SPSB1-mediated HnRNP A1 ubiquitylation regulates alternative splicing and cell migration in EGF signaling

Cell Res. 2017 Apr;27(4):540-558. doi: 10.1038/cr.2017.7. Epub 2017 Jan 13.

Abstract

Extracellular signals have been shown to impact on alternative pre-mRNA splicing; however, the molecular mechanisms and biological significance of signal-induced splicing regulation remain largely unknown. Here, we report that epidermal growth factor (EGF) induces splicing changes through ubiquitylation of a well-known splicing regulator, hnRNP A1. EGF signaling upregulates an E3 ubiquitin (Ub) ligase adaptor, SPRY domain-containing SOCS box protein 1 (SPSB1), which recruits Elongin B/C-Cullin complexes to conjugate lysine 29-linked polyUb chains onto hnRNP A1. Importantly, SPSB1 and ubiquitylation of hnRNP A1 have a critical role in EGF-driven cell migration. Mechanistically, EGF-induced ubiquitylation of hnRNP A1 together with the activation of SR protein kinases (SRPKs) results in the upregulation of a Rac1 splicing isoform, Rac1b, to promote cell motility. These findings unravel a novel crosstalk between protein ubiquitylation and alternative splicing in EGF/EGF receptor signaling, and identify a new EGF/SPSB1/hnRNP A1/Rac1 axis in modulating cell migration, which may have important implications for cancer treatment.

MeSH terms

  • Alternative Splicing / genetics*
  • Cell Movement* / drug effects
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism
  • Cullin Proteins / metabolism
  • Elongin / metabolism
  • Epidermal Growth Factor / pharmacology*
  • ErbB Receptors / metabolism
  • HEK293 Cells
  • HeLa Cells
  • Heterogeneous Nuclear Ribonucleoprotein A1 / metabolism*
  • Humans
  • Lysine / metabolism
  • Polyubiquitin / metabolism
  • Protein Binding / drug effects
  • RNA Precursors / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Signal Transduction* / drug effects
  • Suppressor of Cytokine Signaling Proteins / metabolism*
  • Ubiquitination* / drug effects
  • rac1 GTP-Binding Protein / metabolism

Substances

  • Cullin Proteins
  • Elongin
  • Heterogeneous Nuclear Ribonucleoprotein A1
  • RNA Precursors
  • RNA, Messenger
  • SPSB1 protein, human
  • Suppressor of Cytokine Signaling Proteins
  • Polyubiquitin
  • Epidermal Growth Factor
  • ErbB Receptors
  • rac1 GTP-Binding Protein
  • Lysine