PUBLICATION

Pathogenic proteotoxicity of cryptic splicing is alleviated by ubiquitination and ER-phagy

Authors
Prieto-Garcia, C., Matkovic, V., Mosler, T., Li, C., Liang, J., Oo, J.A., Haidle, F., Mačinković, I., Cabrera-Orefice, A., Berkane, R., Giuliani, G., Xu, F., Jacomin, A.C., Tomaskovic, I., Basoglu, M., Hoffmann, M.E., Rathore, R., Cetin, R., Boutguetait, D., Bozkurt, S., Hernández Cañás, M.C., Keller, M., Busam, J., Shah, V.J., Wittig, I., Kaulich, M., Beli, P., Galej, W.P., Ebersberger, I., Wang, L., Münch, C., Stolz, A., Brandes, R.P., Tse, W.K.F., Eimer, S., Stainier, D.Y.R., Legewie, S., Zarnack, K., Müller-McNicoll, M., Dikic, I.
ID
ZDB-PUB-241115-5
Date
2024
Source
Science (New York, N.Y.)   386: 768776768-776 (Journal)
Registered Authors
Stainier, Didier
Keywords
none
Datasets
GEO:GSE272836
MeSH Terms
  • Mice
  • Zebrafish/genetics
  • Ubiquitin/metabolism
  • RNA Splicing*
  • RNA Splice Sites
  • RNA, Messenger/genetics
  • RNA, Messenger/metabolism
  • Endoplasmic Reticulum*/metabolism
  • Ubiquitination*
  • Proteasome Endopeptidase Complex/metabolism
  • Ubiquitin-Specific Proteases*/genetics
  • Ubiquitin-Specific Proteases*/metabolism
  • Retinitis Pigmentosa*/genetics
  • Retinitis Pigmentosa*/metabolism
  • HEK293 Cells
  • Humans
  • Endoplasmic Reticulum Stress*
  • Autophagy*
  • HeLa Cells
  • Animals
  • Spliceosomes/metabolism
  • Protein Folding
PubMed
39541449 Full text @ Science
Abstract
RNA splicing enables the functional adaptation of cells to changing contexts. Impaired splicing has been associated with diseases, including retinitis pigmentosa, but the underlying molecular mechanisms and cellular responses remain poorly understood. In this work, we report that deficiency of ubiquitin-specific protease 39 (USP39) in human cell lines, zebrafish larvae, and mice led to impaired spliceosome assembly and a cytotoxic splicing profile characterized by the use of cryptic 5' splice sites. Disruptive cryptic variants evaded messenger RNA (mRNA) surveillance pathways and were translated into misfolded proteins, which caused proteotoxic aggregates, endoplasmic reticulum (ER) stress, and, ultimately, cell death. The detrimental consequence of splicing-induced proteotoxicity could be mitigated by up-regulating the ubiquitin-proteasome system and selective autophagy. Our findings provide insight into the molecular pathogenesis of spliceosome-associated diseases.
Genes / Markers
Figures
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Expression
Phenotype
Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Fish
Antibodies
Orthology
Engineered Foreign Genes
Mapping