β-Catenin and Yes-Associated Protein 1 Cooperate in Hepatoblastoma Pathogenesis.


Journal

The American journal of pathology
ISSN: 1525-2191
Titre abrégé: Am J Pathol
Pays: United States
ID NLM: 0370502

Informations de publication

Date de publication:
05 2019
Historique:
received: 06 09 2018
revised: 31 01 2019
accepted: 01 02 2019
pubmed: 23 2 2019
medline: 12 2 2020
entrez: 23 2 2019
Statut: ppublish

Résumé

Hepatoblastoma (HB), the most common pediatric primary liver neoplasm, shows nuclear localization of β-catenin and yes-associated protein 1 (YAP1) in almost 80% of the cases. Co-expression of constitutively active S127A-YAP1 and ΔN90 deletion-mutant β-catenin (YAP1-ΔN90-β-catenin) causes HB in mice. Because heterogeneity in downstream signaling is being identified owing to mutational differences even in the β-catenin gene alone, we investigated if co-expression of point mutants of β-catenin (S33Y or S45Y) with S127A-YAP1 led to similar tumors as YAP1-ΔN90-β-catenin. Co-expression of S33Y/S45Y-β-catenin and S127A-YAP1 led to activation of Yap and Wnt signaling and development of HB, with 100% mortality by 13 to 14 weeks. Co-expression with YAP1-S45Y/S33Y-β-catenin of the dominant-negative T-cell factor 4 or dominant-negative transcriptional enhanced associate domain 2, the respective surrogate transcription factors, prevented HB development. Although histologically similar, HB in YAP1-S45Y/S33Y-β-catenin, unlike YAP1-ΔN90-β-catenin HB, was glutamine synthetase (GS) positive. However, both ΔN90-β-catenin and point-mutant β-catenin comparably induced GS-luciferase reporter in vitro. Finally, using a previously reported 16-gene signature, it was shown that YAP1-ΔN90-β-catenin HB tumors exhibited genetic similarities with more proliferative, less differentiated, GS-negative HB patient tumors, whereas YAP1-S33Y/S45Y-β-catenin HB exhibited heterogeneity and clustered with both well-differentiated GS-positive and proliferative GS-negative patient tumors. Thus, we demonstrate that β-catenin point mutants can also collaborate with YAP1 in HB development, albeit with a distinct molecular profile from the deletion mutant, which may have implications in both biology and therapy.

Identifiants

pubmed: 30794807
pii: S0002-9440(18)30759-4
doi: 10.1016/j.ajpath.2019.02.002
pmc: PMC6521893
pii:
doi:

Substances chimiques

Adaptor Proteins, Signal Transducing 0
Biomarkers, Tumor 0
CTNNB1 protein, human 0
Transcription Factors 0
YAP-Signaling Proteins 0
YAP1 protein, human 0
beta Catenin 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1091-1104

Subventions

Organisme : NCI NIH HHS
ID : R01 CA204586
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK062277
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK100287
Pays : United States

Commentaires et corrections

Type : ErratumIn

Informations de copyright

Copyright © 2019 American Society for Investigative Pathology. Published by Elsevier Inc. All rights reserved.

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Auteurs

Qian Min (Q)

Department of Oncology, Renmin Hospital of Wuhan University, Wuhan, China.

Laura Molina (L)

Division of Experimental Pathology, Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Jing Li (J)

Department of Gynecology, Shiyan Taihe Hospital, Affiliated Hospital of Hubei University of Medicine, Shiyan, China.

Adeola O Adebayo Michael (AO)

Division of Experimental Pathology, Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Jacquelyn O Russell (JO)

Division of Experimental Pathology, Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Morgan E Preziosi (ME)

Division of Experimental Pathology, Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Sucha Singh (S)

Division of Experimental Pathology, Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Minakshi Poddar (M)

Division of Experimental Pathology, Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Madlen Matz-Soja (M)

Department of Neurosurgery, University Hospital Leipzig, Leipzig, Germany.

Sarangarajan Ranganathan (S)

Division of Pediatric Pathology, Department of Pathology, Children's Hospital, Pittburgh, Pennsylvania; Pittsburgh Liver Research Center, Pittsburgh, Pennsylvania.

Aaron W Bell (AW)

Division of Experimental Pathology, Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania; Pittsburgh Liver Research Center, Pittsburgh, Pennsylvania.

Rolf Gebhardt (R)

Institute of Biochemistry, Faculty of Medicine, University of Leipzig, Leipzig, Germany.

Frank Gaunitz (F)

Department of Neurosurgery, University Hospital Leipzig, Leipzig, Germany.

Jinming Yu (J)

Department of Oncology, Renmin Hospital of Wuhan University, Wuhan, China; Department of Radiation Oncology, Shandong Cancer Hospital Affiliated to Shandong University, Shandong Academy of Medical Science, Jinan, China. Electronic address: sdyujinming@163.com.

Junyan Tao (J)

Department of Gynecology, Shiyan Taihe Hospital, Affiliated Hospital of Hubei University of Medicine, Shiyan, China; Pittsburgh Liver Research Center, Pittsburgh, Pennsylvania.

Satdarshan P Monga (SP)

Department of Gynecology, Shiyan Taihe Hospital, Affiliated Hospital of Hubei University of Medicine, Shiyan, China; Pittsburgh Liver Research Center, Pittsburgh, Pennsylvania. Electronic address: smonga@pitt.edu.

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Classifications MeSH