Multisystem proteinopathies (MSPs) and MSP-like disorders: Clinical-pathological-molecular spectrum

Ann Clin Transl Neurol. 2023 Apr;10(4):632-643. doi: 10.1002/acn3.51751. Epub 2023 Mar 1.

Abstract

Objectives: Mutations in VCP, HNRNPA2B1, HNRNPA1, and SQSTM1, encoding RNA-binding proteins or proteins in quality-control pathways, cause multisystem proteinopathies (MSP). They share pathological findings of protein aggregation and clinical combinations of inclusion body myopathy (IBM), neurodegeneration [motor neuron disorder (MND)/frontotemporal dementia (FTD)], and Paget disease of bone (PDB). Subsequently, additional genes were linked to similar but not full clinical-pathological spectrum (MSP-like disorders). We aimed to define the phenotypic-genotypic spectrum of MSP and MSP-like disorders at our institution, including long-term follow-up features.

Methods: We searched the Mayo Clinic database (January 2010-June 2022) to identify patients with mutations in MSP and MSP-like disorders causative genes. Medical records were reviewed.

Results: Thirty-one individuals (27 families) had pathogenic mutations in: VCP (n = 17), SQSTM1 + TIA1 (n = 5), TIA1 (n = 5), MATR3, HNRNPA1, HSPB8, and TFG (n = 1, each). Myopathy occurred in all but 2 VCP-MSP patients with disease onset at age 52 (median). Weakness pattern was limb-girdle in 12/15 VCP-MSP and HSPB8 patient, and distal-predominant in other MSP and MSP-like disorders. Twenty/24 muscle biopsies showed rimmed vacuolar myopathy. MND and FTD occurred in 5 (4 VCP, 1 TFG) and 4 (3 VCP, 1 SQSTM1 + TIA1) patients, respectively. PDB manifested in 4 VCP-MSP. Diastolic dysfunction occurred in 2 VCP-MSP. After 11.5 years (median) from symptom onset, 15 patients ambulated without gait-aids; loss of ambulation (n = 5) and death (n = 3) were recorded only in VCP-MSP.

Interpretation: VCP-MSP was the most common disorder; rimmed vacuolar myopathy was the most frequent manifestation; distal-predominant weakness occurred frequently in non-VCP-MSP; and cardiac involvement was observed only in VCP-MSP.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Frontotemporal Dementia* / genetics
  • Humans
  • Lysosomal Storage Diseases
  • Middle Aged
  • Muscular Diseases* / genetics
  • Nuclear Matrix-Associated Proteins
  • RNA-Binding Proteins
  • Sequestosome-1 Protein / genetics
  • Valosin Containing Protein / genetics

Substances

  • Valosin Containing Protein
  • Sequestosome-1 Protein
  • MATR3 protein, human
  • RNA-Binding Proteins
  • Nuclear Matrix-Associated Proteins

Supplementary concepts

  • Vacuolar myopathy

Grants and funding

This work was funded by Regenerative Medicine Minnesota grant P008848103.