Lysosomal degradation of GMPPB is associated with limb-girdle muscular dystrophy type 2T

Ann Clin Transl Neurol. 2019 May 8;6(6):1062-1071. doi: 10.1002/acn3.787. eCollection 2019 Jun.

Abstract

Objective: GDP-mannose pyrophosphorylase B (GMPPB) related phenotype spectrum ranges widely from congenital myasthenic syndrome (CMS), limb-girdle muscular dystrophy type 2T (LGMD 2T) to severe congenital muscle-eye-brain syndrome. Our study investigates the clinicopathologic features of a patient with novel GMPPB mutations and explores the pathogenetic mechanism.

Methods: The patient was a 22-year-old woman with chronic proximal limb weakness for 9 years without cognitive deterioration. Weakness became worse after fatigue. Elevated serum creatine kinase and decrements on repetitive nerve stimulation test were recorded. MRI showed fatty infiltration in muscles of lower limbs and shoulder girdle on T1 sequence. Open muscle biopsy and genetic analysis were performed.

Results: Muscle biopsy showed myogenic changes. Two missense mutations in GMPPB gene (c.803T>C and c.1060G>A) were identified in the patient. Western blotting and immunostaining showed GMPPB and α-dystroglycan deficiency in the patient's muscle. In vitro, mutant GMPPB forming cytoplasmic aggregates completely colocalized with microtubule-associated protein 1 light chain 3-II (LC3-II), a classical marker of autophagosome. Degradation of GMPPB was accompanied by an upregulation of LC3-II, which could be restored by lysosomal inhibitor leupeptin.

Interpretation: We identified two novel GMPPB mutations causing overlap phenotype between LGMD 2T and CMS. We provided the initial evidence that mutant GMPPB colocalizes with autophagosome at subcellular level. GMPPB mutants degraded by autophagy-lysosome pathway is associated with LGMD 2T. This study shed the light into the enzyme replacement which could become one of the therapeutic targets in the future study.

Publication types

  • Case Reports

MeSH terms

  • Autophagy
  • Dystroglycans / deficiency
  • Dystroglycans / metabolism
  • Extremities
  • Female
  • HEK293 Cells
  • Humans
  • Lysosomes / metabolism
  • Magnetic Resonance Imaging
  • Microtubule-Associated Proteins / metabolism
  • Muscles / pathology
  • Muscular Dystrophies, Limb-Girdle / genetics*
  • Muscular Dystrophies, Limb-Girdle / pathology*
  • Mutation, Missense
  • Myasthenic Syndromes, Congenital / genetics
  • Nucleotidyltransferases / genetics*
  • Pyridostigmine Bromide / therapeutic use
  • Young Adult

Substances

  • MAP1LC3A protein, human
  • Microtubule-Associated Proteins
  • Dystroglycans
  • Nucleotidyltransferases
  • mannose 1-phosphate guanylyltransferase
  • Pyridostigmine Bromide

Grants and funding

This work was funded by National Natural Science Foundation of China grants 81571086, 81870889, 81200965, and 81430022; National Key R&D Program of China grant 2017YFC1310200; Shanghai Municipal Education Commission‐Gaofeng Clinical Medicine Grant Support grant 20161401; Interdisciplinary Project of Shanghai Jiao Tong University grant YG2016MS64; Research Fund for the Doctoral Program of Higher Education grant 20110073120088; Natural Science Foundation of Science and Technology of Shanghai grant 15ZR1426700; Guang Ci Qing Nian grant GCQN‐2017‐A03.