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The Journal of Neuroscience, October 6, 2004, 24(40):8641-8650; doi:10.1523/JNEUROSCI.2892-04.2004

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Cellular/Molecular
The Zebrafish nrc Mutant Reveals a Role for the Polyphosphoinositide Phosphatase Synaptojanin 1 in Cone Photoreceptor Ribbon Anchoring

Heather A. Van Epps,¹ Mitsuko Hayashi,² Louise Lucast,² George W. Stearns,¹ James B. Hurley,¹ Pietro De Camilli,² and Susan E. Brockerhoff¹

¹Department of Biochemistry, University of Washington School of Medicine, Seattle, Washington 98195, and ²Department of Cell Biology and Howard Hughes Medical Institute, Boyer Center for Molecular Medicine, Yale University School of Medicine, New Haven, Connecticut 06510

Visual, vestibular, and auditory neurons rely on ribbon synapses for rapid continuous release and recycling of synaptic vesicles. Molecular mechanisms responsible for the properties of ribbon synapses are mostly unknown. The zebrafish vision mutant nrc has unanchored ribbons and abnormal synaptic transmission at cone photoreceptor synapses. We used positional cloning to identify the nrc mutation as a premature stop codon in the synaptojanin1 (synj1) gene. Synaptojanin 1 (Synj1) is undetectable in nrc extracts, and biochemical activities associated with it are reduced. Furthermore, morpholinos directed against synj1 phenocopy the nrc mutation. Synj1 is a polyphosphoinositide phosphatase important at conventional synapses for clathrin-mediated endocytosis and actin cytoskeletal rearrangement. In the nrc cone photoreceptor pedicle, not only are ribbons unanchored, but synaptic vesicles are reduced in number, abnormally distributed, and interspersed within a dense cytoskeletal matrix. Our findings reveal a new role for Synj1 and link phosphoinositide metabolism to ribbon architecture and function at the cone photoreceptor synapse.

Key words: ribbon synapse; synaptojanin; retina; cone photoreceptor; zebrafish; sensory neurons

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Received July 16, 2004; revised August 20, 2004; accepted August 24, 2004.

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