Both the folate cycle and betaine-homocysteine methyltransferase contribute methyl groups for DNA methylation in mouse blastocysts

FASEB J. 2015 Mar;29(3):1069-79. doi: 10.1096/fj.14-261131. Epub 2014 Dec 2.

Abstract

The embryonic pattern of global DNA methylation is first established in the inner cell mass (ICM) of the mouse blastocyst. The methyl donor S-adenosylmethionine (SAM) is produced in most cells through the folate cycle, but only a few cell types generate SAM from betaine (N,N,N-trimethylglycine) via betaine-homocysteine methyltransferase (BHMT), which is expressed in the mouse ICM. Here, mean ICM cell numbers decreased from 18-19 in controls to 11-13 when the folate cycle was inhibited by the antifolate methotrexate and to 12-14 when BHMT expression was knocked down by antisense morpholinos. Inhibiting both pathways, however, much more severely affected ICM development (7-8 cells). Total SAM levels in mouse blastocysts decreased significantly only when both pathways were inhibited (from 3.1 to 1.6 pmol/100 blastocysts). DNA methylation, detected as 5-methylcytosine (5-MeC) immunofluorescence in isolated ICMs, was minimally affected by inhibition of either pathway alone but decreased by at least 45-55% when both BHMT and the folate cycle were inhibited simultaneously. Effects on cell numbers and 5-MeC levels in the ICM were completely rescued by methionine (immediate SAM precursor) or SAM. Both the folate cycle and betaine/BHMT appear to contribute to a methyl pool required for normal ICM development and establishing initial embryonic DNA methylation.

Keywords: S-adenosylmethionine; embryo; epigenetics; inner cell mass; methionine.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 5-Methylcytosine / analysis
  • Animals
  • Antimetabolites, Antineoplastic / pharmacology
  • Betaine-Homocysteine S-Methyltransferase / antagonists & inhibitors
  • Betaine-Homocysteine S-Methyltransferase / metabolism*
  • Blastocyst / cytology
  • Blastocyst / drug effects
  • Blastocyst / metabolism*
  • Cell Lineage
  • Cells, Cultured
  • DNA Methylation*
  • Embryo, Mammalian / cytology
  • Embryo, Mammalian / drug effects
  • Embryo, Mammalian / metabolism*
  • Female
  • Fluorescent Antibody Technique
  • Folic Acid / metabolism*
  • Gene Expression Regulation, Enzymologic*
  • Liver / cytology
  • Liver / drug effects
  • Liver / metabolism
  • Methotrexate / pharmacology
  • Mice
  • S-Adenosylmethionine / metabolism*
  • snRNP Core Proteins / metabolism

Substances

  • Antimetabolites, Antineoplastic
  • snRNP Core Proteins
  • 5-Methylcytosine
  • S-Adenosylmethionine
  • Folic Acid
  • Betaine-Homocysteine S-Methyltransferase
  • Methotrexate