Peripheral nervous system plasmalogens regulate Schwann cell differentiation and myelination

J Clin Invest. 2014 Jun;124(6):2560-70. doi: 10.1172/JCI72063. Epub 2014 Apr 24.

Abstract

Rhizomelic chondrodysplasia punctata (RCDP) is a developmental disorder characterized by hypotonia, cataracts, abnormal ossification, impaired motor development, and intellectual disability. The underlying etiology of RCDP is a deficiency in the biosynthesis of ether phospholipids, of which plasmalogens are the most abundant form in nervous tissue and myelin; however, the role of plasmalogens in the peripheral nervous system is poorly defined. Here, we used mouse models of RCDP and analyzed the consequence of plasmalogen deficiency in peripheral nerves. We determined that plasmalogens are crucial for Schwann cell development and differentiation and that plasmalogen defects impaired radial sorting, myelination, and myelin structure. Plasmalogen insufficiency resulted in defective protein kinase B (AKT) phosphorylation and subsequent signaling, causing overt activation of glycogen synthase kinase 3β (GSK3β) in nerves of mutant mice. Treatment with GSK3β inhibitors, lithium, or 4-benzyl-2-methyl-1,2,4-thiadiazolidine-3,5-dione (TDZD-8) restored Schwann cell defects, effectively bypassing plasmalogen deficiency. Our results demonstrate the requirement of plasmalogens for the correct and timely differentiation of Schwann cells and for the process of myelination. In addition, these studies identify a mechanism by which the lack of a membrane phospholipid causes neuropathology, implicating plasmalogens as regulators of membrane and cell signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Differentiation / physiology
  • Chondrodysplasia Punctata, Rhizomelic / etiology
  • Chondrodysplasia Punctata, Rhizomelic / pathology
  • Chondrodysplasia Punctata, Rhizomelic / physiopathology
  • Female
  • Glycogen Synthase Kinase 3 / antagonists & inhibitors
  • Glycogen Synthase Kinase 3 / metabolism
  • Glycogen Synthase Kinase 3 beta
  • Humans
  • Male
  • Mice
  • Mice, Knockout
  • Mice, Neurologic Mutants
  • Models, Neurological
  • Myelin Basic Protein / metabolism
  • Myelin Sheath / physiology
  • Nerve Regeneration
  • Peripheral Nervous System / cytology*
  • Peripheral Nervous System / physiology*
  • Peroxisomal Targeting Signal 2 Receptor
  • Plasmalogens / physiology*
  • Proto-Oncogene Proteins c-akt / metabolism
  • Receptors, Cytoplasmic and Nuclear / deficiency
  • Receptors, Cytoplasmic and Nuclear / genetics
  • Schwann Cells / cytology*
  • Schwann Cells / physiology*
  • Signal Transduction

Substances

  • Myelin Basic Protein
  • Peroxisomal Targeting Signal 2 Receptor
  • Plasmalogens
  • Receptors, Cytoplasmic and Nuclear
  • GSK3B protein, human
  • Glycogen Synthase Kinase 3 beta
  • Gsk3b protein, mouse
  • Proto-Oncogene Proteins c-akt
  • Glycogen Synthase Kinase 3

Supplementary concepts

  • Rhizomelic chondrodysplasia punctata, type 2