Matrine suppresses KRAS-driven pancreatic cancer growth by inhibiting autophagy-mediated energy metabolism

Mol Oncol. 2018 Jun;12(7):1203-1215. doi: 10.1002/1878-0261.12324. Epub 2018 Jun 11.

Abstract

Matrine is a natural compound extracted from the herb Sophora flavescens Ait which is widely used in traditional Chinese medicine for treating various diseases. Recently, matrine was reported to have antitumor effects against a variety of cancers without any obvious side effects; however, the molecular mechanisms of its antiproliferative effects on cancer are unclear. Here, we report that matrine inhibits autophagy-mediated energy metabolism, which is necessary for pancreatic cancer growth. We found that matrine significantly reduces pancreatic cancer growth in vitro and in vivo by insufficiently maintaining mitochondrial metabolic function and energy level. We also found that either pyruvate or α-ketoglutarate supplementation markedly rescues pancreatic cancer cell growth following matrine treatment. Inhibition of mitochondrial energy production results from matrine-mediated autophagy inhibition by impairing the function of lysosomal protease. Matrine-mediated autophagy inhibition requires stat3 downregulation. Furthermore, we found that the antitumor effect of matrine on pancreatic cancer growth depends on the mutation of the KRAS oncogene. Together, our data suggest that matrine can suppress the growth of KRAS-mutant pancreatic cancer by inhibiting autophagy-mediated energy metabolism.

Keywords: KRAS; autophagy; lysosomal protease; metabolism; pancreatic cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / metabolism
  • Adenocarcinoma / pathology
  • Alkaloids / pharmacology*
  • Autophagy / drug effects*
  • Cathepsins / metabolism
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Citric Acid Cycle / drug effects
  • Energy Metabolism / drug effects*
  • Humans
  • Lysosomes / drug effects
  • Lysosomes / metabolism
  • Matrines
  • Mutation / genetics
  • Pancreatic Neoplasms / metabolism*
  • Pancreatic Neoplasms / pathology*
  • Peptide Hydrolases / metabolism
  • Proto-Oncogene Proteins p21(ras) / genetics
  • Proto-Oncogene Proteins p21(ras) / metabolism*
  • Quinolizines / pharmacology*
  • STAT3 Transcription Factor / metabolism
  • Vacuoles / drug effects
  • Vacuoles / metabolism
  • Vacuoles / ultrastructure

Substances

  • Alkaloids
  • KRAS protein, human
  • Quinolizines
  • STAT3 Transcription Factor
  • Cathepsins
  • Peptide Hydrolases
  • Proto-Oncogene Proteins p21(ras)
  • Matrines