Long-read sequencing identifies an SVA_D retrotransposon insertion deep within the intron of ATP7A as a novel cause of occipital horn syndrome

J Med Genet. 2024 Sep 24;61(10):950-958. doi: 10.1136/jmg-2024-110056.

Abstract

Background: SINE-VNTR-Alu (SVA) retrotransposons move from one genomic location to another in a 'copy-and-paste' manner. They continue to move actively and cause monogenic diseases through various mechanisms. Currently, disease-causing SVA retrotransposons are classified into human-specific young SVA_E or SVA_F subfamilies. In this study, we identified an evolutionarily old SVA_D retrotransposon as a novel cause of occipital horn syndrome (OHS). OHS is an X-linked, copper metabolism disorder caused by dysfunction of the copper transporter, ATP7A.

Methods: We investigated a 16-year-old boy with OHS whose pathogenic variant could not be detected via routine molecular genetic analyses.

Results: A 2.8 kb insertion was detected deep within the intron of the patient's ATP7A gene. This insertion caused aberrant mRNA splicing activated by a new donor splice site located within it. Long-read circular consensus sequencing enabled us to accurately read the entire insertion sequence, which contained highly repetitive and GC-rich segments. Consequently, the insertion was identified as an SVA_D retrotransposon. Antisense oligonucleotides (AOs) targeting the new splice site restored the expression of normal transcripts and functional ATP7A proteins. AO treatment alleviated excessive accumulation of copper in patient fibroblasts in a dose-dependent manner. Pedigree analysis revealed that the retrotransposon had moved into the OHS-causing position two generations ago.

Conclusion: This is the first report of a human monogenic disease caused by the SVA_D retrotransposon. The fact that the evolutionarily old SVA_D is still actively transposed, leading to increased copy numbers may make a notable impact on rare genetic disease research.

Keywords: Genetic Diseases, X-Linked; Neurology; Pediatrics; Sequence Analysis.

Publication types

  • Case Reports

MeSH terms

  • Adolescent
  • Alu Elements / genetics
  • Brain Diseases / genetics
  • Brain Diseases / pathology
  • Central Nervous System Cysts / genetics
  • Central Nervous System Cysts / pathology
  • Copper-Transporting ATPases* / genetics
  • Cutis Laxa
  • Ehlers-Danlos Syndrome
  • Genetic Diseases, X-Linked / genetics
  • Genetic Diseases, X-Linked / pathology
  • Humans
  • Introns* / genetics
  • Male
  • Mutagenesis, Insertional / genetics
  • RNA Splicing / genetics
  • Retroelements* / genetics

Substances

  • Copper-Transporting ATPases
  • Retroelements
  • ATP7A protein, human

Supplementary concepts

  • Occipital horn syndrome