Docking Protein p130Cas Regulates Acinar to Ductal Metaplasia During Pancreatic Adenocarcinoma Development and Pancreatitis.


Journal

Gastroenterology
ISSN: 1528-0012
Titre abrégé: Gastroenterology
Pays: United States
ID NLM: 0374630

Informations de publication

Date de publication:
04 2022
Historique:
received: 29 06 2021
revised: 18 11 2021
accepted: 12 12 2021
pubmed: 20 12 2021
medline: 3 5 2022
entrez: 19 12 2021
Statut: ppublish

Résumé

Acinar to ductal metaplasia is the prerequisite for the initiation of Kras-driven pancreatic ductal adenocarcinoma (PDAC), and candidate genes regulating this process are emerging from genome-wide association studies. The adaptor protein p130Cas emerged as a potential PDAC susceptibility gene and a Kras-synthetic lethal interactor in pancreatic cell lines; however, its role in PDAC development has remained largely unknown. Human PDAC samples and murine Kras We found that high expression of p130Cas is frequently detected in PDAC and correlates with higher histologic grade and poor prognosis. In a model of Kras-driven PDAC, loss of p130Cas inhibits tumor development and potently extends median survival. Deletion of p130Cas suppresses acinar-derived tumorigenesis and progression by means of repressing PI3K-AKT signaling, even in the presence of a worsening condition like pancreatitis. Our observations finally demonstrated that p130Cas acts downstream of Kras to boost the PI3K activity required for acinar to ductal metaplasia and subsequent tumor initiation. This demonstrates an unexpected driving role of p130Cas downstream of Kras through PI3K/AKT, thus indicating a rational therapeutic strategy of targeting the PI3K pathway in tumors with high expression of p130Cas.

Sections du résumé

BACKGROUND & AIMS
Acinar to ductal metaplasia is the prerequisite for the initiation of Kras-driven pancreatic ductal adenocarcinoma (PDAC), and candidate genes regulating this process are emerging from genome-wide association studies. The adaptor protein p130Cas emerged as a potential PDAC susceptibility gene and a Kras-synthetic lethal interactor in pancreatic cell lines; however, its role in PDAC development has remained largely unknown.
METHODS
Human PDAC samples and murine Kras
RESULTS
We found that high expression of p130Cas is frequently detected in PDAC and correlates with higher histologic grade and poor prognosis. In a model of Kras-driven PDAC, loss of p130Cas inhibits tumor development and potently extends median survival. Deletion of p130Cas suppresses acinar-derived tumorigenesis and progression by means of repressing PI3K-AKT signaling, even in the presence of a worsening condition like pancreatitis.
CONCLUSIONS
Our observations finally demonstrated that p130Cas acts downstream of Kras to boost the PI3K activity required for acinar to ductal metaplasia and subsequent tumor initiation. This demonstrates an unexpected driving role of p130Cas downstream of Kras through PI3K/AKT, thus indicating a rational therapeutic strategy of targeting the PI3K pathway in tumors with high expression of p130Cas.

Identifiants

pubmed: 34922945
pii: S0016-5085(21)04077-4
doi: 10.1053/j.gastro.2021.12.242
pii:
doi:

Substances chimiques

BCAR1 protein, human 0
Crk-Associated Substrate Protein 0
Proto-Oncogene Proteins c-akt EC 2.7.11.1
Proto-Oncogene Proteins p21(ras) EC 3.6.5.2

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1242-1255.e11

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.

Auteurs

Andrea Costamagna (A)

Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Turin, Italy. Electronic address: a.costamagna@unito.it.

Dora Natalini (D)

Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Turin, Italy.

Maria Del Pilar Camacho Leal (MDP)

Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Turin, Italy.

Matilde Simoni (M)

IRCCS Ospedale San Raffaele, Preclinical Models of Cancer Unit, Milan, Italy.

Luca Gozzelino (L)

Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Turin, Italy.

Paola Cappello (P)

Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Turin, Italy; Laboratory of Tumor Immunology, Center for Experimental Research and Medical Studies, Città della Salute e della Scienza di Torino, University of Torino, Torino, Italy.

Francesco Novelli (F)

Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Turin, Italy; Laboratory of Tumor Immunology, Center for Experimental Research and Medical Studies, Città della Salute e della Scienza di Torino, University of Torino, Torino, Italy.

Chiara Ambrogio (C)

Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Turin, Italy.

Paola Defilippi (P)

Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Turin, Italy. Electronic address: paola.defilippi@unito.it.

Emilia Turco (E)

Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Turin, Italy. Electronic address: emilio.hirsch@unito.it.

Elisa Giovannetti (E)

Cancer Pharmacology Laboratory, AIRC-Start-Up, Fondazione Pisana per la Scienza, San Giuliano Terme, Pisa, Italy; Department of Medical Oncology, Cancer Center Amsterdam, Amsterdam University Medical Centers, Vrije Universiteit, Amsterdam, The Netherlands.

Emilio Hirsch (E)

Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Turin, Italy.

Sara Cabodi (S)

Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Turin, Italy. Electronic address: sara.cabodi@unito.it.

Miriam Martini (M)

Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Turin, Italy. Electronic address: miriam.martini@unito.it.

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Classifications MeSH