Feroniellin A-induced autophagy causes apoptosis in multidrug-resistant human A549 lung cancer cells

Int J Oncol. 2014 Apr;44(4):1233-42. doi: 10.3892/ijo.2014.2297. Epub 2014 Feb 11.

Abstract

During the screening of natural chemicals that can reverse multidrug resistance in human A549 lung cancer cells resistant to etoposide (A549RT-eto), we discovered that Feroniellin A (FERO), a novel furanocoumarin, shows toxicity toward A549RT-eto cells in a dose- and time-dependent manner. FERO reduced the expression of NF-κB, leading to downregulation of P-glycoprotein (P-gp), encoded by MDR1, which eventually sensitized A549RT-eto cells to apoptosis. FERO specifically diminished transcription and promoter activity of MDR1 but did not inhibit the expression of other multidrug resistance genes MRP2 and BCRP. Moreover, co-administration of FERO with Bay11-7802, an inhibitor of NF-κB, accelerated apoptosis of A549RT-eto cells through decreased expression of P-gp, indicating that NF-κB is involved in multidrug resistance. Conversely, addition of Z-VAD, a pan-caspase inhibitor, blocked FERO-induced apoptosis in A549RT-eto cells but did not block downregulation of P-gp, indicating that a decrease in P-gp expression is necessary but not sufficient for FERO-induced apoptosis. Interestingly, we found that FERO also induces autophagy, which is characterized by the conversion of LC3 I to LC3 II, induction of GFP-LC3 puncta, enhanced expression of Beclin-1 and ATG5, and inactivation of mTOR. Furthermore, suppression of Beclin-1 by siRNA reduced FERO-induced apoptosis in A549RT-eto cells and activation of autophagy by rapamycin accelerated FERO-induced apoptosis, suggesting that autophagy plays an active role in FERO-induced apoptosis. Herein, we report that FERO reverses multidrug resistance in A549RT-eto cells and exerts its cytotoxic effect by induction of both autophagy and apoptosis, which suggests that FERO can be a useful anticancer drug for multidrug-resistant lung cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter, Subfamily B / biosynthesis
  • Antineoplastic Agents / pharmacology
  • Apoptosis / drug effects*
  • Apoptosis / genetics
  • Apoptosis Regulatory Proteins / genetics
  • Autophagy / drug effects
  • Beclin-1
  • Cell Line, Tumor
  • Coumarins / pharmacology*
  • Drug Resistance, Neoplasm / drug effects
  • Etoposide / pharmacology
  • Furans / pharmacology*
  • Glycosides / pharmacology*
  • Humans
  • Lung Neoplasms / drug therapy*
  • Membrane Proteins / genetics
  • Microfilament Proteins
  • Nitriles / pharmacology
  • Promoter Regions, Genetic
  • RNA Interference
  • RNA, Small Interfering
  • Sirolimus / pharmacology
  • Sulfones / pharmacology
  • Transcription Factor RelA / antagonists & inhibitors
  • Transcription Factor RelA / biosynthesis*
  • Transcription, Genetic

Substances

  • 3-(4-methylphenylsulfonyl)-2-propenenitrile
  • ABCB1 protein, human
  • ATP Binding Cassette Transporter, Subfamily B
  • Antineoplastic Agents
  • Apoptosis Regulatory Proteins
  • BECN1 protein, human
  • Beclin-1
  • Coumarins
  • Furans
  • Glycosides
  • KLHL1 protein, human
  • Membrane Proteins
  • Microfilament Proteins
  • Nitriles
  • RELA protein, human
  • RNA, Small Interfering
  • Sulfones
  • Transcription Factor RelA
  • feronielloside
  • Etoposide
  • Sirolimus