PUBLICATION

Homozygous Mutations in CSF1R Cause a Pediatric-Onset Leukoencephalopathy and Can Result in Congenital Absence of Microglia

Authors
Oosterhof, N., Chang, I.J., Karimiani, E.G., Kuil, L.E., Jensen, D.M., Daza, R., Young, E., Astle, L., van der Linde, H.C., Shivaram, G.M., Demmers, J., Latimer, C.S., Keene, C.D., Loter, E., Maroofian, R., van Ham, T.J., Hevner, R.F., Bennett, J.T.
ID
ZDB-PUB-190416-8
Date
2019
Source
American journal of human genetics   104(5): 936-947 (Journal)
Registered Authors
Kuil, Laura, van der Linde, Herma, van Ham, Tjakko
Keywords
CSF1R, CUX1, agenesis corpus callosum, axonal spheroids, leukoencephalopathy, microglia, neuropathology, osteopetrosis, recessive, zebrafish
MeSH Terms
  • Adult
  • Animals
  • Child
  • Congenital Abnormalities/etiology*
  • Congenital Abnormalities/pathology
  • Homeodomain Proteins/genetics
  • Homeodomain Proteins/metabolism
  • Homozygote
  • Humans
  • Infant
  • Infant, Newborn
  • Leukoencephalopathies/genetics*
  • Leukoencephalopathies/pathology*
  • Microglia/metabolism
  • Microglia/pathology*
  • Mutation*
  • Pedigree
  • Phenotype
  • Protein-Tyrosine Kinases/genetics
  • Protein-Tyrosine Kinases/metabolism
  • Receptors, Granulocyte-Macrophage Colony-Stimulating Factor/genetics*
  • Repressor Proteins/genetics
  • Repressor Proteins/metabolism
  • Transcription Factors/genetics
  • Transcription Factors/metabolism
  • Young Adult
  • Zebrafish
  • Zebrafish Proteins/genetics
  • Zebrafish Proteins/metabolism
PubMed
30982608 Full text @ Am. J. Hum. Genet.
Abstract
Microglia are CNS-resident macrophages that scavenge debris and regulate immune responses. Proliferation and development of macrophages, including microglia, requires Colony Stimulating Factor 1 Receptor (CSF1R), a gene previously associated with a dominant adult-onset neurological condition (adult-onset leukoencephalopathy with axonal spheroids and pigmented glia). Here, we report two unrelated individuals with homozygous CSF1R mutations whose presentation was distinct from ALSP. Post-mortem examination of an individual with a homozygous splice mutation (c.1754-1G>C) demonstrated several structural brain anomalies, including agenesis of corpus callosum. Immunostaining demonstrated almost complete absence of microglia within this brain, suggesting that it developed in the absence of microglia. The second individual had a homozygous missense mutation (c.1929C>A [p.His643Gln]) and presented with developmental delay and epilepsy in childhood. We analyzed a zebrafish model (csf1rDM) lacking Csf1r function and found that their brains also lacked microglia and had reduced levels of CUX1, a neuronal transcription factor. CUX1+ neurons were also reduced in sections of homozygous CSF1R mutant human brain, identifying an evolutionarily conserved role for CSF1R signaling in production or maintenance of CUX1+ neurons. Since a large fraction of CUX1+ neurons project callosal axons, we speculate that microglia deficiency may contribute to agenesis of the corpus callosum via reduction in CUX1+ neurons. Our results suggest that CSF1R is required for human brain development and establish the csf1rDM fish as a model for microgliopathies. In addition, our results exemplify an under-recognized form of phenotypic expansion, in which genes associated with well-recognized, dominant conditions produce different phenotypes when biallelically mutated.
Genes / Markers
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Expression
Phenotype
Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Fish
Antibodies
Orthology
Engineered Foreign Genes
Mapping