Cycloart-24-ene-26-ol-3-one, a New Cycloartane Isolated from Leaves of Aglaia exima Triggers Tumour Necrosis Factor-Receptor 1-Mediated Caspase-Dependent Apoptosis in Colon Cancer Cell Line

PLoS One. 2016 Apr 12;11(4):e0152652. doi: 10.1371/journal.pone.0152652. eCollection 2016.

Abstract

Plants in the Meliaceae family are known to possess interesting biological activities, such as antimalaral, antihypertensive and antitumour activities. Previously, our group reported the plant-derived compound cycloart-24-ene-26-ol-3-one isolated from the hexane extracts of Aglaia exima leaves, which shows cytotoxicity towards various cancer cell lines, in particular, colon cancer cell lines. In this report, we further demonstrate that cycloart-24-ene-26-ol-3-one, from here forth known as cycloartane, reduces the viability of the colon cancer cell lines HT-29 and CaCO-2 in a dose- and time-dependent manner. Further elucidation of the compound's mechanism showed that it binds to tumour necrosis factor-receptor 1 (TNF-R1) leading to the initiation of caspase-8 and, through the activation of Bid, in the activation of caspase-9. This activity causes a reduction in mitochondrial membrane potential (MMP) and the release of cytochrome-C. The activation of caspase-8 and -9 both act to commit the cancer cells to apoptosis through downstream caspase-3/7 activation, PARP cleavage and the lack of NFkB translocation into the nucleus. A molecular docking study showed that the cycloartane binds to the receptor through a hydrophobic interaction with cysteine-96 and hydrogen bonds with lysine-75 and -132. The results show that further development of the cycloartane as an anti-cancer drug is worthwhile.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aglaia / chemistry*
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology
  • Apoptosis / drug effects*
  • Caco-2 Cells
  • Caspases / metabolism
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Colonic Neoplasms / drug therapy*
  • Colonic Neoplasms / metabolism
  • Cytochromes c / metabolism
  • HT29 Cells
  • Humans
  • Membrane Potential, Mitochondrial / drug effects
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Plant Leaves / chemistry*
  • Receptors, Tumor Necrosis Factor, Type I / metabolism*
  • Triterpenes / chemistry
  • Triterpenes / pharmacology*

Substances

  • Antineoplastic Agents
  • Receptors, Tumor Necrosis Factor, Type I
  • Triterpenes
  • cycloartane
  • Cytochromes c
  • Caspases

Grants and funding

This work was supported by the University of Malaya [grants RP001/2012A, RP001A-13BIO]; University Malaya High Impact Research [grant H-20001-E00002]; and the Ministry of Higher Education of Malaysia [grant FP006-2011A]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.