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

Molecular Psychiatry volume 19, pages 1115–1124 (2014)Cite this article

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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.

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Acknowledgements

We thank Dr Shmuel Mandel for his work on drebrin identification. Initial studies were supported by Allon Therapeutics Inc., Joe and Grace Alter, Barbara and Don Seal, and the Oberfeld family. Further studies were supported by AMN Foundation and the Adams family (Montreal Circle of Friends of Tel Aviv University). Y Ivashco-Pachima is supported by the Joseph Sagol Scholarship for Brain Studies. These studies are in partial fulfilment of the requirements for graduate work at the Dr. Miriam and Sheldon G. Adelson Graduate School of Medicine, and at the Sackler Faculty of Medicine at Tel Aviv University of Drs. S. Oz and N. Skalka, Y. and O Kapitansky (M.Sc.), Y Ivashco-Pachima (Ph.D. studies) and A Malishkevich (Ph.D. studies). Professor Gozes is the incumbent of the Lily and Avraham Gildor Chair for the Investigation of Growth Factors and the Head of the Adams Super Center for Brain Studies, the Levie-Edersheim Gitter fMRI Institute and the Elton Laboratory for Molecular Neuroendocrinology. Professor Gozes is currently a Humboldt Award Recipient and a fellow at the Hanse-Wissenschftenkolleg, Germany.

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Authors and Affiliations

  1. Department of Human Molecular Genetics and Biochemistry, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel,

    S Oz, O Kapitansky, Y Ivashco-Pachima, A Malishkevich, E Giladi & I Gozes

  2. Department of Anatomy, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel,

    N Skalka & R Rosin-Arbesfeld

  3. Department of Interdepartmental Services, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel,

    L Mittelman

  4. Department of Biochemistry and Molecular Biology, George Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel,

    O Segev & J A Hirsch

  5. Sagol School of Neuroscience and Adams Super Center for Brain Studies, Tel Aviv University, Tel Aviv, Israel

    O Segev & I Gozes

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Oz, S., Kapitansky, O., Ivashco-Pachima, Y. et al. The NAP motif of activity-dependent neuroprotective protein (ADNP) regulates dendritic spines through microtubule end binding proteins. Mol Psychiatry 19, 1115–1124 (2014). https://doi.org/10.1038/mp.2014.97

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