A novel PMCA3 mutation in an ataxic patient with hypomorphic phosphomannomutase 2 (PMM2) heterozygote mutations: Biochemical characterization of the pump defect

Biochim Biophys Acta Mol Basis Dis. 2017 Dec;1863(12):3303-3312. doi: 10.1016/j.bbadis.2017.08.006. Epub 2017 Aug 12.

Abstract

The neuron-restricted isoform 3 of the plasma membrane Ca2+ ATPase plays a major role in the regulation of Ca2+ homeostasis in the brain, where the precise control of Ca2+ signaling is a necessity. Several function-affecting genetic mutations in the PMCA3 pump associated to X-linked congenital cerebellar ataxias have indeed been described. Interestingly, the presence of co-occurring mutations in additional genes suggest their synergistic action in generating the neurological phenotype as digenic modulators of the role of PMCA3 in the pathologies. Here we report a novel PMCA3 mutation (G733R substitution) in the catalytic P-domain of the pump in a patient affected by non-progressive ataxia, muscular hypotonia, dysmetria and nystagmus. Biochemical studies of the pump have revealed impaired ability to control cellular Ca2+ handling both under basal and under stimulated conditions. A combined analysis by homology modeling and molecular dynamics have revealed a role for the mutated residue in maintaining the correct 3D configuration of the local structure of the pump. Mutation analysis in the patient has revealed two additional function-impairing compound heterozygous missense mutations (R123Q and G214S substitution) in phosphomannomutase 2 (PMM2), a protein that catalyzes the isomerization of mannose 6-phosphate to mannose 1-phosphate. These mutations are known to be associated with Type Ia congenital disorder of glycosylation (PMM2-CDG), the most common group of disorders of N-glycosylation. The findings highlight the association of PMCA3 mutations to cerebellar ataxia and strengthen the possibility that PMCAs act as digenic modulators in Ca2+-linked pathologies.

Keywords: Calcium signaling; Phosphomannomutase 2 mutation; Plasma membrane calcium ATPases; Pump mutation; X-linked cerebellar ataxia.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Ataxia / genetics*
  • Ataxia / metabolism*
  • Brain / diagnostic imaging
  • Brain / pathology
  • Calcium / metabolism
  • Child, Preschool
  • Congenital Disorders of Glycosylation / diagnostic imaging
  • Congenital Disorders of Glycosylation / genetics
  • Congenital Disorders of Glycosylation / metabolism*
  • Congenital Disorders of Glycosylation / pathology
  • Glycosylation
  • HeLa Cells
  • Humans
  • Male
  • Mutation, Missense*
  • Phosphotransferases (Phosphomutases) / deficiency*
  • Phosphotransferases (Phosphomutases) / genetics
  • Phosphotransferases (Phosphomutases) / metabolism
  • Plasma Membrane Calcium-Transporting ATPases / genetics*
  • Plasma Membrane Calcium-Transporting ATPases / metabolism

Substances

  • Plasma Membrane Calcium-Transporting ATPases
  • Phosphotransferases (Phosphomutases)
  • phosphomannomutase 2, human
  • ATP2B3 protein, human
  • Calcium

Supplementary concepts

  • Congenital disorder of glycosylation type 1A