TY - JOUR
AU - Woeste, Marina A
AU - Stern, Sina
AU - Raju, Diana N
AU - Grahn, Elena
AU - Dittmann, Dominik
AU - Gutbrod, Katharina
AU - Dörmann, Peter
AU - Hansen, Jan N
AU - Schonauer, Sophie
AU - Marx, Carina E
AU - Hamzeh, Hussein
AU - Körschen, Heinz G
AU - Aerts, Johannes M F G
AU - Bönigk, Wolfgang
AU - Endepols, Heike
AU - Sandhoff, Roger
AU - Geyer, Matthias
AU - Berger, Thomas K
AU - Bradke, Frank
AU - Wachten, Dagmar
TI - Species-specific differences in nonlysosomal glucosylceramidase GBA2 function underlie locomotor dysfunction arising from loss-of-function mutations.
JO - The journal of biological chemistry
VL - 294
IS - 11
SN - 0021-9258
CY - Bethesda, Md.
PB - Soc.60645
M1 - DZNE-2020-06906
SP - 3853-3871
PY - 2019
AB - The nonlysosomal glucosylceramidase β2 (GBA2) catalyzes the hydrolysis of glucosylceramide to glucose and ceramide. Mutations in the human GBA2 gene have been associated with hereditary spastic paraplegia (HSP), autosomal-recessive cerebellar ataxia (ARCA), and the Marinesco-Sjögren-like syndrome. However, the underlying molecular mechanisms are ill-defined. Here, using biochemistry, immunohistochemistry, structural modeling, and mouse genetics, we demonstrate that all but one of the spastic gait locus #46 (SPG46)-connected mutations cause a loss of GBA2 activity. We demonstrate that GBA2 proteins form oligomeric complexes and that protein-protein interactions are perturbed by some of these mutations. To study the pathogenesis of GBA2-related HSP and ARCA in vivo, we investigated GBA2-KO mice as a mammalian model system. However, these mice exhibited a high phenotypic variance and did not fully resemble the human phenotype, suggesting that mouse and human GBA2 differ in function. Whereas some GBA2-KO mice displayed a strong locomotor defect, others displayed only mild alterations of the gait pattern and no signs of cerebellar defects. On a cellular level, inhibition of GBA2 activity in isolated cerebellar neurons dramatically affected F-actin dynamics and reduced neurite outgrowth, which has been associated with the development of neurological disorders. Our results shed light on the molecular mechanism underlying the pathogenesis of GBA2-related HSP and ARCA and reveal species-specific differences in GBA2 function in vivo.
KW - Glucosylceramidase
KW - Animals
KW - Biocatalysis
KW - Cerebellar Ataxia: genetics
KW - Cerebellar Ataxia: metabolism
KW - Humans
KW - Locomotion: genetics
KW - Loss of Function Mutation
KW - Mice
KW - Mice, Knockout
KW - Spastic Paraplegia, Hereditary: genetics
KW - Spastic Paraplegia, Hereditary: metabolism
KW - Species Specificity
KW - beta-Glucosidase: antagonists & inhibitors
KW - beta-Glucosidase: deficiency
KW - beta-Glucosidase: genetics
KW - beta-Glucosidase: metabolism
KW - beta-Glucosidase (NLM Chemicals)
KW - beta-glucosidase 2, mouse (NLM Chemicals)
KW - GBA2 protein, human (NLM Chemicals)
LB - PUB:(DE-HGF)16
C6 - pmid:30662006
C2 - pmc:PMC6422076
DO - DOI:10.1074/jbc.RA118.006311
UR - https://pub.dzne.de/record/140584
ER -