The NAP motif of activity-dependent neuroprotective protein (ADNP) regulates dendritic spines through microtubule end binding proteins

Mol Psychiatry. 2014 Oct;19(10):1115-24. doi: 10.1038/mp.2014.97. Epub 2014 Sep 2.

Abstract

The NAP motif of activity-dependent neuroprotective protein (ADNP) enhanced memory scores in patients suffering from mild cognitive impairment and protected activities of daily living in schizophrenia patients, while fortifying microtubule (MT)-dependent axonal transport, in mice and flies. The question is how does NAP fortify MTs? Our sequence analysis identified the MT end-binding protein (EB1)-interacting motif SxIP (SIP, Ser-Ile-Pro) in ADNP/NAP and showed specific SxIP binding sites in all members of the EB protein family (EB1-3). Others found that EB1 enhancement of neurite outgrowth is attenuated by EB2, while EB3 interacts with postsynaptic density protein 95 (PSD-95) to modulate dendritic plasticity. Here, NAP increased PSD-95 expression in dendritic spines, which was inhibited by EB3 silencing. EB1 or EB3, but not EB2 silencing inhibited NAP-mediated cell protection, which reflected NAP binding specificity. NAPVSKIPQ (SxIP=SKIP), but not NAPVAAAAQ mimicked NAP activity. ADNP, essential for neuronal differentiation and brain formation in mouse, a member of the SWI/SNF chromatin remodeling complex and a major protein mutated in autism and deregulated in schizophrenia in men, showed similar EB interactions, which were enhanced by NAP treatment. The newly identified shared MT target of NAP/ADNP is directly implicated in synaptic plasticity, explaining the breadth and efficiency of neuroprotective/neurotrophic capacities.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • COS Cells
  • Cells, Cultured
  • Chlorocebus aethiops
  • Dendritic Spines / physiology*
  • Disks Large Homolog 4 Protein
  • Escherichia coli
  • Guanylate Kinases / metabolism
  • Homeodomain Proteins / metabolism*
  • Humans
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Membrane Proteins / metabolism
  • Microtubule-Associated Proteins / metabolism
  • Microtubules / metabolism*
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Neurons / physiology
  • PC12 Cells
  • Protein Interaction Domains and Motifs
  • Rats
  • Recombinant Proteins / metabolism
  • Tubulin / metabolism

Substances

  • ADNP protein, rat
  • Adnp protein, mouse
  • Disks Large Homolog 4 Protein
  • Dlg4 protein, mouse
  • Dlg4 protein, rat
  • Homeodomain Proteins
  • Intracellular Signaling Peptides and Proteins
  • MAPRE1 protein, human
  • MAPRE3 protein, human
  • Mapre1 protein, rat
  • Mapre3 protein, rat
  • Membrane Proteins
  • Microtubule-Associated Proteins
  • Nerve Tissue Proteins
  • Recombinant Proteins
  • Tubulin
  • Guanylate Kinases