Aggressive pancreatic ductal adenocarcinoma in mice caused by pancreas-specific blockade of transforming growth factor-beta signaling in cooperation with active Kras expression

Genes Dev. 2006 Nov 15;20(22):3147-60. doi: 10.1101/gad.1475506.

Abstract

Pancreatic ductal adenocarcinoma (PDAC) is an almost uniformly lethal disease in humans. Transforming growth factor-beta (TGF-beta) signaling plays an important role in PDAC progression, as indicated by the fact that Smad4, which encodes a central signal mediator downstream from TGF-beta, is deleted or mutated in 55% and the type II TGF-beta receptor (Tgfbr2) gene is altered in a smaller subset of human PDAC. Pancreas-specific Tgfbr2 knockout mice have been generated, alone or in the context of active Kras (Kras(G12D)) expression, using the Cre-loxP system driven by the endogenous Ptf1a (pancreatic transcription factor-1a) locus. Pancreas-selective Tgfbr2 knockout alone gave no discernable phenotype in 1.5 yr. Pancreas-specific Kras(G12D) activation alone essentially generated only intraepithelial neoplasia within 1 yr. In contrast, the Tgfbr2 knockout combined with Kras(G12D) expression developed well-differentiated PDAC with 100% penetrance and a median survival of 59 d. Heterozygous deletion of Tgfbr2 with Kras(G12D) expression also developed PDAC, which indicated a haploinsufficiency of TGF-beta signaling in this genetic context. The clinical and histopathological manifestations of the combined Kras(G12D) expression and Tgfbr2 knockout mice recapitulated human PDAC. The data show that blockade of TGF-beta signaling and activated Ras signaling cooperate to promote PDAC progression.

Publication types

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

MeSH terms

  • Adenocarcinoma / pathology*
  • Aging
  • Animals
  • Carcinoma, Pancreatic Ductal / pathology*
  • Connective Tissue Growth Factor
  • Disease Progression
  • Epithelium / pathology
  • Gene Expression*
  • Genes, ras*
  • Heterozygote
  • Immediate-Early Proteins / metabolism
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mutation / genetics
  • Neoplasm Invasiveness
  • Pancreas / cytology
  • Pancreas / growth & development
  • Pancreas / pathology
  • Pancreatic Neoplasms / pathology*
  • Protein Serine-Threonine Kinases
  • Receptor, Transforming Growth Factor-beta Type II
  • Receptors, Transforming Growth Factor beta / deficiency
  • Signal Transduction*
  • Stromal Cells / cytology
  • Stromal Cells / pathology
  • Transcription Factors / metabolism
  • Transforming Growth Factor beta / metabolism*
  • Tumor Cells, Cultured

Substances

  • CCN2 protein, human
  • CCN2 protein, mouse
  • Immediate-Early Proteins
  • Intercellular Signaling Peptides and Proteins
  • Receptors, Transforming Growth Factor beta
  • Transcription Factors
  • Transforming Growth Factor beta
  • transcription factor PTF1
  • Connective Tissue Growth Factor
  • Protein Serine-Threonine Kinases
  • Receptor, Transforming Growth Factor-beta Type II