Abstract
Efforts to model pancreatic cancer in mice have focused on mimicking genetic changes found in the human disease, particularly the activating KRAS mutations that occur in pancreatic tumors and their putative precursors, pancreatic intraepithelial neoplasia (PanIN). Although activated mouse Kras mutations induce PanIN lesions similar to those of human, only a small minority of cells that express mutant Kras go on to form PanINs. The basis for this selective response is unknown, and it is similarly unknown what cell types in the mature pancreas actually contribute to PanINs. One clue comes from the fact that PanINs, unlike most cells in the adult pancreas, exhibit active Notch signaling. We hypothesize that Notch, which inhibits differentiation in the embryonic pancreas, contributes to PanIN formation by abrogating the normal differentiation program of tumor-initiating cells. Through conditional expression in the mouse pancreas, we find dramatic synergy between activated Notch and Kras in inducing PanIN formation. Furthermore, we find that Kras activation in mature acinar cells induces PanIN lesions identical to those seen upon ubiquitous Kras activation, and that Notch promotes both initiation and dysplastic progression of these acinar-derived PanINs, albeit short of invasive adenocarcinoma. At the cellular level, Notch/Kras coactivation promotes rapid reprogramming of acinar cells to a duct-like phenotype, providing an explanation for how a characteristically ductal tumor can arise from nonductal acinar cells.
MeSH Terms
Animals
Carcinoma, Pancreatic Ductal/metabolism,pathology
Estrogen Antagonists/metabolism
Female
Humans
Mice
Pancreatic Ducts/cytology,metabolism,pathology
Pancreatic Neoplasms/metabolism,pathology
Precancerous Conditions/metabolism,pathology
Pregnancy
Proto-Oncogene Proteins/genetics,metabolism
Proto-Oncogene Proteins p21(ras)
Receptors, Notch/genetics,metabolism
Signal Transduction/physiology
Tamoxifen/metabolism
Transgenes
ras Proteins/genetics,metabolism
Chemicals
Estrogen Antagonists
KRAS protein, human
Proto-Oncogene Proteins
Receptors, Notch
Tamoxifen
Proto-Oncogene Proteins p21(ras)
ras Proteins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
De La O Jean-Paul
Department of Human Genetics, University of Utah, 15 North 2030 East, Room 2100, Salt Lake City, UT 84112, USA.
Emerson Lyska L
Goodman Jessica L
Froebe Scott C
Illum Benjamin E
Curtis Andrew B
Murtaugh L Charles
References (27)
27 references, click to expand
-
The Nestin progenitor lineage is the compartment of origin for pancreatic intraepithelial neoplasia.
Proc Natl Acad Sci U S A. 2007 Mar 13;104(11):4437-42
PMID: 17360542
-
Gene regulatory factors in pancreatic development.
Dev Dyn. 2004 Jan;229(1):176-200
PMID: 14699589
-
Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors.
Development. 2002 May;129(10):2447-57
PMID: 11973276
-
Mist1-KrasG12D knock-in mice develop mixed differentiation metastatic exocrine pancreatic carcinoma and hepatocellular carcinoma.
Cancer Res. 2006 Jan 1;66(1):242-7
PMID: 16397237
-
The love-hate relationship between Ras and Notch.
Genes Dev. 2005 Aug 15;19(16):1825-39
PMID: 16103211
-
Recapitulation of elements of embryonic development in adult mouse pancreatic regeneration.
Gastroenterology. 2005 Mar;128(3):728-41
PMID: 15765408
-
Pancreatic cancer.
Annu Rev Pathol. 2008;3:157-88
PMID: 18039136
-
Notch mediates TGF alpha-induced changes in epithelial differentiation during pancreatic tumorigenesis.
Cancer Cell. 2003 Jun;3(6):565-76
PMID: 12842085
-
Beta-catenin is essential for pancreatic acinar but not islet development.
Development. 2005 Nov;132(21):4663-74
PMID: 16192304
-
Notch signaling controls multiple steps of pancreatic differentiation.
Proc Natl Acad Sci U S A. 2003 Dec 9;100(25):14920-5
PMID: 14657333
-
Increased expression of hypoxia-inducible factor-1alpha, p48, and the Notch signaling cascade during acute pancreatitis in mice.
Pancreas. 2004 Jan;28(1):58-64
PMID: 14707731
-
Activation of Notch-1 signaling maintains the neoplastic phenotype in human Ras-transformed cells.
Nat Med. 2002 Sep;8(9):979-86
PMID: 12185362
-
Pancreatic epithelial plasticity mediated by acinar cell transdifferentiation and generation of nestin-positive intermediates.
Development. 2005 Aug;132(16):3767-76
PMID: 16020518
-
Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice.
Cancer Cell. 2007 Mar;11(3):291-302
PMID: 17349585
-
Preinvasive pancreatic neoplasia of ductal phenotype induced by acinar cell targeting of mutant Kras in transgenic mice.
Cancer Res. 2003 May 1;63(9):2016-9
PMID: 12727811
-
Pten constrains centroacinar cell expansion and malignant transformation in the pancreas.
Cancer Cell. 2005 Sep;8(3):185-95
PMID: 16169464
-
Notch signaling is required for exocrine regeneration after acute pancreatitis.
Gastroenterology. 2008 Feb;134(2):544-55
PMID: 18242220
-
Tumor induction by an endogenous K-ras oncogene is highly dependent on cellular context.
Cancer Cell. 2003 Aug;4(2):111-20
PMID: 12957286
-
In vivo lineage tracing defines the role of acinar-to-ductal transdifferentiation in inflammatory ductal metaplasia.
Gastroenterology. 2007 Dec;133(6):1999-2009
PMID: 18054571
-
Isolation of RNA using guanidinium salts.
Methods Enzymol. 1987;152:219-27
PMID: 2443794
-
Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma.
Genes Dev. 2003 Dec 15;17(24):3112-26
PMID: 14681207
-
Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras.
Genes Dev. 2001 Dec 15;15(24):3243-8
PMID: 11751630
-
Pathology of genetically engineered mouse models of pancreatic exocrine cancer: consensus report and recommendations.
Cancer Res. 2006 Jan 1;66(1):95-106
PMID: 16397221
-
Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse.
Cancer Cell. 2003 Dec;4(6):437-50
PMID: 14706336
-
The mutant K-ras oncogene causes pancreatic periductal lymphocytic infiltration and gastric mucous neck cell hyperplasia in transgenic mice.
Cancer Res. 2003 May 1;63(9):2005-9
PMID: 12727809
-
A PCR primer bank for quantitative gene expression analysis.
Nucleic Acids Res. 2003 Dec 15;31(24):e154
PMID: 14654707
-
Acinar cells contribute to the molecular heterogeneity of pancreatic intraepithelial neoplasia.
Am J Pathol. 2007 Jul;171(1):263-73
PMID: 17591971