The HMGA1-COX-2 axis: a key molecular pathway and potential target in pancreatic adenocarcinoma

Pancreatology. 2012 Jul-Aug;12(4):372-9. doi: 10.1016/j.pan.2012.05.005. Epub 2012 May 29.

Abstract

Context: Although pancreatic cancer is a common, highly lethal malignancy, the molecular events that enable precursor lesions to become invasive carcinoma remain unclear. We previously reported that the high-mobility group A1 (HMGA1) protein is overexpressed in >90% of primary pancreatic cancers, with absent or low levels in early precursor lesions.

Methods: Here, we investigate the role of HMGA1 in reprogramming pancreatic epithelium into invasive cancer cells. We assessed oncogenic properties induced by HMGA1 in non-transformed pancreatic epithelial cells expressing activated K-RAS. We also explored the HMGA1-cyclooxygenase (COX-2) pathway in human pancreatic cancer cells and the therapeutic effects of COX-2 inhibitors in xenograft tumorigenesis.

Results: HMGA1 cooperates with activated K-RAS to induce migration, invasion, and anchorage-independent cell growth in a cell line derived from normal human pancreatic epithelium. Moreover, HMGA1 and COX-2 expression are positively correlated in pancreatic cancer cell lines (r(2) = 0.93; p < 0.001). HMGA1 binds directly to the COX-2 promoter at an AT-rich region in vivo in three pancreatic cancer cell lines. In addition, HMGA1 induces COX-2 expression in pancreatic epithelial cells, while knock-down of HMGA1 results in repression of COX-2 in pancreatic cancer cells. Strikingly, we also discovered that Sulindac (a COX-1/COX-2 inhibitor) or Celecoxib (a more specific COX-2 inhibitor) block xenograft tumorigenesis from pancreatic cancer cells expressing high levels of HMGA1.

Conclusions: Our studies identify for the first time an important role for the HMGA1-COX-2 pathway in pancreatic cancer and suggest that targeting this pathway could be effective to treat, or even prevent, pancreatic cancer.

Publication types

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

MeSH terms

  • Adenocarcinoma / drug therapy
  • Adenocarcinoma / genetics*
  • Adenocarcinoma / prevention & control
  • Animals
  • Celecoxib
  • Cell Division / genetics
  • Cell Line, Tumor
  • Cell Movement / genetics
  • Cyclooxygenase 2 / genetics*
  • Cyclooxygenase 2 / physiology
  • Cyclooxygenase Inhibitors / administration & dosage
  • Gene Expression
  • HMGA1a Protein / genetics*
  • HMGA1a Protein / physiology
  • Humans
  • Mice
  • Mice, Nude
  • Neoplasm Invasiveness / genetics
  • Neoplasm Metastasis / genetics
  • Neoplasm Transplantation
  • Pancreatic Neoplasms / drug therapy
  • Pancreatic Neoplasms / genetics*
  • Pancreatic Neoplasms / prevention & control
  • Pyrazoles / administration & dosage
  • Sulfonamides / administration & dosage
  • Sulindac / administration & dosage
  • Transplantation, Heterologous
  • ras Proteins / physiology

Substances

  • Cyclooxygenase Inhibitors
  • Pyrazoles
  • Sulfonamides
  • HMGA1a Protein
  • Sulindac
  • Cyclooxygenase 2
  • ras Proteins
  • Celecoxib