Distinct and Overlapping Roles of Hippo Effectors YAP and TAZ During Human and Mouse Hepatocarcinogenesis.


Journal

Cellular and molecular gastroenterology and hepatology
ISSN: 2352-345X
Titre abrégé: Cell Mol Gastroenterol Hepatol
Pays: United States
ID NLM: 101648302

Informations de publication

Date de publication:
2021
Historique:
received: 22 07 2020
revised: 11 11 2020
accepted: 12 11 2020
pubmed: 25 11 2020
medline: 8 3 2022
entrez: 24 11 2020
Statut: ppublish

Résumé

Yes-associated protein (YAP) and its paralog transcriptional co-activator with post synaptic density protein, drosophila disc large tumor suppressor and zonula occludens-1-binding motif (TAZ) are 2 co-activators downstream of Hippo tumor-suppressor cascade. Both have been implicated in the development of hepatocellular carcinoma (HCC). However, whether YAP and TAZ have distinct or overlapping functions during hepatocarcinogenesis remains unknown. Expression patterns of YAP and TAZ were analyzed in human HCC samples. The requirement of Yap and/or Taz in protein kinase B (Akt)/ neuroblastoma RAS viral oncogene homolog (NRas) -driven liver tumorigenesis was analyzed using conditional Yap, Taz, and Yap;Taz knockout mice. Transcriptional programs regulated by YAP and/or TAZ were identified via RNA sequencing. We found that in human HCC samples, an almost ubiquitous activation of YAP or TAZ occurs, underlying their role in this tumor type. Intriguingly, 70% of HCC samples showed only nuclear YAP or TAZ immunoreactivity. In the Akt/NRas liver tumor model, where nuclear Yap and Taz can be detected readily, deletion of Yap or Taz alone only mildly delayed liver tumor development, whereas their concomitant ablation strongly inhibited tumor cell proliferation and significantly suppressed Akt/NRas-driven hepatocarcinogenesis. In HCC cell lines, silencing of either YAP or TAZ led to decreased expression of both overlapping and distinct sets of genes, with the most prominent gene signatures related to cell-cycle progression and DNA replication. YAP and TAZ have overlapping and distinct roles in hepatocarcinogenesis. HCCs may display unique activation of YAP or TAZ, thus relying on either YAP or TAZ for their growth.

Sections du résumé

BACKGROUND & AIMS
Yes-associated protein (YAP) and its paralog transcriptional co-activator with post synaptic density protein, drosophila disc large tumor suppressor and zonula occludens-1-binding motif (TAZ) are 2 co-activators downstream of Hippo tumor-suppressor cascade. Both have been implicated in the development of hepatocellular carcinoma (HCC). However, whether YAP and TAZ have distinct or overlapping functions during hepatocarcinogenesis remains unknown.
METHODS
Expression patterns of YAP and TAZ were analyzed in human HCC samples. The requirement of Yap and/or Taz in protein kinase B (Akt)/ neuroblastoma RAS viral oncogene homolog (NRas) -driven liver tumorigenesis was analyzed using conditional Yap, Taz, and Yap;Taz knockout mice. Transcriptional programs regulated by YAP and/or TAZ were identified via RNA sequencing.
RESULTS
We found that in human HCC samples, an almost ubiquitous activation of YAP or TAZ occurs, underlying their role in this tumor type. Intriguingly, 70% of HCC samples showed only nuclear YAP or TAZ immunoreactivity. In the Akt/NRas liver tumor model, where nuclear Yap and Taz can be detected readily, deletion of Yap or Taz alone only mildly delayed liver tumor development, whereas their concomitant ablation strongly inhibited tumor cell proliferation and significantly suppressed Akt/NRas-driven hepatocarcinogenesis. In HCC cell lines, silencing of either YAP or TAZ led to decreased expression of both overlapping and distinct sets of genes, with the most prominent gene signatures related to cell-cycle progression and DNA replication.
CONCLUSIONS
YAP and TAZ have overlapping and distinct roles in hepatocarcinogenesis. HCCs may display unique activation of YAP or TAZ, thus relying on either YAP or TAZ for their growth.

Identifiants

pubmed: 33232824
pii: S2352-345X(20)30187-9
doi: 10.1016/j.jcmgh.2020.11.008
pmc: PMC7903139
pii:
doi:

Substances chimiques

Cell Cycle Proteins 0
Transcription Factors 0
YAP-Signaling Proteins 0
YY1AP1 protein, human 0
Yap1 protein, mouse 0
Acyltransferases EC 2.3.-
tafazzin protein, mouse EC 2.3.-
TAFAZZIN protein, human EC 2.3.1.-

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

1095-1117

Subventions

Organisme : NIDDK NIH HHS
ID : P30 DK026743
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA190606
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA204586
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA239251
Pays : United States

Informations de copyright

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Auteurs

Haichuan Wang (H)

Liver Transplantation Division, Department of Liver Surgery, Laboratory of Liver Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan, People's Republic of China; Department of Bioengineering and Therapeutic Sciences and Liver Center, University of California, San Francisco, California.

Jingxiao Wang (J)

Department of Bioengineering and Therapeutic Sciences and Liver Center, University of California, San Francisco, California; School of Life Sciences, Beijing University of Chinese Medicine, Beijing, China.

Shanshan Zhang (S)

Department of Bioengineering and Therapeutic Sciences and Liver Center, University of California, San Francisco, California.

Jiaoyuan Jia (J)

Department of Bioengineering and Therapeutic Sciences and Liver Center, University of California, San Francisco, California; Department of Oncology and Hematology, The Second Hospital, Jilin University, Changchun, China.

Xianqiong Liu (X)

Department of Bioengineering and Therapeutic Sciences and Liver Center, University of California, San Francisco, California; School of Pharmacy, Hubei University of Chinese Medicine Wuhan, Hubei, China.

Jie Zhang (J)

Department of Bioengineering and Therapeutic Sciences and Liver Center, University of California, San Francisco, California.

Pan Wang (P)

Department of Bioengineering and Therapeutic Sciences and Liver Center, University of California, San Francisco, California.

Xinhua Song (X)

Department of Bioengineering and Therapeutic Sciences and Liver Center, University of California, San Francisco, California.

Li Che (L)

Department of Bioengineering and Therapeutic Sciences and Liver Center, University of California, San Francisco, California.

Ke Liu (K)

Department of Pediatrics and Human Development, East Lansing, Michigan; Department of Pharmacology and Toxicology, College of Human Medicine, Michigan State University, East Lansing, Michigan.

Silvia Ribback (S)

Institute of Pathology, University of Greifswald, Greifswald, Germany.

Antonio Cigliano (A)

Institute of Pathology, University Clinic of Regensburg, Regensburg, Germany.

Matthias Evert (M)

Institute of Pathology, University Clinic of Regensburg, Regensburg, Germany.

Hong Wu (H)

Liver Transplantation Division, Department of Liver Surgery, Laboratory of Liver Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan, People's Republic of China.

Diego F Calvisi (DF)

Institute of Pathology, University Clinic of Regensburg, Regensburg, Germany. Electronic address: diego.calvisi@klinik.uni-regensburg.de.

Yong Zeng (Y)

Liver Transplantation Division, Department of Liver Surgery, Laboratory of Liver Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan, People's Republic of China. Electronic address: zengyong@medmail.com.cn.

Xin Chen (X)

Department of Bioengineering and Therapeutic Sciences and Liver Center, University of California, San Francisco, California. Electronic address: xin.chen@ucsf.edu.

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Classifications MeSH