An iPSC model of hereditary sensory neuropathy-1 reveals L-serine-responsive deficits in neuronal ganglioside composition and axoglial interactions

Cell Rep Med. 2021 Jul 21;2(7):100345. doi: 10.1016/j.xcrm.2021.100345. eCollection 2021 Jul 20.

Abstract

Hereditary sensory neuropathy type 1 (HSN1) is caused by mutations in the SPTLC1 or SPTLC2 sub-units of the enzyme serine palmitoyltransferase, resulting in the production of toxic 1-deoxysphingolipid bases (DSBs). We used induced pluripotent stem cells (iPSCs) from patients with HSN1 to determine whether endogenous DSBs are neurotoxic, patho-mechanisms of toxicity and response to therapy. HSN1 iPSC-derived sensory neurons (iPSCdSNs) endogenously produce neurotoxic DSBs. Complex gangliosides, which are essential for membrane micro-domains and signaling, are reduced, and neurotrophin signaling is impaired, resulting in reduced neurite outgrowth. In HSN1 myelinating cocultures, we find a major disruption of nodal complex proteins after 8 weeks, which leads to complete myelin breakdown after 6 months. HSN1 iPSC models have, therefore, revealed that SPTLC1 mutation alters lipid metabolism, impairs the formation of complex gangliosides, and reduces axon and myelin stability. Many of these changes are prevented by l-serine supplementation, supporting its use as a rational therapy.

Keywords: 1-deoxySLBs; DSBs; HSN1; SPT; SPTLC1; axon; ganglioside; hereditary sensory neuropathy type 1; l-serine; myelin; sensory neuron; serine palmitoyltransferase; serine palmitoyltransferase long-chain base subunit 1; sphingolipid.

Publication types

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

MeSH terms

  • Aging / pathology
  • Axons / drug effects
  • Axons / metabolism*
  • Axons / ultrastructure
  • Base Sequence
  • Caspase 3 / metabolism
  • Cell Line
  • Gangliosides / metabolism*
  • Gene Expression Regulation / drug effects
  • Hereditary Sensory and Autonomic Neuropathies / genetics
  • Hereditary Sensory and Autonomic Neuropathies / pathology*
  • Humans
  • Induced Pluripotent Stem Cells / pathology*
  • Induced Pluripotent Stem Cells / ultrastructure
  • Membrane Microdomains / drug effects
  • Membrane Microdomains / metabolism
  • Membrane Microdomains / ultrastructure
  • Models, Biological*
  • Myelin Sheath / metabolism
  • Nerve Growth Factors / metabolism
  • Neuroglia / drug effects
  • Neuroglia / metabolism*
  • Neuronal Outgrowth / drug effects
  • Nodal Protein / metabolism
  • Sensory Receptor Cells / drug effects
  • Sensory Receptor Cells / metabolism
  • Sensory Receptor Cells / pathology
  • Sensory Receptor Cells / ultrastructure
  • Serine / pharmacology*
  • Signal Transduction / drug effects
  • Sphingolipids / metabolism
  • Transcriptome / genetics

Substances

  • Gangliosides
  • Nerve Growth Factors
  • Nodal Protein
  • Sphingolipids
  • Serine
  • Caspase 3