Interactive effects of fatty acid and butyrate-induced mitochondrial Ca²⁺ loading and apoptosis in colonocytes

Cancer. 2011 Dec 1;117(23):5294-303. doi: 10.1002/cncr.26205. Epub 2011 May 11.

Abstract

Background: The combination of fish oil-derived docosahexaenoic acid (DHA) (22:6; omega 3 [n-3]) and butyrate (4:0), a fiber fermentation product, synergized to enhance colonocyte apoptosis by inducing a p53-independent, oxidation sensitive, mitochondrial Ca(2+) -dependent (intrinsic) pathway.

Methods: In this study, the authors probed the specificity of n-6 and n-3 polyunsaturated fatty acid induction of Ca(2+) -dependent proapoptotic events in immortalized young adult mouse colonocytes and determined whether combinations of polyunsaturated fatty acid and butyrate could trigger endoplasmic reticulum (ER) stress conditions, thereby promoting mitochondrial Ca(2+) overload. Cultures were treated with 0 μM to 50 μM of DHA (22:6; n-3), EPA (20:5; n-3), arachidoinic acid (AA) (20:4; n-6), linoleic acid (18:2; n-6), or oleic acid (OA) (18:1; n-9) for a total of 72 hours with or without RU-360 (to inhibit the mitochondrial Ca(2+) uniporter) for 30 minutes before cotreatment with butyrate (0 mM or 5 mM).

Results: Combined DHA and butyrate maximally induced apoptosis and mitochondrial-to-cytosolic Ca(2+) levels. By comparison, EPA, a precursor to DHA, was minimally effective. Similarly, AA and OA in combination with butyrate had no effect on mitochondrial Ca(2+) or apoptosis compared with butyrate alone. DHA with or without butyrate cotreatment minimally altered the ER stress-regulated genes DNA damage-inducible transcript 3, the CCAAT enhancer binding protein (C/EBP) homologous protein (CHOP), and eukaryotic initiation factor 2α.

Conclusions: The current data indicated that butyrate and DHA, but not EPA, worked in a coordinated fashion to trigger an ER-independent, Ca(2+) -dependent, intrinsic mitochondrial-mediated apoptotic pathway in colonocytes.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Apoptosis / drug effects*
  • Butyrates / pharmacology*
  • Calcium / metabolism*
  • Cells, Cultured
  • Colon / cytology
  • Colon / drug effects*
  • Endoplasmic Reticulum Stress / drug effects
  • Fatty Acids, Omega-3 / pharmacology*
  • Fatty Acids, Unsaturated / pharmacology*
  • Mice
  • Mitochondria / metabolism*
  • Ruthenium Compounds / pharmacology

Substances

  • Butyrates
  • Fatty Acids, Omega-3
  • Fatty Acids, Unsaturated
  • Ru 360
  • Ruthenium Compounds
  • Calcium