Erik Nutma

188 Chapter 8 Leukodystrophies Leukodystrophies have recently been classified based on the pathological changes and mechanisms driving disease and its progression101. Until recently, only a few leukodystrophies had been discovered based on gene mutations affecting microglia development/behaviour, also known as microgliopathies. Adult-onset leukoencephalopathy with axonal spheroids and pigmented glia (ALSP), previously known as hereditary diffuse leukoencephalopathy with spheroids (HDLS) or pigmentary orthochromatic leukodystrophy (POLD)102, is a leukoencephalopathy caused by heterozygous mutations in the colony stimulating factor-1 receptor gene (CSF1R). CSF1R is a cell-surface receptor regulating survival, proliferation, and differentiation of macrophages, including microglia. ALSP presents with progressively altered microglia morphology and reduced microglia density, particularly in the white matter103. In ALSP, microglial expression of CD68, CD163 and CD204 was found to precede loss of axons and axonal swelling103 suggesting that microglia undergo changes in immune sensing and initiate phagocytosis. Experimental models lacking expression of, or inhibiting the function of CSF1R, have revealed its importance in maintaining microglia numbers3,104-106. Additionally, while microglia were seen to retain their specific microglial signature in zebrafish with csf1r mutations106, this was not found in humans, where microglia in the white matter lose their homeostatic signature and expression of IBA-1 and P2RY12107. Furthermore, Kempthorne et al showed that, in humans, white matter closer to the cortex was less affected than the deep white matter, indicating regional differences in response to microglial changes . Additionally, white matter in the frontal lobe was found to be more affected than white matter elsewhere in the brain in ALSP, and is associated with increased expression of 75 genes including APOE, CCL4, JUN, and HEXB107. Reduced microglia numbers were also found in brain tissue with no apparent myelin damage, suggesting changes in microglia function could also underpin white matter degeneration, leading to regional heterogeneity in white matter vulnerability. Another microgliopathy is Nasu-Hakola disease (NHD)108-111, also known as polycystic lipomembraneous osteodysplasia with sclerosing leukoencephalopathy (PLOSL). NHD is an autosomal recessive disorder caused by genetic mutations in either TREM2 or TYROBP (DAP12) resulting in loss of function112. TREM2 and TYROBP encode for different subunits of the same receptor-signalling complex113 involved in regulating microglial activity in immune processes114. While NHD shows widespread activation of microglia due to lack of TREM2 signalling115, damage to the white matter is most prominent in the frontotemporal lobe and basal ganglia, while subcortical arcuate fibres are more preserved115,116. This suggests that regional heterogeneity in the brain influences microglial function, resulting in differences in white matter damage. Clinical and pathological presentation of the disease might also be dependent on the type and severity of the mutation. Overall, these findings demonstrate that mutations in microglia-associated genes result in aberrant function and myelin damage, underlining the importance of microglial homeostasis for normal CNS function. Another likely microgliopathy is pseudo-TORCH syndrome, which develops due to genetic loss-of-function mutations in USP18117-119, which dampens microglial activation in the context of upregulation of type I interferon genes. USP18 is highly enriched in white matter microglia and in pseudo-TORCH syndrome associated with microgliosis and calcifications in the white matter118,120. How or why USP18 expression is differentially regulated in white and grey matter is unknown, further investigation may reveal regional heterogeneity in microglial function.

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