Phase-II metabolism limits the antiproliferative activity of urolithins in human colon cancer cells

Eur J Nutr. 2014 Apr;53(3):853-64. doi: 10.1007/s00394-013-0589-4.

Abstract

Purpose: Urolithins, gut microbiota metabolites derived from ellagic acid and ellagitannins, reach micromolar concentrations in the colon lumen where can have anti-inflammatory and anticancer effects. The antiproliferative activity of urolithins (Uro-A, Uro-B, Uro-C and Uro-D) and their most relevant in vivo glucuronides were evaluated in three human colon cancer cell lines (Caco-2, SW480 and HT-29).

Methods: Cell proliferation was evaluated by 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2H-tetrazolium bromide and Trypan blue exclusion assays. Cell cycle was evaluated by flow cytometry and urolithins metabolism by HPLC–MS/MS.

Results: Urolithins inhibited cell proliferation and cell cycle progression in a time- and dose-dependent manner and arrested the cells at S and G2/M phases, depending on the urolithin. Uro-A exerted the highest antiproliferative activity, followed by Uro-C, Uro-D and Uro-B. Unlike Caco-2 and SW480 cells, HT-29 cells partially overcame the effects after 48 h, which was related to the complete glucuronidation of urolithins. Uro-A or Uro-B glucuronides did not affect cell cycle and showed lower antiproliferative activity than their aglycone counterparts. Uro-A or Uro-B plus inhibitors of drug efflux ABC transporters partially prevented the glucuronidation of urolithins in HT-29 cells which became more sensitive.

Conclusions: Uro-A, Uro-B, Uro-C and Uro-D exerted different antiproliferative effects depending on the colon cancer cell line. We also report here, for the first time, the role of ABC transporters and Phase-II metabolism in HT-29 cells as a mechanism of cancer resistance against urolithins due to their conversion to glucuronide conjugates that exerted lower antiproliferative activity.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP-Binding Cassette Transporters / antagonists & inhibitors
  • ATP-Binding Cassette Transporters / metabolism
  • Anti-Inflammatory Agents, Non-Steroidal / antagonists & inhibitors
  • Anti-Inflammatory Agents, Non-Steroidal / chemistry
  • Anti-Inflammatory Agents, Non-Steroidal / metabolism
  • Anti-Inflammatory Agents, Non-Steroidal / pharmacology
  • Antibiotics, Antineoplastic / chemistry
  • Antibiotics, Antineoplastic / metabolism
  • Antibiotics, Antineoplastic / pharmacology*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Colon / drug effects
  • Colon / metabolism
  • Colonic Neoplasms / drug therapy*
  • Colonic Neoplasms / metabolism
  • Coumarins / antagonists & inhibitors
  • Coumarins / chemistry
  • Coumarins / metabolism
  • Coumarins / pharmacology*
  • Drug Resistance, Neoplasm / drug effects
  • G2 Phase / drug effects
  • Glucuronides / chemistry
  • Glucuronides / metabolism
  • Humans
  • Hydrolyzable Tannins / antagonists & inhibitors
  • Hydrolyzable Tannins / chemistry
  • Hydrolyzable Tannins / metabolism
  • Hydrolyzable Tannins / pharmacology*
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / metabolism
  • Kinetics
  • Membrane Transport Modulators / pharmacology
  • Metabolic Detoxication, Phase II*
  • S Phase / drug effects

Substances

  • ATP-Binding Cassette Transporters
  • Anti-Inflammatory Agents, Non-Steroidal
  • Antibiotics, Antineoplastic
  • Coumarins
  • Glucuronides
  • Hydrolyzable Tannins
  • Membrane Transport Modulators
  • urolithin B
  • urolithin C
  • urolithin D
  • 3,8-dihydroxy-6H-dibenzo(b,d)pyran-6-one