Digenic inheritance of STUB1 variants and TBP polyglutamine expansions explains the incomplete penetrance of SCA17 and SCA48

Genet Med. 2022 Jan;24(1):29-40. doi: 10.1016/j.gim.2021.08.003. Epub 2021 Nov 30.

Abstract

Purpose: This study aimed to unravel the genetic factors underlying missing heritability in spinocerebellar ataxia type 17 (SCA17) caused by polyglutamine-encoding CAG/CAA repeat expansions in the TBP gene. Alleles with >49 CAG/CAA repeats are fully penetrant. Most patients, however, carry intermediate TBP41-49 alleles that show incomplete penetrance.

Methods: Using next-generation sequencing approaches, we investigated 40 SCA17/TBP41-54 index patients, their affected (n = 55) and unaffected (n = 51) relatives, and a cohort of patients with ataxia (n = 292).

Results: All except 1 (30/31) of the index cases with TBP41-46 alleles carried a heterozygous pathogenic variant in the STUB1 gene associated with spinocerebellar ataxias SCAR16 (autosomal recessive) and SCA48 (autosomal dominant). No STUB1 variant was found in patients carrying TBP47-54 alleles. TBP41-46 expansions and STUB1 variants cosegregate in all affected family members, whereas the presence of either TBP41-46 expansions or STUB1 variants individually was never associated with the disease.

Conclusion: Our data reveal an unexpected genetic interaction between STUB1 and TBP in the pathogenesis of SCA17 and raise questions on the existence of SCA48 as a monogenic disease with crucial implications for diagnosis and counseling. They provide a convincing explanation for the incomplete penetrance of intermediate TBP alleles and demonstrate a dual inheritance pattern for SCA17, which is a monogenic dominant disorder for TBP≥47 alleles and a digenic TBP/STUB1 disease (SCA17-DI) for intermediate expansions.

Keywords: CHIP; Digenic disease; Huntington disease-like phenotype; Polyglutamine; Spinocerebellar ataxia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Humans
  • Penetrance
  • Peptides* / genetics
  • Spinocerebellar Ataxias* / genetics
  • Spinocerebellar Ataxias* / pathology
  • TATA-Box Binding Protein* / genetics
  • Trinucleotide Repeat Expansion / genetics
  • Ubiquitin-Protein Ligases* / genetics

Substances

  • Peptides
  • TATA-Box Binding Protein
  • TBP protein, human
  • polyglutamine
  • STUB1 protein, human
  • Ubiquitin-Protein Ligases