Differential alternative splicing analysis links variation in ZRSR2 to a novel type of oral-facial-digital syndrome

Genet Med. 2024 Apr;26(4):101059. doi: 10.1016/j.gim.2023.101059. Epub 2023 Dec 27.

Abstract

Purpose: Oral-facial-digital (OFD) syndromes are genetically heterogeneous developmental disorders, caused by pathogenic variants in genes involved in primary cilia formation and function. We identified a previously undescribed type of OFD with brain anomalies, ranging from alobar holoprosencephaly to pituitary anomalies, in 6 unrelated families.

Methods: Exome sequencing of affected probands was supplemented with alternative splicing analysis in patient and control lymphoblastoid and fibroblast cell lines, and primary cilia structure analysis in patient fibroblasts.

Results: In 1 family with 2 affected males, we identified a germline variant in the last exon of ZRSR2, NM_005089.4:c.1211_1212del NP_005080.1:p.(Gly404GlufsTer23), whereas 7 affected males from 5 unrelated families were hemizygous for the ZRSR2 variant NM_005089.4:c.1207_1208del NP_005080.1:p.(Arg403GlyfsTer24), either occurring de novo or inherited in an X-linked recessive pattern. ZRSR2, located on chromosome Xp22.2, encodes a splicing factor of the minor spliceosome complex, which recognizes minor introns, representing 0.35% of human introns. Patient samples showed significant enrichment of minor intron retention. Among differentially spliced targets are ciliopathy-related genes, such as TMEM107 and CIBAR1. Primary fibroblasts containing the NM_005089.4:c.1207_1208del ZRSR2 variant had abnormally elongated cilia, confirming an association between defective U12-type intron splicing, OFD and abnormal primary cilia formation.

Conclusion: We introduce a novel type of OFD associated with elongated cilia and differential splicing of minor intron-containing genes due to germline variation in ZRSR2.

Keywords: Differential Splicing; Holoprosencephaly; Minor Spliceosome; Orofaciodigital Syndrome; ZRSR2.

Publication types

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

MeSH terms

  • Alternative Splicing* / genetics
  • Humans
  • Introns
  • Male
  • Orofaciodigital Syndromes* / genetics
  • RNA Splicing
  • Ribonucleoproteins / genetics
  • Spliceosomes / genetics

Substances

  • ZRSR2 protein, human
  • Ribonucleoproteins