Mannose controls mesoderm specification and symmetry breaking in mouse gastruloids

Dev Cell. 2024 Jun 17;59(12):1523-1537.e6. doi: 10.1016/j.devcel.2024.03.031. Epub 2024 Apr 17.

Abstract

Patterning and growth are fundamental features of embryonic development that must be tightly coordinated. To understand how metabolism impacts early mesoderm development, we used mouse embryonic stem-cell-derived gastruloids, that co-expressed glucose transporters with the mesodermal marker T/Bra. We found that the glucose mimic, 2-deoxy-D-glucose (2-DG), blocked T/Bra expression and abolished axial elongation in gastruloids. However, glucose removal did not phenocopy 2-DG treatment despite a decline in glycolytic intermediates. As 2-DG can also act as a competitive inhibitor of mannose in protein glycosylation, we added mannose together with 2-DG and found that it could rescue the mesoderm specification both in vivo and in vitro. We further showed that blocking production and intracellular recycling of mannose abrogated mesoderm specification. Proteomics analysis demonstrated that mannose reversed glycosylation of the Wnt pathway regulator, secreted frizzled receptor Frzb. Our study showed how mannose controls mesoderm specification in mouse gastruloids.

Keywords: FGF; Wnt; gastrulation; gastruloids; glycosylation; metabolomics; self-organisation.

MeSH terms

  • Animals
  • Body Patterning / drug effects
  • Body Patterning / genetics
  • Cell Differentiation / drug effects
  • Deoxyglucose / metabolism
  • Deoxyglucose / pharmacology
  • Frizzled Receptors / genetics
  • Frizzled Receptors / metabolism
  • Gastrula / metabolism
  • Gene Expression Regulation, Developmental / drug effects
  • Glycosylation
  • Mannose* / metabolism
  • Mesoderm* / metabolism
  • Mice
  • Mouse Embryonic Stem Cells / cytology
  • Mouse Embryonic Stem Cells / drug effects
  • Mouse Embryonic Stem Cells / metabolism
  • Wnt Signaling Pathway / drug effects

Substances

  • Mannose
  • Deoxyglucose
  • Frizzled Receptors