Macrophages Expressing GALC Improve Peripheral Krabbe Disease by a Mechanism Independent of Cross-Correction

Neuron. 2020 Jul 8;107(1):65-81.e9. doi: 10.1016/j.neuron.2020.03.031. Epub 2020 May 5.

Abstract

Many therapies for lysosomal storage disorders rely on cross-correction of lysosomal enzymes. In globoid cell leukodystrophy (GLD), mutations in GALC cause psychosine accumulation, inducing demyelination, a neuroinflammatory "globoid" reaction and neurodegeneration. The efficiency of GALC cross-correction in vivo, the role of the GALC substrate galactosylceramide, and the origin of psychosine are poorly understood. Using a novel GLD model, we show that cross-correction does not occur efficiently in vivo and that Galc-deficient Schwann cells autonomously produce psychosine. Furthermore, macrophages require GALC to degrade myelin, as Galc-deficient macrophages are transformed into globoid cells by exposure to galactosylceramide and produce a more severe GLD phenotype. Finally, hematopoietic stem cell transplantation in patients reduces globoid cells in nerves, suggesting that the phagocytic response of healthy macrophages, rather than cross-correction, contributes to the therapeutic effect. Thus, GLD may be caused by at least two mechanisms: psychosine-induced demyelination and secondary neuroinflammation from galactosylceramide storage in macrophages.

Keywords: GALC; Krabbe disease; Schwann cell; cross-correction; demyelination; galactosylceramide; globoid cell leukodystrophy; hematopoietic stem cell therapy; lysosomal storage disorder; lysosomes; macrophage; psychosine.

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

  • Animals
  • Demyelinating Diseases / enzymology
  • Demyelinating Diseases / pathology
  • Galactosylceramidase / metabolism*
  • Hematopoietic Stem Cell Transplantation
  • Humans
  • Leukodystrophy, Globoid Cell / enzymology*
  • Leukodystrophy, Globoid Cell / pathology
  • Leukodystrophy, Globoid Cell / therapy
  • Macrophages / enzymology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nerve Degeneration / enzymology
  • Nerve Degeneration / pathology
  • Schwann Cells / enzymology*

Substances

  • Galactosylceramidase