Disordered protein interactions for an ordered cellular transition: Cdc2-like kinase 1 is transported to the nucleus via its Ser-Arg protein substrate

J Biol Chem. 2019 Jun 14;294(24):9631-9641. doi: 10.1074/jbc.RA119.008463. Epub 2019 May 7.

Abstract

Serine-arginine (SR) proteins are essential splicing factors that promote numerous steps associated with mRNA processing and whose biological function is tightly regulated through multi-site phosphorylation. In the nucleus, the cdc2-like kinases (CLKs) phosphorylate SR proteins on their intrinsically disordered Arg-Ser (RS) domains, mobilizing them from storage speckles to the splicing machinery. The CLKs have disordered N termini that bind tightly to RS domains, enhancing SR protein phosphorylation. The N termini also promote nuclear localization of CLKs, but their transport mechanism is presently unknown. To explore cytoplasmic-nuclear transitions, several classical nuclear localization sequences in the N terminus of the CLK1 isoform were identified, but their mutation had no effect on subcellular localization. Rather, we found that CLK1 amplifies its presence in the nucleus by forming a stable complex with the SR protein substrate and appropriating its NLS for transport. These findings indicate that, along with their well-established roles in mRNA splicing, SR proteins use disordered protein-protein interactions to carry their kinase regulator from the cytoplasm to the nucleus.

Keywords: Arg–Ser repeat; RNA processing; RNA splicing; SR protein; cdc2-like kinase (CLK); intrinsically disordered protein; nuclear translocation; phosphorylation; post-transcriptional regulation; serine/threonine protein kinase; splicing factor.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Sequence
  • Arginine / metabolism*
  • Cell Nucleus / metabolism*
  • HeLa Cells
  • Humans
  • Phosphorylation
  • Protein Conformation
  • Protein Serine-Threonine Kinases / chemistry
  • Protein Serine-Threonine Kinases / metabolism*
  • Protein-Tyrosine Kinases / chemistry
  • Protein-Tyrosine Kinases / metabolism*
  • Sequence Homology
  • Serine / metabolism*
  • Serine-Arginine Splicing Factors / metabolism
  • Substrate Specificity
  • beta Karyopherins / metabolism

Substances

  • SRSF1 protein, human
  • TNPO1 protein, human
  • beta Karyopherins
  • Serine-Arginine Splicing Factors
  • Serine
  • Arginine
  • Clk dual-specificity kinases
  • Protein-Tyrosine Kinases
  • Protein Serine-Threonine Kinases