Slug-dependent upregulation of L1CAM is responsible for the increased invasion potential of pancreatic cancer cells following long-term 5-FU treatment

PLoS One. 2015 Apr 10;10(4):e0123684. doi: 10.1371/journal.pone.0123684. eCollection 2015.

Abstract

Background: Pancreatic adenocarcinoma is a lethal disease with 5-year survival of less than 5%. 5-fluorouracil (5-FU) is a principal first-line therapy, but treatment only extends survival modestly and is seldom curative. Drug resistance and disease recurrence is typical and there is a pressing need to overcome this. To investigate acquired 5-FU resistance in pancreatic adenocarcinoma, we established chemoresistant monoclonal cell lines from the Panc 03.27 cell line by long-term exposure to increasing doses of 5-FU.

Results: 5-FU-resistant cell lines exhibited increased expression of markers associated with multidrug resistance explaining their reduced sensitivity to 5-FU. In addition, 5-FU-resistant cell lines showed alterations typical for an epithelial-to-mesenchymal transition (EMT), including upregulation of mesenchymal markers and increased invasiveness. Microarray analysis revealed the L1CAM pathway as one of the most upregulated pathways in the chemoresistant clones, and a significant upregulation of L1CAM was seen on the RNA and protein level. In pancreatic cancer, expression of L1CAM is associated with a chemoresistant and migratory phenotype. Using esiRNA targeting L1CAM, or by blocking the extracellular part of L1CAM with antibodies, we show that the increased invasiveness observed in the chemoresistant cells functionally depends on L1CAM. Using esiRNA targeting β-catenin and/or Slug, we demonstrate that in the chemoresistant cell lines, L1CAM expression depends on Slug rather than β-catenin.

Conclusion: Our findings establish Slug-induced L1CAM expression as a mediator of a chemoresistant and migratory phenotype in pancreatic adenocarcinoma cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis / genetics
  • Cell Line, Tumor
  • Cell Proliferation
  • Drug Resistance, Neoplasm / genetics
  • Epithelial-Mesenchymal Transition / genetics
  • Fluorouracil / pharmacology
  • Fluorouracil / therapeutic use
  • Gene Expression Regulation, Neoplastic*
  • Humans
  • Neoplasm Invasiveness
  • Neural Cell Adhesion Molecule L1 / genetics*
  • Pancreatic Neoplasms / drug therapy
  • Pancreatic Neoplasms / genetics*
  • Pancreatic Neoplasms / metabolism*
  • Pancreatic Neoplasms / pathology
  • Snail Family Transcription Factors
  • Transcription Factors / metabolism*
  • Transcription, Genetic
  • Up-Regulation
  • beta Catenin / metabolism

Substances

  • Neural Cell Adhesion Molecule L1
  • SNAI1 protein, human
  • Snail Family Transcription Factors
  • Transcription Factors
  • beta Catenin
  • Fluorouracil

Grants and funding

KL is founded by the Research Council of Norway, grant nr. 205783, and Affitech Research AS. Affitech Research AS partly supported KL during an industrial PhD, together with the Research Council of Norway, grant nr. 205783. AU was funded by Molecular Life Sciences (University of Oslo) and Helse Sor-Ost. NS was funded by the Norwegian Cancer Society. JLD was funded by The Research Council of Norway. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.