Macrophage depletion blocks congenital SARM1-dependent neuropathy

J Clin Invest. 2022 Dec 1;132(23):e159800. doi: 10.1172/JCI159800.

Abstract

Axon loss contributes to many common neurodegenerative disorders. In healthy axons, the axon survival factor NMNAT2 inhibits SARM1, the central executioner of programmed axon degeneration. We identified 2 rare NMNAT2 missense variants in 2 brothers afflicted with a progressive neuropathy syndrome. The polymorphisms resulted in amino acid substitutions V98M and R232Q, which reduced NMNAT2 NAD+-synthetase activity. We generated a mouse model to mirror the human syndrome and found that Nmnat2V98M/R232Q compound-heterozygous CRISPR mice survived to adulthood but developed progressive motor dysfunction, peripheral axon loss, and macrophage infiltration. These disease phenotypes were all SARM1-dependent. Remarkably, macrophage depletion therapy blocked and reversed neuropathic phenotypes in Nmnat2V98M/R232Q mice, identifying a SARM1-dependent neuroimmune mechanism as a key driver of disease pathogenesis. These findings demonstrate that SARM1 induced inflammatory neuropathy and highlight the potential of immune therapy as a treatment for this rare syndrome and other neurodegenerative conditions associated with NMNAT2 loss and SARM1 activation.

Keywords: Macrophages; Mouse models; Neurodegeneration; Neuroscience.

Publication types

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

MeSH terms

  • Adult
  • Animals
  • Armadillo Domain Proteins / genetics
  • Armadillo Domain Proteins / metabolism
  • Axons / metabolism
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / metabolism
  • Humans
  • Macrophages / metabolism
  • Male
  • Mice
  • Nerve Degeneration / genetics
  • Nicotinamide-Nucleotide Adenylyltransferase* / metabolism
  • Peripheral Nervous System Diseases* / metabolism

Substances

  • Armadillo Domain Proteins
  • Nicotinamide-Nucleotide Adenylyltransferase
  • Cytoskeletal Proteins
  • SARM1 protein, human
  • SARM1 protein, mouse
  • Nmnat2 protein, mouse