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MBC in Press, published online ahead of print March 2, 2005
Mol. Biol. Cell 10.1091/mbc.E04-12-1054

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Submitted on December 10, 2004
Revised on February 8, 2005
Accepted on February 22, 2005

Neurabin/Protein Phosphatase-1 Complex Regulates Dendritic Spine Morphogenesis and Maturation

Ryan T. Terry-Lorenzo,*{dagger}{ddagger} David W. Roadcap,*{dagger} Takeshi Otsuka,{sect} Thomas A. Blanpied,{sect} Pedro L. Zamorano,|| Craig C. Garner,|| Shirish Shenolikar,* and Michael D. Ehlers*{sect}

Departments of *Pharmacology and Cancer Biology, {sect}Neurobiology, and Cell Biology, Duke University Medical Center, Durham, NC 27710; ||Department of Psychiatry and Behavioral Sciences, Nancy Pritzker Laboratory, Stanford University, Palo Alto, CA 94304

Monitoring Editor: Anthony Bretscher

Majority of excitatory synapses in the mammalian brain form on filopodia and spines, actin-rich membrane protrusions present on neuronal dendrites. The biochemical events that induce filopodia and remodel these structures into dendritic spines remain poorly understood. Here, we show that the neuronal actin- and protein phosphatase-1-binding protein, neurabin-I, promotes filopodia in neurons and nonneuronal cells. Neurabin-I actin-binding domain bundled F-actin, promoted filopodia, and delayed the maturation of dendritic spines in cultured hippocampal neurons. In contrast, dimerization of neurabin-I via C-terminal coiled-coil domains and association of protein phosphatase-1 (PP1) with neurabin-I through a canonical KIXF motif inhibited filopodia. Furthermore, the expression of a neurabin-I polypeptide unable to bind PP1 delayed the maturation of neuronal filopodia into spines, reduced the synaptic targeting of AMPA-type glutamate (GluR1) receptors, and decreased AMPA receptor-mediated synaptic transmission. Reduction of endogenous neurabin levels by interference RNA (RNAi) mediated knockdown also inhibited the surface expression of GluR1 receptors. Together, our studies suggested that disrupting the functions of a cytoskeletal neurabin/PP1 complex enhanced filopodia and impaired surface GluR1 expression in hippocampal neurons, thereby hindering the morphological and functional maturation of dendritic spines.

{dagger}These two authors contributed equally to this work.

{ddagger}Present address: Department of Psychiatry and Behavioral Sciences, Nancy Pritzker Laboratory, Stanford University, Palo Alto, CA 94304.

Address correspondence to: Shirish Shenolikar (sheno001{at}mc.duke.edu)




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