Paragangliomas arise through an autonomous vasculo-angio-neurogenic program inhibited by imatinib View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2018-05

AUTHORS

Fabio Verginelli, Silvia Perconti, Simone Vespa, Francesca Schiavi, Sampath Chandra Prasad, Paola Lanuti, Alessandro Cama, Lorenzo Tramontana, Diana Liberata Esposito, Simone Guarnieri, Artenca Sheu, Mattia Russel Pantalone, Rosalba Florio, Annalisa Morgano, Cosmo Rossi, Giuseppina Bologna, Marco Marchisio, Andrea D’Argenio, Elisa Taschin, Rosa Visone, Giuseppe Opocher, Angelo Veronese, Carlo T. Paties, Vinagolu K. Rajasekhar, Cecilia Söderberg-Nauclér, Mario Sanna, Lavinia Vittoria Lotti, Renato Mariani-Costantini

ABSTRACT

Tumours can be viewed as aberrant tissues or organs sustained by tumorigenic stem-like cells that engage into dysregulated histo/organogenetic processes. Paragangliomas, prototypical organoid tumours constituted by dysmorphic variants of the vascular and neural tissues found in normal paraganglia, provide a model to test this hypothesis. To understand the origin of paragangliomas, we built a biobank comprising 77 cases, 18 primary cultures, 4 derived cell lines, 80 patient-derived xenografts and 11 cell-derived xenografts. We comparatively investigated these unique complementary materials using morphofunctional, ultrastructural and flow cytometric assays accompanied by microRNA studies. We found that paragangliomas contain stem-like cells with hybrid mesenchymal/vasculoneural phenotype, stabilized and expanded in the derived cultures. The viability and growth of such cultures depended on the downregulation of the miR-200 and miR-34 families, which allowed high PDGFRA and ZEB1 protein expression levels. Both tumour tissue- and cell culture-derived xenografts recapitulated the vasculoneural paraganglioma structure and arose from mesenchymal-like cells through a fixed developmental sequence. First, vasculoangiogenesis organized the microenvironment, building a perivascular niche which in turn supported neurogenesis. Neuroepithelial differentiation was associated with severe mitochondrial dysfunction, not present in cultured paraganglioma cells, but acquired in vivo during xenograft formation. Vasculogenesis was the Achilles' heel of xenograft development. In fact, imatinib, that targets endothelial-mural signalling, blocked paraganglioma xenograft formation (11 xenografts from 12 cell transplants in the control group versus 2 out of 10 in the treated group, P = 0.0015). Overall our key results were unaffected by the SDHx gene carrier status of the patient, characterized for 70 out of 77 cases. In conclusion, we explain the biphasic vasculoneural structure of paragangliomas and identify an early and pharmacologically actionable phase of paraganglioma organization. More... »

PAGES

779-798

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  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1007/s00401-017-1799-2

    DOI

    http://dx.doi.org/10.1007/s00401-017-1799-2

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1100200203

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/29305721


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