A novel quinone-based derivative (DTNQ-Pro) induces apoptotic death via modulation of heat shock protein expression in Caco-2 cells

Br J Pharmacol. 2010 Jun;160(4):931-40. doi: 10.1111/j.1476-5381.2010.00718.x.

Abstract

Background and purpose: The resistance of human colon adenocarcinoma cells to antineoplastic agents may be related to the high endogenous expression of stress proteins, including the family of heat shock proteins (HSPs). Recently, a quinone-based pentacyclic derivative, DTNQ-Pro, showed high cytotoxic activity in human colon carcinoma cell lines. The aim of the present study was to determine the precise cellular mechanisms of this cytotoxic action of DTNQ-Pro.

Experimental approach: Using human colorectal carcinoma-derived Caco-2 cells as a model, we studied the effects of DTNQ-Pro on cellular viability and oxidative stress; HSP70 and HSP27 accumulation; and cell cycle, differentiation and apoptosis.

Key results: Incubation of Caco-2 cells with DTNQ-Pro reduced cell growth and increased the levels of reactive oxygen species in mitochondria. After 48 h of treatment, cells surviving showed an increased expression of Mn-superoxide dismutase (SOD), nitric oxide production and membrane lipid peroxidation. Treatment with DTNQ-Pro decreased HSP70 expression, and redistributed HSP27 and vimentin within the cell. DTNQ-Pro down-regulated the expression of A and B cyclins with arrest of the cell cycle in S phase and increased cellular differentiation. A second treatment of Caco-2 cells with DTNQ-Pro induced cellular death by activation of the apoptotic pathway.

Conclusions and implications: DTNQ-Pro causes Caco-2 cell death by induction of apoptosis via inhibition of HSP70 accumulation and the intracellular redistribution of HSP27. These findings suggest the potential use of DTNQ-Pro in combination chemotherapy for colon cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / drug therapy*
  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects*
  • Caco-2 Cells
  • Cell Differentiation / drug effects
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Colonic Neoplasms / drug therapy*
  • Down-Regulation / drug effects*
  • HSP27 Heat-Shock Proteins / metabolism
  • HSP70 Heat-Shock Proteins / metabolism
  • Heat-Shock Proteins / metabolism*
  • Humans
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Molecular Chaperones
  • Osmolar Concentration
  • Oxidative Stress / drug effects
  • Protein Transport / drug effects
  • Quinolines / pharmacology*
  • Quinones / pharmacology*
  • Reactive Oxygen Species / metabolism
  • S Phase / drug effects
  • Spiro Compounds / pharmacology*
  • Vimentin / metabolism

Substances

  • (3,3')spiro((hexahydropyrrolo(1,2-a)pyrazine-1,4-dione)-6,3'-(2',3'-dihydrothieno(2,3-b)naphtho-4',9'-dione))
  • Antineoplastic Agents
  • HSP27 Heat-Shock Proteins
  • HSP70 Heat-Shock Proteins
  • HSPB1 protein, human
  • Heat-Shock Proteins
  • Molecular Chaperones
  • Quinolines
  • Quinones
  • Reactive Oxygen Species
  • Spiro Compounds
  • Vimentin