p35 regulates the CRM1-dependent nucleocytoplasmic shuttling of nuclear hormone receptor coregulator-interacting factor 1 (NIF-1)

PLoS One. 2014 Oct 16;9(10):e110584. doi: 10.1371/journal.pone.0110584. eCollection 2014.

Abstract

Cyclin-dependent kinase 5 (Cdk5) is a proline-directed serine/threonine kinase, which plays critical roles in a wide spectrum of neuronal functions including neuronal survival, neurite outgrowth, and synapse development and plasticity. Cdk5 activity is controlled by its specific activators: p35 or p39. While knockout studies reveal that Cdk5/p35 is critical for neuronal migration during early brain development, functions of Cdk5/p35 have been unraveled through the identification of the interacting proteins of p35, most of which are Cdk5/p35 substrates. However, it remains unclear whether p35 can regulate neuronal functions independent of Cdk5 activity. Here, we report that a nuclear protein, nuclear hormone receptor coregulator (NRC)-interacting factor 1 (NIF-1), is a new interacting partner of p35. Interestingly, p35 regulates the functions of NIF-1 independent of Cdk5 activity. NIF-1 was initially discovered as a transcriptional regulator that enhances the transcriptional activity of nuclear hormone receptors. Our results show that p35 interacts with NIF-1 and regulates its nucleocytoplasmic trafficking via the nuclear export pathway. Furthermore, we identified a nuclear export signal on p35; mutation of this site or blockade of the CRM1/exportin-dependent nuclear export pathway resulted in the nuclear accumulation of p35. Intriguingly, blocking the nuclear export of p35 attenuated the nuclear accumulation of NIF-1. These findings reveal a new p35-dependent mechanism in transcriptional regulation that involves the nucleocytoplasmic shuttling of transcription regulators.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus / genetics*
  • Animals
  • COS Cells
  • Chlorocebus aethiops
  • Cytoplasm / genetics
  • Cytoplasm / metabolism
  • DNA-Binding Proteins
  • Exportin 1 Protein
  • Gene Expression Regulation, Developmental
  • Intracellular Signaling Peptides and Proteins / biosynthesis*
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Karyopherins / genetics
  • Mice
  • Nerve Tissue Proteins / biosynthesis*
  • Nerve Tissue Proteins / genetics
  • Neurons / metabolism
  • Neurons / physiology*
  • Nuclear Proteins / biosynthesis*
  • Nuclear Proteins / metabolism
  • Phosphorylation
  • Receptors, Cytoplasmic and Nuclear / genetics
  • Transcription Factors

Substances

  • DNA-Binding Proteins
  • Intracellular Signaling Peptides and Proteins
  • Karyopherins
  • Nerve Tissue Proteins
  • Nuclear Proteins
  • Receptors, Cytoplasmic and Nuclear
  • Transcription Factors
  • Znf335 protein, mouse
  • neuronal Cdk5 activator (p25-p35)

Grants and funding

This study was supported in part by the Research Grants Council of Hong Kong SAR (HKUST661109, 660810 and 661111), the National Key Basic Research Program of China (2013CB530900), the Hong Kong Research Grants Council Theme-based Research Scheme (T13-607/12R), and the Innovation and Technology Fund for State Key Laboratory (ITCPT/17-9). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.