FGFR2 fusion proteins drive oncogenic transformation of mouse liver organoids towards cholangiocarcinoma.


Journal

Journal of hepatology
ISSN: 1600-0641
Titre abrégé: J Hepatol
Pays: Netherlands
ID NLM: 8503886

Informations de publication

Date de publication:
08 2021
Historique:
received: 04 06 2020
revised: 03 02 2021
accepted: 25 02 2021
pubmed: 21 3 2021
medline: 8 2 2022
entrez: 20 3 2021
Statut: ppublish

Résumé

About 15% of intrahepatic cholangiocarcinomas (iCCAs) express fibroblast growth factor receptor 2 (FGFR2) fusion proteins (FFs), usually alongside mutational inactivation of TP53, CDKN2A or BAP1. In FFs, FGFR2 residues 1-768 fuse to sequences encoded by a diverse array of partner genes (>60) causing oncogenic FF activation. While FGFR-specific tyrosine kinase inhibitors (F-TKI) provide clinical benefit in FF Four iCCA FFs carrying different fusion sequences were expressed in Tp53 Transplantation of FF-expressing liver organoids yielded tumors diagnosed as CCA based on histological, phenotypic and transcriptomic analyses. The penetrance of this tumorigenic phenotype was influenced by FF identity. Tumor organoids and 2D cell lines derived from CCA lesions were addicted to FF signaling via Ras-Erk, regardless of FF identity or V565F mutation. Dual blockade of FF and the Ras-Erk pathway by concomitant pharmacological inhibition of FFs and Mek1/2 provided greater therapeutic efficacy than single agent F-TKI in vitro and in vivo. FF-driven iCCA pathogenesis was successfully modeled on a Tp53 Intrahepatic cholangiocarcinoma (iCCA) is a rare cancer that is difficult to treat. A subtype of iCCA is caused by genomic alterations that generate oncogenic drivers known as FGFR2 fusions. Patients with FGFR2 fusions respond to FGFR inhibitors, but clinical responses are often of modest duration. We used animal and cellular models to show that FGFR2 fusions require the activity of a downstream effector named Mek1/2. We found that dual blockade of FGFR2 fusions and Mek1/2 was more effective than isolated inhibition of FGFR2 fusions, pointing to the potential clinical utility of dual FGFR2-MEK1/2 blockade in patients with iCCA.

Sections du résumé

BACKGROUND & AIMS
About 15% of intrahepatic cholangiocarcinomas (iCCAs) express fibroblast growth factor receptor 2 (FGFR2) fusion proteins (FFs), usually alongside mutational inactivation of TP53, CDKN2A or BAP1. In FFs, FGFR2 residues 1-768 fuse to sequences encoded by a diverse array of partner genes (>60) causing oncogenic FF activation. While FGFR-specific tyrosine kinase inhibitors (F-TKI) provide clinical benefit in FF
METHODS
Four iCCA FFs carrying different fusion sequences were expressed in Tp53
RESULTS
Transplantation of FF-expressing liver organoids yielded tumors diagnosed as CCA based on histological, phenotypic and transcriptomic analyses. The penetrance of this tumorigenic phenotype was influenced by FF identity. Tumor organoids and 2D cell lines derived from CCA lesions were addicted to FF signaling via Ras-Erk, regardless of FF identity or V565F mutation. Dual blockade of FF and the Ras-Erk pathway by concomitant pharmacological inhibition of FFs and Mek1/2 provided greater therapeutic efficacy than single agent F-TKI in vitro and in vivo.
CONCLUSIONS
FF-driven iCCA pathogenesis was successfully modeled on a Tp53
LAY SUMMARY
Intrahepatic cholangiocarcinoma (iCCA) is a rare cancer that is difficult to treat. A subtype of iCCA is caused by genomic alterations that generate oncogenic drivers known as FGFR2 fusions. Patients with FGFR2 fusions respond to FGFR inhibitors, but clinical responses are often of modest duration. We used animal and cellular models to show that FGFR2 fusions require the activity of a downstream effector named Mek1/2. We found that dual blockade of FGFR2 fusions and Mek1/2 was more effective than isolated inhibition of FGFR2 fusions, pointing to the potential clinical utility of dual FGFR2-MEK1/2 blockade in patients with iCCA.

Identifiants

pubmed: 33741397
pii: S0168-8278(21)00172-0
doi: 10.1016/j.jhep.2021.02.032
pii:
doi:

Substances chimiques

Trp53 protein, mouse 0
Tumor Suppressor Protein p53 0
FGFR2 protein, human EC 2.7.10.1
Receptor, Fibroblast Growth Factor, Type 2 EC 2.7.10.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

351-362

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2021 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Conflict of interest All Authors, except M.J.B., have no personal, professional or financial conflicts to disclose. M.J.B. disclosures: ADC Therapeutics – Consulting to self; Exelixis Pharmaceuticals – Consulting to self; Inspyr Therapeutics – Consulting to self; G1 Therapeutics – Consulting to self; Immunovative Therapies – Consulting to self; OncBioMune Pharmaceuticals – Consulting to self; Western Oncolytics – Consulting to self; Lynx Group – Consulting to self; Genentech – Consulting to self; Merck – Consulting to self; Huya – Consulting to self; Astra Zeneca – Travel Support to self. Please refer to the accompanying ICMJE disclosure forms for further details.

Auteurs

Giulia Cristinziano (G)

Unit of Oncogenomics and Epigenetics, IRCCS Regina Elena National Cancer Institute, Rome, Italy.

Manuela Porru (M)

Unit of Oncogenomics and Epigenetics, IRCCS Regina Elena National Cancer Institute, Rome, Italy.

Dante Lamberti (D)

Unit of Oncogenomics and Epigenetics, IRCCS Regina Elena National Cancer Institute, Rome, Italy.

Simonetta Buglioni (S)

Department of Pathology, IRCCS Regina Elena National Cancer Institute, Rome, Italy.

Francesca Rollo (F)

Department of Pathology, IRCCS Regina Elena National Cancer Institute, Rome, Italy.

Carla Azzurra Amoreo (CA)

Department of Pathology, IRCCS Regina Elena National Cancer Institute, Rome, Italy.

Isabella Manni (I)

SAFU, IRCCS Regina Elena National Cancer Institute, Rome, Italy.

Diana Giannarelli (D)

UOSD Clinical Trial Center, Biostatistics and Bioinformatics, IRCCS Regina Elena National Cancer Institute, Rome, Italy.

Cristina Cristofoletti (C)

Istituto Dermopatico dell'Immacolata, IDI-IRCCS, Rome, Italy.

Giandomenico Russo (G)

Istituto Dermopatico dell'Immacolata, IDI-IRCCS, Rome, Italy.

Mitesh J Borad (MJ)

Division of Hematology and Oncology, Mayo Clinic, Scottsdale, USA.

Gian Luca Grazi (GL)

Division of Hepatobiliary Pancreatic Surgery, IRCCS Regina Elena National Cancer Institute, Rome, Italy.

Maria Grazia Diodoro (MG)

Department of Pathology, IRCCS Regina Elena National Cancer Institute, Rome, Italy.

Silvia Giordano (S)

Department of Oncology, University of Torino, Candiolo, Italy; Candiolo Cancer Institute, FPO-IRCCS, Candiolo, Italy.

Andrea Sacconi (A)

UOSD Clinical Trial Center, Biostatistics and Bioinformatics, IRCCS Regina Elena National Cancer Institute, Rome, Italy.

Mattia Forcato (M)

Center for Genome Research, Department of Life Sciences, University of Modena and Reggio Emilia, Modena, Italy.

Sergio Anastasi (S)

Unit of Oncogenomics and Epigenetics, IRCCS Regina Elena National Cancer Institute, Rome, Italy. Electronic address: sergio.anastasi@ifo.gov.it.

Carlo Leonetti (C)

SAFU, IRCCS Regina Elena National Cancer Institute, Rome, Italy. Electronic address: carlo.leonetti@ifo.gov.it.

Oreste Segatto (O)

Unit of Oncogenomics and Epigenetics, IRCCS Regina Elena National Cancer Institute, Rome, Italy. Electronic address: oreste.segatto@ifo.gov.it.

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Classifications MeSH