Acid Ceramidase Deficiency in Mice Leads to Severe Ocular Pathology and Visual Impairment

Am J Pathol. 2019 Feb;189(2):320-338. doi: 10.1016/j.ajpath.2018.10.018. Epub 2018 Nov 23.

Abstract

Farber disease (FD) is a debilitating lysosomal storage disorder characterized by severe inflammation and neurodegeneration. FD is caused by mutations in the ASAH1 gene, resulting in deficient acid ceramidase (ACDase) activity. Patients with ACDase deficiency exhibit a broad clinical spectrum. In classic cases, patients develop hepatosplenomegaly, nervous system involvement, and childhood mortality. Ocular manifestations include decreased vision, a grayish appearance to the retina with a cherry red spot, and nystagmus. That said, the full effect of ACDase deficiency on the visual system has not been studied in detail. We previously developed a mouse model that is orthologous for a known patient mutation in Asah1 that recapitulates human FD. Herein, we report evidence of a severe ocular pathology in Asah1P361R/P361R mice. Asah1P361R/P361R mice exhibit progressive retinal and optic nerve pathology. Through noninvasive ocular imaging and histopathological analyses of these Asah1P361R/P361R animals, we revealed progressive inflammation, the presence of retinal dysplasia, and significant storage pathology in various cell types in both the retina and optic nerves. Lipidomic analyses of retinal tissues revealed an abnormal accumulation of ceramides and other sphingolipids. Electroretinograms and behavioral tests showed decreased retinal and visual responses. Taken together, these data suggest that ACDase deficiency leads to sphingolipid imbalance, inflammation, dysmorphic retinal and optic nerve pathology, and severe visual impairment.

Publication types

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

MeSH terms

  • Acid Ceramidase / genetics*
  • Acid Ceramidase / metabolism
  • Amino Acid Substitution
  • Animals
  • Ceramides / genetics
  • Ceramides / metabolism
  • Disease Models, Animal
  • Farber Lipogranulomatosis* / enzymology
  • Farber Lipogranulomatosis* / genetics
  • Farber Lipogranulomatosis* / pathology
  • Inflammation / enzymology
  • Inflammation / genetics
  • Inflammation / pathology
  • Mice
  • Mice, Mutant Strains
  • Mutation, Missense*
  • Optic Nerve* / enzymology
  • Optic Nerve* / pathology
  • Retina* / enzymology
  • Retina* / pathology
  • Sphingolipids / genetics
  • Sphingolipids / metabolism
  • Vision Disorders* / enzymology
  • Vision Disorders* / genetics
  • Vision Disorders* / pathology

Substances

  • Ceramides
  • Sphingolipids
  • Acid Ceramidase
  • Asah1 protein, mouse