Elevated Exogenous Pyruvate Potentiates Mesodermal Differentiation through Metabolic Modulation and AMPK/mTOR Pathway in Human Embryonic Stem Cells

Stem Cell Reports. 2019 Aug 13;13(2):338-351. doi: 10.1016/j.stemcr.2019.06.003. Epub 2019 Jul 25.

Abstract

Pyruvate is a key metabolite in glycolysis and the tricarboxylic acid (TCA) cycle. Exogenous pyruvate modulates metabolism, provides cellular protection, and is essential for the maintenance of human preimplantation embryos and human embryonic stem cells (hESCs). However, little is known about how pyruvate contributes to cell-fate determination during epiblast stage. In this study, we used hESCs as a model to demonstrate that elevated exogenous pyruvate shifts metabolic balance toward oxidative phosphorylation in both maintenance and differentiation conditions. During differentiation, pyruvate potentiates mesoderm and endoderm lineage specification. Pyruvate production and its mitochondrial metabolism are required in BMP4-induced mesoderm differentiation. However, the TCA-cycle metabolites do not have the same effect as pyruvate on differentiation. Further study shows that pyruvate increases AMP/ATP ratio, activates AMPK, and modulates the mTOR pathway to enhance mesoderm differentiation. This study reveals that exogenous pyruvate not only controls metabolism but also modulates signaling pathways in hESC differentiation.

Keywords: AMPK; BMP4; TCA cycle; WNT; differentiation; glycolysis; hESCs; mesoderm; metabolism; pyruvate.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases / metabolism
  • Bone Morphogenetic Protein 4 / pharmacology
  • Cell Differentiation / drug effects*
  • Cell Lineage
  • Citric Acid Cycle / drug effects
  • Endoderm / cytology
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Human Embryonic Stem Cells / cytology
  • Human Embryonic Stem Cells / metabolism
  • Humans
  • Mesoderm / cytology*
  • Mesoderm / metabolism
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Oxidative Phosphorylation / drug effects
  • Pyruvic Acid / pharmacology*
  • Signal Transduction / drug effects*
  • T-Box Domain Proteins / genetics
  • T-Box Domain Proteins / metabolism
  • TOR Serine-Threonine Kinases / metabolism
  • Up-Regulation / drug effects

Substances

  • Bone Morphogenetic Protein 4
  • Homeodomain Proteins
  • MIXL1 protein, human
  • T-Box Domain Proteins
  • Pyruvic Acid
  • MTOR protein, human
  • TOR Serine-Threonine Kinases
  • AMP-Activated Protein Kinases