Rescue of neurodegeneration in the Fig4 null mouse by a catalytically inactive FIG4 transgene

Hum Mol Genet. 2016 Jan 15;25(2):340-7. doi: 10.1093/hmg/ddv480. Epub 2015 Nov 24.

Abstract

The lipid phosphatase FIG4 is a subunit of the protein complex that regulates biosynthesis of the signaling lipid PI(3,5)P2. Mutations of FIG4 result in juvenile lethality and spongiform neurodegeneration in the mouse, and are responsible for the human disorders Charcot-Marie-Tooth disease, Yunis-Varon syndrome and polymicrogyria with seizures. We previously demonstrated that conditional expression of a wild-type FIG4 transgene in neurons is sufficient to rescue most of the abnormalities of Fig4 null mice, including juvenile lethality and extensive neurodegeneration. To evaluate the contribution of the phosphatase activity to the in vivo function of Fig4, we introduced the mutation p.Cys486Ser into the Sac phosphatase active-site motif CX5RT. Transfection of the Fig4(Cys486Ser) cDNA into cultured Fig4(-/-) fibroblasts was effective in preventing vacuolization. The neuronal expression of an NSE-Fig4(Cys486Ser) transgene in vivo prevented the neonatal neurodegeneration and juvenile lethality seen in Fig4 null mice. These observations demonstrate that the catalytically inactive FIG4 protein provides significant function, possibly by stabilization of the PI(3,5)P2 biosynthetic complex and/or localization of the complex to endolysosomal vesicles. Despite this partial rescue, later in life the NSE-Fig4(Cys486Ser) transgenic mice display significant abnormalities that include hydrocephalus, defective myelination and reduced lifespan. The late onset phenotype of the NSE-Fig4(Cys486Ser) transgenic mice demonstrates that the phosphatase activity of FIG4 has an essential role in vivo.

Publication types

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

MeSH terms

  • Animals
  • Catalytic Domain / genetics
  • Charcot-Marie-Tooth Disease / genetics
  • Charcot-Marie-Tooth Disease / metabolism
  • Cleidocranial Dysplasia / genetics
  • Cleidocranial Dysplasia / metabolism
  • Ectodermal Dysplasia / genetics
  • Ectodermal Dysplasia / metabolism
  • Flavoproteins / genetics*
  • Flavoproteins / metabolism
  • Hydrocephalus / genetics*
  • Hydrocephalus / metabolism
  • Limb Deformities, Congenital / genetics
  • Limb Deformities, Congenital / metabolism
  • Mice
  • Mice, Transgenic
  • Micrognathism / genetics
  • Micrognathism / metabolism
  • Mutation*
  • Neurons / metabolism*
  • Phosphatidylinositol Phosphates / metabolism
  • Phosphoinositide Phosphatases
  • Phosphoric Monoester Hydrolases / genetics
  • Phosphoric Monoester Hydrolases / metabolism
  • Polymicrogyria / genetics
  • Polymicrogyria / metabolism
  • Schwann Cells / metabolism

Substances

  • Flavoproteins
  • Phosphatidylinositol Phosphates
  • phosphatidylinositol 3,5-diphosphate
  • Phosphoric Monoester Hydrolases
  • Fig4 protein, mouse
  • Phosphoinositide Phosphatases

Supplementary concepts

  • Yunis Varon syndrome