ELAV/Hu RNA binding proteins determine multiple programs of neural alternative splicing

PLoS Genet. 2021 Apr 7;17(4):e1009439. doi: 10.1371/journal.pgen.1009439. eCollection 2021 Apr.

Abstract

ELAV/Hu factors are conserved RNA binding proteins (RBPs) that play diverse roles in mRNA processing and regulation. The founding member, Drosophila Elav, was recognized as a vital neural factor 35 years ago. Nevertheless, little was known about its impacts on the transcriptome, and potential functional overlap with its paralogs. Building on our recent findings that neural-specific lengthened 3' UTR isoforms are co-determined by ELAV/Hu factors, we address their impacts on splicing. While only a few splicing targets of Drosophila are known, ectopic expression of each of the three family members (Elav, Fne and Rbp9) alters hundreds of cassette exon and alternative last exon (ALE) splicing choices. Reciprocally, double mutants of elav/fne, but not elav alone, exhibit opposite effects on both classes of regulated mRNA processing events in larval CNS. While manipulation of Drosophila ELAV/Hu RBPs induces both exon skipping and inclusion, characteristic ELAV/Hu motifs are enriched only within introns flanking exons that are suppressed by ELAV/Hu factors. Moreover, the roles of ELAV/Hu factors in global promotion of distal ALE splicing are mechanistically linked to terminal 3' UTR extensions in neurons, since both processes involve bypass of proximal polyadenylation signals linked to ELAV/Hu motifs downstream of cleavage sites. We corroborate the direct action of Elav in diverse modes of mRNA processing using RRM-dependent Elav-CLIP data from S2 cells. Finally, we provide evidence for conservation in mammalian neurons, which undergo broad programs of distal ALE and APA lengthening, linked to ELAV/Hu motifs downstream of regulated polyadenylation sites. Overall, ELAV/Hu RBPs orchestrate multiple broad programs of neuronal mRNA processing and isoform diversification in Drosophila and mammalian neurons.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3' Untranslated Regions / genetics
  • Alternative Splicing / genetics*
  • Animals
  • Cell Differentiation / genetics*
  • Central Nervous System / growth & development
  • Central Nervous System / metabolism
  • Drosophila Proteins / genetics*
  • ELAV Proteins / genetics*
  • ELAV-Like Protein 1 / genetics*
  • Humans
  • Larva / genetics
  • Larva / growth & development
  • Nerve Tissue Proteins / genetics
  • Neurons / metabolism*
  • Polyadenylation / genetics
  • RNA Processing, Post-Transcriptional / genetics
  • RNA, Messenger / genetics
  • RNA-Binding Proteins / genetics
  • Transcriptome / genetics

Substances

  • 3' Untranslated Regions
  • Drosophila Proteins
  • ELAV Proteins
  • ELAV protein, Drosophila
  • ELAV-Like Protein 1
  • ELAVL1 protein, human
  • Nerve Tissue Proteins
  • RNA, Messenger
  • RNA-Binding Proteins
  • Rbp9 protein, Drosophila
  • fne protein, Drosophila