Neuroprotection and lifespan extension in Ppt1(-/-) mice by NtBuHA: therapeutic implications for INCL

Nat Neurosci. 2013 Nov;16(11):1608-17. doi: 10.1038/nn.3526. Epub 2013 Sep 22.

Abstract

Infantile neuronal ceroid lipofuscinosis (INCL) is a devastating childhood neurodegenerative lysosomal storage disease (LSD) that has no effective treatment. It is caused by inactivating mutations in the palmitoyl-protein thioesterase-1 (PPT1) gene. PPT1 deficiency impairs the cleavage of thioester linkage in palmitoylated proteins (constituents of ceroid), preventing degradation by lysosomal hydrolases. Consequently, accumulation of lysosomal ceroid leads to INCL. Thioester linkage is cleaved by nucleophilic attack. Hydroxylamine, a potent nucleophilic cellular metabolite, may have therapeutic potential for INCL, but its toxicity precludes clinical application. We found that a hydroxylamine derivative, N-(tert-Butyl) hydroxylamine (NtBuHA), was non-toxic, cleaved thioester linkage in palmitoylated proteins and mediated lysosomal ceroid depletion in cultured cells from INCL patients. In Ppt1(-/-) mice, which mimic INCL, NtBuHA crossed the blood-brain barrier, depleted lysosomal ceroid, suppressed neuronal apoptosis, slowed neurological deterioration and extended lifespan. Our findings provide a proof of concept that thioesterase-mimetic and antioxidant small molecules such as NtBuHA are potential drug targets for thioesterase deficiency diseases such as INCL.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Apoptosis / genetics
  • Carbon Isotopes / metabolism
  • Cells, Cultured
  • Cerebral Cortex / pathology
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / genetics
  • Hydroxylamines / metabolism
  • Hydroxylamines / pharmacology
  • Hydroxylamines / therapeutic use*
  • Longevity / drug effects
  • Longevity / genetics
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neuronal Ceroid-Lipofuscinoses / drug therapy*
  • Neuronal Ceroid-Lipofuscinoses / genetics*
  • Neuronal Ceroid-Lipofuscinoses / pathology
  • Neurons / drug effects
  • Neurons / metabolism
  • Neurons / ultrastructure
  • Neuroprotective Agents / metabolism
  • Neuroprotective Agents / therapeutic use*
  • Palmitoyl Coenzyme A / drug effects
  • Palmitoyl Coenzyme A / metabolism
  • Thiolester Hydrolases / deficiency*
  • Time Factors

Substances

  • Carbon Isotopes
  • Hydroxylamines
  • N-(tert-butyl)hydroxylamine
  • Neuroprotective Agents
  • Palmitoyl Coenzyme A
  • Thiolester Hydrolases
  • palmitoyl-protein thioesterase

Supplementary concepts

  • Ceroid lipofuscinosis, neuronal 1, infantile