Serine and Lipid Metabolism in Macular Disease and Peripheral Neuropathy

N Engl J Med. 2019 Oct 10;381(15):1422-1433. doi: 10.1056/NEJMoa1815111. Epub 2019 Sep 11.

Abstract

Background: Identifying mechanisms of diseases with complex inheritance patterns, such as macular telangiectasia type 2, is challenging. A link between macular telangiectasia type 2 and altered serine metabolism has been established previously.

Methods: Through exome sequence analysis of a patient with macular telangiectasia type 2 and his family members, we identified a variant in SPTLC1 encoding a subunit of serine palmitoyltransferase (SPT). Because mutations affecting SPT are known to cause hereditary sensory and autonomic neuropathy type 1 (HSAN1), we examined 10 additional persons with HSAN1 for ophthalmologic disease. We assayed serum amino acid and sphingoid base levels, including levels of deoxysphingolipids, in patients who had macular telangiectasia type 2 but did not have HSAN1 or pathogenic variants affecting SPT. We characterized mice with low serine levels and tested the effects of deoxysphingolipids on human retinal organoids.

Results: Two variants known to cause HSAN1 were identified as causal for macular telangiectasia type 2: of 11 patients with HSAN1, 9 also had macular telangiectasia type 2. Circulating deoxysphingolipid levels were 84.2% higher among 125 patients with macular telangiectasia type 2 who did not have pathogenic variants affecting SPT than among 94 unaffected controls. Deoxysphingolipid levels were negatively correlated with serine levels, which were 20.6% lower than among controls. Reduction of serine levels in mice led to increases in levels of retinal deoxysphingolipids and compromised visual function. Deoxysphingolipids caused photoreceptor-cell death in retinal organoids, but not in the presence of regulators of lipid metabolism.

Conclusions: Elevated levels of atypical deoxysphingolipids, caused by variant SPTLC1 or SPTLC2 or by low serine levels, were risk factors for macular telangiectasia type 2, as well as for peripheral neuropathy. (Funded by the Lowy Medical Research Institute and others.).

Publication types

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

MeSH terms

  • Adult
  • Aged
  • Animals
  • DNA Mutational Analysis
  • Disease Models, Animal
  • Exome / genetics
  • Female
  • Hereditary Sensory and Autonomic Neuropathies / complications
  • Hereditary Sensory and Autonomic Neuropathies / genetics*
  • Hereditary Sensory and Autonomic Neuropathies / metabolism
  • Humans
  • Lipid Metabolism
  • Macula Lutea / pathology
  • Male
  • Mice
  • Middle Aged
  • Mutation*
  • Pedigree
  • Retinal Telangiectasis / complications
  • Retinal Telangiectasis / genetics*
  • Retinal Telangiectasis / metabolism
  • Risk Factors
  • Serine / blood
  • Serine / metabolism*
  • Serine C-Palmitoyltransferase / genetics*
  • Sphingolipids / metabolism*
  • Sphingosine / analogs & derivatives
  • Sphingosine / analysis
  • Young Adult

Substances

  • Sphingolipids
  • Serine
  • SPTLC1 protein, human
  • SPTLC2 protein, human
  • Serine C-Palmitoyltransferase
  • Sphingosine
  • safingol