Selective killing of hypoxia-inducible factor-1-active cells improves survival in a mouse model of invasive and metastatic pancreatic cancer

Clin Cancer Res. 2009 May 15;15(10):3433-41. doi: 10.1158/1078-0432.CCR-08-2267. Epub 2009 May 5.

Abstract

Purpose: Pancreatic cancer is characterized by intratumoral hypoxia, early and aggressive local invasion, and metastatic potential. Hypoxia-inducible factor-1 (HIF-1) is the major transcriptional activator of hypoxia-responsive genes and intratumoral hypoxia is associated with increased risk of metastasis. However, the behavior of the cells having HIF-1 activity during the malignant progression in pancreatic cancer has not been tested.

Experimental design: We orthotopically transplanted pancreatic cancer cells stably transfected with a HIF-1-dependent luciferase reporter gene and monitored HIF-1 activity in vivo in control and POP33-treated mice. POP33 is a novel prodrug, which has potential to increase caspase-3 activity and induce apoptosis in HIF-1-active/hypoxic cells.

Results: In vivo optical imaging showed that HIF-1 activity proceeded along with local invasion, the peritoneal dissemination, and the liver metastasis. HIF-1-active hypoxic cells were selectively eradicated by POP33. Moreover, selective killing of HIF-1-active hypoxic cells significantly suppressed malignant progression, resulting in a significant improvement in survival rate.

Conclusions: These results show that HIF-1-active cells constitute a large proportion of invading and metastatic cells and suggest that eradication of these cells may improve the outcome in advanced pancreatic cancer, a condition for which no effective therapy currently exists.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Abdominal Cavity / pathology
  • Amino Acid Sequence
  • Animals
  • Caspase 3 / metabolism
  • Cell Line, Tumor
  • Disease Progression
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Humans
  • Hypoxia-Inducible Factor 1 / genetics
  • Hypoxia-Inducible Factor 1 / metabolism*
  • Liver Neoplasms / drug therapy*
  • Liver Neoplasms / metabolism
  • Liver Neoplasms / secondary
  • Luciferases / genetics
  • Luciferases / metabolism
  • Luminescent Measurements / methods
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Molecular Sequence Data
  • Neoplasm Invasiveness
  • Oxygen / metabolism
  • Pancreatic Neoplasms / drug therapy*
  • Pancreatic Neoplasms / metabolism
  • Pancreatic Neoplasms / pathology
  • Peritoneum / drug effects
  • Peritoneum / metabolism
  • Peritoneum / pathology
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / pharmacology*
  • Survival Analysis
  • Transfection
  • Xenograft Model Antitumor Assays

Substances

  • Hypoxia-Inducible Factor 1
  • Recombinant Fusion Proteins
  • TOP3 fusion protein
  • Green Fluorescent Proteins
  • Luciferases
  • Caspase 3
  • Oxygen