Loss of HIF1A From Pancreatic Cancer Cells Increases Expression of PPP1R1B and Degradation of p53 to Promote Invasion and Metastasis.


Journal

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

Informations de publication

Date de publication:
11 2020
Historique:
received: 14 11 2019
revised: 11 07 2020
accepted: 27 07 2020
pubmed: 10 8 2020
medline: 13 4 2021
entrez: 10 8 2020
Statut: ppublish

Résumé

Pancreatic ductal adenocarcinomas (PDACs) are hypovascular, resulting in the up-regulation of hypoxia inducible factor 1 alpha (HIF1A), which promotes the survival of cells under low-oxygen conditions. We studied the roles of HIF1A in the development of pancreatic tumors in mice. We performed studies with Kras EKPC mice with pancreas-specific deletion of HIF1A developed more advanced pancreatic neoplasias and PDACs with more invasion and metastasis, and had significantly shorter survival times, than EKPC mice. Pancreatic cancer cells from these tumors had higher invasive and metastatic activity in culture than cells from tumors of EKPC mice. HIF1A-knockout pancreatic cancer cells had increased expression of protein phosphatase 1 regulatory inhibitor subunit 1B (PPP1R1B). There was an inverse correlation between levels of HIF1A and PPP1R1B in human PDAC tumors; higher expression of PPP1R1B correlated with shorter survival times of patients. Metastatic human pancreatic cancer cell lines had increased levels of PPP1R1B and lower levels of HIF1A compared with nonmetastatic cancer cell lines; knockdown of PPP1R1B significantly reduced the ability of pancreatic cancer cells to form lung metastases in mice. PPP1R1B promoted degradation of p53 by stabilizing phosphorylation of MDM2 at Ser166. HIF1A can act a tumor suppressor by preventing the expression of PPP1R1B and subsequent degradation of the p53 protein in pancreatic cancer cells. Loss of HIF1A from pancreatic cancer cells increases their invasive and metastatic activity.

Sections du résumé

BACKGROUND & AIMS
Pancreatic ductal adenocarcinomas (PDACs) are hypovascular, resulting in the up-regulation of hypoxia inducible factor 1 alpha (HIF1A), which promotes the survival of cells under low-oxygen conditions. We studied the roles of HIF1A in the development of pancreatic tumors in mice.
METHODS
We performed studies with Kras
RESULTS
EKPC mice with pancreas-specific deletion of HIF1A developed more advanced pancreatic neoplasias and PDACs with more invasion and metastasis, and had significantly shorter survival times, than EKPC mice. Pancreatic cancer cells from these tumors had higher invasive and metastatic activity in culture than cells from tumors of EKPC mice. HIF1A-knockout pancreatic cancer cells had increased expression of protein phosphatase 1 regulatory inhibitor subunit 1B (PPP1R1B). There was an inverse correlation between levels of HIF1A and PPP1R1B in human PDAC tumors; higher expression of PPP1R1B correlated with shorter survival times of patients. Metastatic human pancreatic cancer cell lines had increased levels of PPP1R1B and lower levels of HIF1A compared with nonmetastatic cancer cell lines; knockdown of PPP1R1B significantly reduced the ability of pancreatic cancer cells to form lung metastases in mice. PPP1R1B promoted degradation of p53 by stabilizing phosphorylation of MDM2 at Ser166.
CONCLUSIONS
HIF1A can act a tumor suppressor by preventing the expression of PPP1R1B and subsequent degradation of the p53 protein in pancreatic cancer cells. Loss of HIF1A from pancreatic cancer cells increases their invasive and metastatic activity.

Identifiants

pubmed: 32768595
pii: S0016-5085(20)35009-5
doi: 10.1053/j.gastro.2020.07.046
pmc: PMC7680408
mid: NIHMS1618842
pii:
doi:

Substances chimiques

Dopamine and cAMP-Regulated Phosphoprotein 32 0
HIF1A protein, human 0
Hif1a protein, mouse 0
Homeodomain Proteins 0
Hypoxia-Inducible Factor 1, alpha Subunit 0
PPP1R1B protein, human 0
Ppp1r1b protein, mouse 0
TP53 protein, human 0
Trans-Activators 0
Trp53 protein, mouse 0
Tumor Suppressor Protein p53 0
pancreatic and duodenal homeobox 1 protein 0
Hras protein, mouse EC 3.6.5.2
Proto-Oncogene Proteins p21(ras) EC 3.6.5.2

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

1882-1897.e5

Subventions

Organisme : NCI NIH HHS
ID : R01 CA207189
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA200643
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA030199
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA181385
Pays : United States
Organisme : NCI NIH HHS
ID : U54 CA210190
Pays : United States

Informations de copyright

Copyright © 2020 AGA Institute. Published by Elsevier Inc. All rights reserved.

Auteurs

Ashutosh Tiwari (A)

Tumor Initiation and Maintenance Program, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California. Electronic address: atiwari@sbpdiscovery.org.

Kojiro Tashiro (K)

Tumor Initiation and Maintenance Program, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.

Ajay Dixit (A)

Department of Biomedical Engineering, University of Minnesota, Minneapolis, Minnesota.

Aditi Soni (A)

Tumor Initiation and Maintenance Program, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.

Keianna Vogel (K)

Tumor Initiation and Maintenance Program, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.

Bryan Hall (B)

Tumor Initiation and Maintenance Program, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.

Iram Shafqat (I)

Masonic Cancer Center, University of Minnesota, Minneapolis, Minnesota.

Joseph Slaughter (J)

Masonic Cancer Center, University of Minnesota, Minneapolis, Minnesota.

Nesteen Param (N)

Masonic Cancer Center, University of Minnesota, Minneapolis, Minnesota.

An Le (A)

Masonic Cancer Center, University of Minnesota, Minneapolis, Minnesota.

Emily Saunders (E)

Masonic Cancer Center, University of Minnesota, Minneapolis, Minnesota.

Utkarsha Paithane (U)

Tumor Initiation and Maintenance Program, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.

Guillermina Garcia (G)

Histology Core, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.

Alexandre Rosa Campos (AR)

Proteomics Core, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.

Jon Zettervall (J)

Department of Biomedical Engineering, University of Minnesota, Minneapolis, Minnesota.

Marjorie Carlson (M)

Department of Biomedical Engineering, University of Minnesota, Minneapolis, Minnesota.

Timothy K Starr (TK)

Department of Obstetrics, Gynecology and Women's Health, University of Minnesota, Minneapolis, Minnesota.

York Marahrens (Y)

Department of Genetics, Cell Biology and Development, University of Minnesota, Minneapolis, Minnesota.

Aniruddha J Deshpande (AJ)

Tumor Initiation and Maintenance Program, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.

Cosimo Commisso (C)

Tumor Initiation and Maintenance Program, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.

Paolo P Provenzano (PP)

Department of Biomedical Engineering, University of Minnesota, Minneapolis, Minnesota.

Anindya Bagchi (A)

Tumor Initiation and Maintenance Program, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California. Electronic address: abagchi@sbpdiscovery.org.

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Classifications MeSH