative invadopodia. Contrasting with the well-established role of actin filament branching factor cortactin in invadopodia function during cancer cell invasion, the contribution of coronin-family debranching factors to invadopodia-based matrix remodeling is not known. Here, we investigated the contribution of coronin 1C to the invasive potential of breast cancer cells. We report that expression of coronin 1C is elevated in invasive human breast cancers, correlates positively with MT1-MMP expression in relation with increased metastatic risk and is a new independent prognostic factor in breast cancer. We provide evidence that, akin to cortactin, coronin 1C is required for invadopodia formation and matrix degradation by breast cancer cells lines and for 3D collagen invasion by multicellular spheroids. Using intravital imaging of orthotopic human breast tumor xenografts, we find that coronin 1C accumulates in structures forming in association with collagen fibrils in the tumor microenvironment. Moreover, we establish the role of coronin 1C in the regulation of positioning and trafficking of MT1-MMP-positive endolysosomes. These results identify coronin 1C as a novel player of the multi-faceted mechanism responsible for invadopodia formation, MT1-MMP surface exposure and invasiveness in breast cancer cells.

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Acknowledgements

The authors greatly acknowledge the Breast Cancer Study Group and patients of Institut Curie for breast tumor samples. They thank the Cell and Tissue Imaging facility (PICT-IBiSA) and Nikon Imaging Centre, Institut Curie, member of the French National Research Infrastructure France-BioImaging (ANR10-INBS-04) for help with image acquisition and Dr Jakko van Rheenen for help with the mammary window and intravital imaging. AC was supported by a grant from Worldwide Cancer Research (Grant 16-1235 to PC), ACC by an EMBO Long Term postdoctoral fellowship and a grant from ‘Institut National du Cancer’ (INCA_6521 to PC), AG by INVADE grant from ITMO Cancer (Call Systems Biology 2012) to PC, SAG by a grant from INCa (INCa PLBIO14-161 to PC). and AAN and CSC by a grant from the German Research Foundation (DFG NO 113/22-2). The intravital imaging was supported by the Fondation pour la Recherche Médicale (FRM N° DGE20111123020), the Cancerople-IdF (n°2012-2-EML-04-IC-1), InCA (Cancer National Institute, n° 2011-1-LABEL-IC-4) and SiRIC (INCa-DGOS- 4654). This work was supported by grants from ‘Institut National du Cancer’ (INCa PLBIO14-161 and INCA_6521), Worldwide Cancer Research (Grant 16-1235) and ‘Equipe labellisée 2015’ from ‘Ligue Nationale contre le Cancer’ to PC.

Author contributions

AC carried out invadopodia formation and collagen degradation assays with the help of AZM and characterized the effects of CORO1C depletion on endolysosomal morphology and position. ACC who initiated the study, generated the cell lines stably expressing GFPCORO1C constructs and analyzed CORO1B and -1C expression in lysates of breast cancer cell lines provided by TD. LF and AVS generated the breast cancer TMA, performed CORO1C IHC labeling, and scored the breast tumor TMA for CORO1C expression with the help of CEK. SV and IB generated the invasive breast cancer cohort and performed RT-qPCR and multivariate analyses. MI performed multicellular spheroid invasion assays, analyzed the phenotype of cells silenced for cortactin, and performed intravital imaging. AG, CL, and SAG carried out mammary gland injections and analyzed tumor xenografts. MR and GR performed electron microscopy analyses. JEB, AAN, and CSC provided essential reagents. PC supervised the study and wrote the manuscript with contribution of all authors.

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Author notes

  1. These authors contributed equally: Alessia Castagnino and Antonio Castro-Castro.

Authors and Affiliations

  1. Institut Curie, PSL Research University, CNRS UMR144, Membrane and Cytoskeleton Dynamics group, 26 rue d’Ulm, F-75005, Paris, France

    Alessia Castagnino, Antonio Castro-Castro, Marie Irondelle, Alan Guichard, Catalina Lodillinsky, Sonia Agüera-González, Anna Zagryazhskaya-Masson & Philippe Chavrier

  2. Institut Curie, PSL Research University, Cell and Tissue Imaging Facility (PICT-IBiSA), 26 rue d’Ulm, F-75005, Paris, France

    Marie Irondelle

  3. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Oncología A. H. Roffo. Área de Investigación. San Martin 5481, Buenos Aires, C1417DTB, Argentina

    Catalina Lodillinsky

  4. Member of Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Catalina Lodillinsky

  5. Institut Curie, PSL Research University, Pathology-Genetics-Immunology Department, 26 rue d’Ulm, F-75005, Paris, France

    Laetitia Fuhrmann, Carole El Kesrouani & Anne Vincent-Salomon

  6. Department of Genetics, Institut Curie, PSL Research University, Pharmacogenomic Unit, 26 rue d’Ulm, F-75005, Paris, France

    Sophie Vacher & Ivan Bièche

  7. Institut Curie, PSL Research University, CNRS UMR144, Biogenesis and Functions of Lysosome-Related Organelles group, 26 rue d’Ulm, F-75005, Paris, France

    Maryse Romao & Graça Raposo

  8. Center for Biochemistry, Institute of Biochemistry I, Medical Faculty, University of Cologne, Joseph-Stelzmann-Str. 52, 50931, Cologne, Germany

    Angelika A. Noegel & Christoph S. Clemen

  9. Institut Curie, PSL Research University, Translational Research Department, Breast Cancer Biology Group, Paris, France

    Thierry Dubois

  10. UNC Lineberger Comprehensive Cancer Center and the Department of Cell Biology and Physiology, The University of North Carolina at Chapel Hill, Chapel Hill, NC, 27599, USA

    James E. Bear

  11. Department of Neurology, Heimer Institute for Muscle Research, University Hospital Bergmannsheil, Ruhr-University Bochum, Bürkle-de-la-Camp-Platz 1, 44789, Bochum, Germany

    Christoph S. Clemen

  12. EA7331, Paris Descartes University, Sorbonne Paris Cité, Faculty of Pharmaceutical and Biological Sciences, 4 avenue de l’observatoire, F-75006, Paris, France

    Ivan Bièche

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  1. Alessia Castagnino
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Castagnino, A., Castro-Castro, A., Irondelle, M. et al. Coronin 1C promotes triple-negative breast cancer invasiveness through regulation of MT1-MMP traffic and invadopodia function. Oncogene 37, 6425–6441 (2018). https://doi.org/10.1038/s41388-018-0422-x

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