Oncogenic mutations convert MET from a pro-apoptotic tumor suppressor to an oncogenic driver

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MET exon 14 skipping mutations in lung adenocarcinomas abolish MET's pro-apoptotic function, converting it from a tumor suppressor into an oncogenic driver by preventing p40MET fragment generation.

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This study investigated MET as a dependence receptor and asked whether oncogenic MET mutations can abolish its caspase-mediated pro-apoptotic tumor-suppressive function. Using lung adenocarcinoma samples (notably the ~3% carrying MET exon 14 skipping, METex14Del) and mechanistic models including HGF-humanized mice and genome editing, the authors found that METex14Del removes the caspase cleavage site and adjacent CBL-binding motif, preventing production of the pro-apoptotic p40MET fragment. They report that METex14Del confers sustained signaling, apoptosis resistance, increased invasion, and enhanced tumor growth, and that combined caspase-site and CBL-site mutations phenocopy METex14Del, while inducible re-expression of p40MET restores apoptosis and suppresses tumor formation. The paper does not explicitly discuss endometriosis or adenomyosis; it was included in the corpus via a keyword match in the upstream search index.

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Abstract

SUMMARY Dependence receptors can exert both oncogenic and tumor-suppressive activities. In cancers, downregulation of dependence receptors or overexpression of their ligands are well-established mechanisms that drive tumor progression. However, direct genetic alterations abolishing the pro-apoptotic function of dependence receptors have not been documented so far. MET, a receptor tyrosine kinase classically viewed as an oncogene, has also been proposed to act as a dependence receptor through its caspase-mediated cleavage, but whether this property impacts tumorigenesis remained unknown. In ∼3% of lung adenocarcinomas, MET mutations leading to exon 14 skipping (METex14Del) remove both the caspase site and the adjacent CBL-binding motif, thereby preventing generation of the pro-apoptotic p40MET fragment. METex14Del promotes sustained signaling, enhanced invasion, apoptosis resistance, and tumor growth in HGF-humanized mice. Genome editing revealed that combined —but not individual— mutations of the caspase and CBL sites phenocopy METex14Del. Moreover, inducible re-expression of p40MET in METex14Del-expressing cells restored apoptosis and suppressed tumor formation. Altogether, our findings identify MET exon 14 skipping as the first oncogenic mutation that drives tumorigenesis by abolishing the tumor-suppressive pro-apoptotic function of a dependence receptor, thereby redefining the oncogenic potential of MET.
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SUMMARY Dependence receptors can exert both oncogenic and tumor-suppressive activities. In cancers, downregulation of dependence receptors or overexpression of their ligands are well-established mechanisms that drive tumor progression. However, direct genetic alterations abolishing the pro-apoptotic function of dependence receptors have not been documented so far. MET, a receptor tyrosine kinase classically viewed as an oncogene, has also been proposed to act as a dependence receptor through its caspase-mediated cleavage, but whether this property impacts tumorigenesis remained unknown. In ∼3% of lung adenocarcinomas, MET mutations leading to exon 14 skipping (METex14Del) remove both the caspase site and the adjacent CBL-binding motif, thereby preventing generation of the pro-apoptotic p40MET fragment. METex14Del promotes sustained signaling, enhanced invasion, apoptosis resistance, and tumor growth in HGF-humanized mice. Genome editing revealed that combined —but not individual— mutations of the caspase and CBL sites phenocopy METex14Del. Moreover, inducible re-expression of p40MET in METex14Del-expressing cells restored apoptosis and suppressed tumor formation. Altogether, our findings identify MET exon 14 skipping as the first oncogenic mutation that drives tumorigenesis by abolishing the tumor-suppressive pro-apoptotic function of a dependence receptor, thereby redefining the oncogenic potential of MET. Competing Interest Statement ABC participated in advisory boards or received honoraria from Abbvie, Amgen, Astra-Zeneca, Bristol-661 Myers Squibb, Merck & Co, Pfizer, Roche, Novartis, Takeda, Janssen, Sanofi and received grants paid to ABC's institution from Novartis, Merck, Roche. Footnotes Financial Support: This work was supported by the CNRS, INSERM, the Institut Pasteur de Lille, the University of Lille, the Lille University Hospital, the “Region Hauts-de-France”, by the Fondation ARC pour la recherche sur le cancer and by grants from “Cancéropôle Nord-Ouest”, the “Ligue Contre le Cancer, Comités Nord et Aisne” the “SIRIC ONCOLille”, and the “Institut National du Cancer”. Canther laboratory is part of the ONCOLille institute. This work is supported by a grant from Contrat de Plan Etat-Région CPER Cancer 2015-2020.

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