Epigenetic footprint enables molecular risk stratification of hepatoblastoma with clinical implications.


Journal

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

Informations de publication

Date de publication:
08 2020
Historique:
received: 05 09 2019
revised: 11 03 2020
accepted: 13 03 2020
pubmed: 3 4 2020
medline: 4 11 2021
entrez: 3 4 2020
Statut: ppublish

Résumé

Hepatoblastoma (HB) is a rare disease. Nevertheless, it is the predominant pediatric liver cancer, with limited therapeutic options for patients with aggressive tumors. Herein, we aimed to uncover the mechanisms of HB pathobiology and to identify new biomarkers and therapeutic targets in a move towards precision medicine for patients with advanced HB. We performed a comprehensive genomic, transcriptomic and epigenomic characterization of 159 clinically annotated samples from 113 patients with HB, using high-throughput technologies. We discovered a widespread epigenetic footprint of HB that includes hyperediting of the tumor suppressor BLCAP concomitant with a genome-wide dysregulation of RNA editing and the overexpression of mainly non-coding genes of the oncogenic 14q32 DLK1-DIO3 locus. By unsupervised analysis, we identified 2 epigenomic clusters (Epi-CA, Epi-CB) with distinct degrees of DNA hypomethylation and CpG island hypermethylation that are associated with the C1/C2/C2B transcriptomic subtypes. Based on these findings, we defined the first molecular risk stratification of HB (MRS-HB), which encompasses 3 main prognostic categories and improves the current clinical risk stratification approach. The MRS-3 category (28%), defined by strong 14q32 locus expression and Epi-CB methylation features, was characterized by CTNNB1 and NFE2L2 mutations, a progenitor-like phenotype and clinical aggressiveness. Finally, we identified choline kinase alpha as a promising therapeutic target for intermediate and high-risk HBs, as its inhibition in HB cell lines and patient-derived xenografts strongly abrogated tumor growth. These findings provide a detailed insight into the molecular features of HB and could be used to improve current clinical stratification approaches and to develop treatments for patients with HB. Hepatoblastoma is a rare childhood liver cancer that has been understudied. We have used cutting-edge technologies to expand our molecular knowledge of this cancer. Our biological findings can be used to improve clinical management and pave the way for the development of novel therapies for this cancer.

Sections du résumé

BACKGROUND & AIMS
Hepatoblastoma (HB) is a rare disease. Nevertheless, it is the predominant pediatric liver cancer, with limited therapeutic options for patients with aggressive tumors. Herein, we aimed to uncover the mechanisms of HB pathobiology and to identify new biomarkers and therapeutic targets in a move towards precision medicine for patients with advanced HB.
METHODS
We performed a comprehensive genomic, transcriptomic and epigenomic characterization of 159 clinically annotated samples from 113 patients with HB, using high-throughput technologies.
RESULTS
We discovered a widespread epigenetic footprint of HB that includes hyperediting of the tumor suppressor BLCAP concomitant with a genome-wide dysregulation of RNA editing and the overexpression of mainly non-coding genes of the oncogenic 14q32 DLK1-DIO3 locus. By unsupervised analysis, we identified 2 epigenomic clusters (Epi-CA, Epi-CB) with distinct degrees of DNA hypomethylation and CpG island hypermethylation that are associated with the C1/C2/C2B transcriptomic subtypes. Based on these findings, we defined the first molecular risk stratification of HB (MRS-HB), which encompasses 3 main prognostic categories and improves the current clinical risk stratification approach. The MRS-3 category (28%), defined by strong 14q32 locus expression and Epi-CB methylation features, was characterized by CTNNB1 and NFE2L2 mutations, a progenitor-like phenotype and clinical aggressiveness. Finally, we identified choline kinase alpha as a promising therapeutic target for intermediate and high-risk HBs, as its inhibition in HB cell lines and patient-derived xenografts strongly abrogated tumor growth.
CONCLUSIONS
These findings provide a detailed insight into the molecular features of HB and could be used to improve current clinical stratification approaches and to develop treatments for patients with HB.
LAY SUMMARY
Hepatoblastoma is a rare childhood liver cancer that has been understudied. We have used cutting-edge technologies to expand our molecular knowledge of this cancer. Our biological findings can be used to improve clinical management and pave the way for the development of novel therapies for this cancer.

Identifiants

pubmed: 32240714
pii: S0168-8278(20)30187-2
doi: 10.1016/j.jhep.2020.03.025
pii:
doi:

Substances chimiques

BLCAP protein, human 0
Biomarkers, Tumor 0
CTNNB1 protein, human 0
Calcium-Binding Proteins 0
DLK1 protein, human 0
Membrane Proteins 0
Neoplasm Proteins 0
beta Catenin 0
CHKA protein, human EC 2.7.1.32
Choline Kinase EC 2.7.1.32

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

328-341

Subventions

Organisme : Cancer Research UK
ID : 26813
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C9380/A26813
Pays : United Kingdom
Organisme : NCI NIH HHS
ID : P30 CA196521
Pays : United States

Informations de copyright

Copyright © 2020 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Conflict of interest Prof. Josep M. Llovet is receiving research support from Bayer HealthCare Pharmaceuticals, Eisai Inc, Bristol-Myers Squibb and Ipsen, and consulting fees from Bayer HealthCare Pharmaceuticals, Bristol-Myers Squibb, Eisai Inc, Celsion Corporation, Eli Lilly, Exelixis, Merck, Ipsen, Glycotest, Navigant, Leerink Swann LLC, Midatech Ltd, Fortress Biotech, Sprink Pharmaceuticals and Nucleix and CANFITE. CA has a research contract with CHIOME Biosciences Inc. The other authors report no conflicts of interest in this work. Please refer to the accompanying ICMJE disclosure forms for further details.

Auteurs

Juan Carrillo-Reixach (J)

Childhood Liver Oncology Group, Germans Trias i Pujol Research Institute (IGTP), Program for Predictive and Personalized Medicine of Cancer (PMPPC), Badalona, Spain.

Laura Torrens (L)

Mount Sinai Liver Cancer Program, Divisions of Liver Diseases, Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, USA; Translational research in Hepatic Oncology, Liver Unit, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain.

Marina Simon-Coma (M)

Childhood Liver Oncology Group, Germans Trias i Pujol Research Institute (IGTP), Program for Predictive and Personalized Medicine of Cancer (PMPPC), Badalona, Spain; CIBER, Hepatic and Digestive Diseases, Barcelona, Spain.

Laura Royo (L)

Childhood Liver Oncology Group, Germans Trias i Pujol Research Institute (IGTP), Program for Predictive and Personalized Medicine of Cancer (PMPPC), Badalona, Spain.

Montserrat Domingo-Sàbat (M)

Childhood Liver Oncology Group, Germans Trias i Pujol Research Institute (IGTP), Program for Predictive and Personalized Medicine of Cancer (PMPPC), Badalona, Spain.

Jordi Abril-Fornaguera (J)

Mount Sinai Liver Cancer Program, Divisions of Liver Diseases, Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, USA; Translational research in Hepatic Oncology, Liver Unit, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain.

Nicholas Akers (N)

Translational research in Hepatic Oncology, Liver Unit, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain; Department of Genetics and Genomic Sciences, The Icahn Institute for Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai, New York, USA.

Margarita Sala (M)

CIBER, Hepatic and Digestive Diseases, Barcelona, Spain; Gastroenterology Department, Hospital Universitari Germans Trias i Pujol Hospital, Badalona, Spain; Gastroenterology Department, Hospital Universitari Josep Trueta, Girona, Spain.

Sonia Ragull (S)

Childhood Liver Oncology Group, Germans Trias i Pujol Research Institute (IGTP), Program for Predictive and Personalized Medicine of Cancer (PMPPC), Badalona, Spain.

Magdalena Arnal (M)

MARGenomics, IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain.

Núria Villalmanzo (N)

PMPPC, IGTP, Badalona, Spain.

Stefano Cairo (S)

XenTech, Evry, France; Instituto di Ricerca Pediatrica, Corso Stati Uniti 4, Padova, Italy.

Alberto Villanueva (A)

Chemoresistance and Predictive Factors Group, Program Against Cancer Therapeutic Resistance, Catalan Institute of Oncology (ICO), Bellvitge Biomedical Research Institute, L'Hospitalet del Llobregat, Barcelona, Spain.

Roland Kappler (R)

Department of Pediatric Surgery, Dr. von Hauner Children's Hospital, Ludwig-Maximilians-University Munich, Lindwurmstr. 2a, 80337 Munich, Germany.

Marta Garrido (M)

Hospital Vall d'Hebron, Pathology Department, Barcelona, Spain.

Laura Guerra (L)

University Hospital La Paz, Pathology Department, Madrid, Spain.

Constantino Sábado (C)

Hospital Vall d'Hebron, Pediatric Oncology Department, Barcelona, Spain.

Gabriela Guillén (G)

Hospital Vall d'Hebron, Pediatric Surgery Department, Barcelona, Spain.

Mar Mallo (M)

MDS Research Group, Josep Carreras Leukaemia Research Institute, ICO-Hospital Germans Trias i Pujol, Universitat Autònoma de Barcelona, Badalona, Spain.

David Piñeyro (D)

High Content Genomics and Bioinformatics Unit, PMPPC, IGTP, Badalona, Spain.

María Vázquez-Vitali (M)

Childhood Liver Oncology Group, Germans Trias i Pujol Research Institute (IGTP), Program for Predictive and Personalized Medicine of Cancer (PMPPC), Badalona, Spain.

Olga Kuchuk (O)

Mount Sinai Liver Cancer Program, Divisions of Liver Diseases, Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, USA.

María Elena Mateos (ME)

Pediatric Oncology Unit, Department of Pediatrics, University Hospital Reina Sofía, Córdoba, Spain.

Gema Ramírez (G)

University Hospital Universitario Virgen del Rocío, Pediatric Oncology Department, Sevilla, Spain.

Manuel López Santamaría (ML)

University Hospital La Paz, Pediatric Surgery Department, Madrid, Spain.

Yasmina Mozo (Y)

University Hospital La Paz, Pediatric Oncology Department, Madrid, Spain.

Aroa Soriano (A)

Biomedical Research in Cancer Stem Cells Group, Pathology Department, Institut de Recerca Hospital Vall d'Hebron (VHIR), Barcelona, Spain.

Michael Grotzer (M)

Department of Pediatric Oncology, University Children's Hospital Zurich, University of Zurich, Zurich, Switzerland.

Sophie Branchereau (S)

Bicêtre Hospital, Le Kremlin-Bicêtre, France.

Nagore García de Andoin (NG)

Pediatric Oncology, Hospital Universitario Donostia, Doctor Begiristain Kalea, 117, 20080, Donostia, Spain.

Blanca López-Ibor (B)

Department of Pediatric Hematology and Oncology, HM Montepríncipe Hospital, Boadilla del Monte, Madrid, Spain.

Ricardo López-Almaraz (R)

Pediatric Oncology and Hematology, Hospital Universitario Cruces, Bilbao, Spain.

José Antonio Salinas (JA)

Division of Hematology-Oncology, Department of Pediatrics, Hospital Universitari Son Espases, Palma de Mallorca, Spain.

Bárbara Torres (B)

Medical Oncology Department, Pediatric Oncology Department, University Hospital La Fe, Valencia, Spain.

Francisco Hernández (F)

University Hospital La Paz, Pediatric Surgery Department, Madrid, Spain.

José Javier Uriz (JJ)

Pediatric Oncology, Hospital Universitario Donostia, Doctor Begiristain Kalea, 117, 20080, Donostia, Spain.

Monique Fabre (M)

Department of Pathology, Hôpital Universitaire Necker-Enfants Malades, Assistance Publique-Hôpitaux de Paris, and Université Paris Descartes, Paris, France.

Julià Blanco (J)

IrsiCaixa AIDS Research Institute, IGTP, Badalona, Catalonia, Spain; University of Vic - Central University of Catalonia, Vic, Spain.

Claudia Paris (C)

Stem Cell Transplant Unit, Hospital Luis Calvo Mackenna, Santiago, Chile.

Viera Bajčiová (V)

Department of Pediatric Oncology, Childrens University Hospital Brno, Brno, Czech.

Geneviève Laureys (G)

Department of Pediatric Hematology, Oncology and Hematopoietic Stem Cell Transplantation, Ghent University Hospital, Ghent, Belgium.

Helena Masnou (H)

Gastroenterology Department, Hospital Universitari Germans Trias i Pujol Hospital, Badalona, Spain.

Ariadna Clos (A)

Gastroenterology Department, Hospital Universitari Germans Trias i Pujol Hospital, Badalona, Spain.

Cristina Belendez (C)

Oncohematology Service, Hospital Gregorio Marañón, Madrid, Spain.

Catherine Guettier (C)

Bicêtre Hospital, Le Kremlin-Bicêtre, France.

Lauro Sumoy (L)

High Content Genomics and Bioinformatics Unit, PMPPC, IGTP, Badalona, Spain.

Ramón Planas (R)

CIBER, Hepatic and Digestive Diseases, Barcelona, Spain; Gastroenterology Department, Hospital Universitari Germans Trias i Pujol Hospital, Badalona, Spain.

Mireia Jordà (M)

PMPPC, IGTP, Badalona, Spain; Consortium for the Study of Thyroid Cancer, CECaT, Barcelona, Spain.

Lara Nonell (L)

MARGenomics, IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain.

Piotr Czauderna (P)

Department of Surgery and Urology for Children and Adolescents, Medical University of Gdansk, Gdansk, Poland.

Bruce Morland (B)

Department of Oncology, Birmingham Women's and Children's Hospital, Birmingham, UK.

Daniela Sia (D)

Mount Sinai Liver Cancer Program, Divisions of Liver Diseases, Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, USA.

Bojan Losic (B)

Department of Genetics and Genomic Sciences, The Icahn Institute for Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai, New York, USA; Graduate School of Biomedical Sciences, One Gustave L. Levy Place, Box 1022, New York, NY; Tisch Cancer Institute, Cancer Immunology Program, Icahn School of Medicine at Mount Sinai, New York, NY; Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, New York, NY.

Marie Annick Buendia (MA)

INSERM, UMR 1193, Paul-Brousse Hospital, Hepatobiliary Centre, Villejuif, France.

Maria Rosa Sarrias (MR)

CIBER, Hepatic and Digestive Diseases, Barcelona, Spain; Innate Immunity Group, IGTP, Badalona, Spain.

Josep M Llovet (JM)

Mount Sinai Liver Cancer Program, Divisions of Liver Diseases, Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, USA; Translational research in Hepatic Oncology, Liver Unit, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain; Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain.

Carolina Armengol (C)

Childhood Liver Oncology Group, Germans Trias i Pujol Research Institute (IGTP), Program for Predictive and Personalized Medicine of Cancer (PMPPC), Badalona, Spain; CIBER, Hepatic and Digestive Diseases, Barcelona, Spain. Electronic address: carmengol@igtp.cat.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH