Resveratrol induces AMPK-dependent MDR1 inhibition in colorectal cancer HCT116/L-OHP cells by preventing activation of NF-κB signaling and suppressing cAMP-responsive element transcriptional activity

Tumour Biol. 2015 Dec;36(12):9499-510. doi: 10.1007/s13277-015-3636-3. Epub 2015 Jul 1.

Abstract

Resveratrol, a natural polyphenolic compound found in foods and beverages, has attracted increasing attention in recent years because of its potent chemopreventive and anti-tumor effects. In this study, the effects of resveratrol on the expression of P-glycoprotein/multi-drug resistance protein 1 (P-gp/MDR1), and the underlying molecular mechanisms, were investigated in oxaliplatin (L-OHP)-resistant colorectal cancer cells (HCT116/L-OHP). Resveratrol downregulated MDR1 protein and mRNA expression levels and reduced MDR1 promoter activity. It also enhanced the intracellular accumulation of rhodamine 123, suggesting that resveratrol can reverse multi-drug resistance by downregulating MDR1 expression and reducing drug efflux. Resveratrol treatment also reduced nuclear factor-κB (NF-κB) activity, reduced phosphorylation levels of IκBα, and reduced nuclear translocation of the NF-κB subunit p65. Moreover, downregulation of MDR1 expression and promoter activity was mediated by resveratrol-induced AMP-activated protein kinase (AMPK) phosphorylation. The inhibitory effects of resveratrol on MDR1 expression and cAMP-responsive element-binding protein (CREB) phosphorylation were reversed by AMPKα siRNA transfection. We found that the transcriptional activity of cAMP-responsive element (CRE) was inhibited by resveratrol. These results demonstrated that the inhibitory effects of resveratrol on MDR1 expression in HCT116/L-OHP cells were closely associated with the inhibition of NF-κB signaling and CREB activation in an AMPK-dependent manner.

Keywords: AMPKα; Colorectal cancer; Multi-drug resistance; Resveratrol.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases / biosynthesis*
  • AMP-Activated Protein Kinases / genetics
  • ATP Binding Cassette Transporter, Subfamily B / biosynthesis
  • ATP Binding Cassette Transporter, Subfamily B / genetics
  • ATP Binding Cassette Transporter, Subfamily B, Member 1 / genetics
  • Colorectal Neoplasms / drug therapy
  • Colorectal Neoplasms / genetics*
  • Colorectal Neoplasms / pathology
  • Cyclic AMP Response Element-Binding Protein / genetics
  • Doxorubicin / administration & dosage
  • Drug Resistance, Multiple / genetics
  • Drug Resistance, Neoplasm / genetics
  • Gene Expression Regulation, Neoplastic / drug effects
  • HCT116 Cells
  • Humans
  • I-kappa B Proteins / biosynthesis
  • I-kappa B Proteins / genetics
  • NF-KappaB Inhibitor alpha
  • Organoplatinum Compounds / administration & dosage
  • Oxaliplatin
  • Resveratrol
  • Signal Transduction / drug effects
  • Stilbenes / administration & dosage*
  • Transcriptional Activation / drug effects
  • eIF-2 Kinase / biosynthesis
  • eIF-2 Kinase / genetics*

Substances

  • ABCB1 protein, human
  • ATP Binding Cassette Transporter, Subfamily B
  • ATP Binding Cassette Transporter, Subfamily B, Member 1
  • Cyclic AMP Response Element-Binding Protein
  • I-kappa B Proteins
  • NFKBIA protein, human
  • Organoplatinum Compounds
  • Stilbenes
  • Oxaliplatin
  • NF-KappaB Inhibitor alpha
  • Doxorubicin
  • eIF-2 Kinase
  • AMP-Activated Protein Kinases
  • Resveratrol