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J. Biol. Chem., Vol. 283, Issue 39, 26461-26467, September 26, 2008

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RIBEYE Recruits Munc119, a Mammalian Ortholog of the Caenorhabditis elegans Protein unc119, to Synaptic Ribbons of Photoreceptor Synapses^*

Kannan Alpadi, Venkat Giri Magupalli, Stefanie Käppel, Louise Köblitz, Karin Schwarz, Gail M. Seigel¹, Ching-Hwa Sung^¶, and Frank Schmitz²

From the Department of Neuroanatomy, Institute for Anatomy and Cell Biology, Saarland University, Medical School Homburg/Saar, 66421 Homburg/Saar, Germany, the Department of Ophthalmology, Physiology, and Biophysics, SUNY University at Buffalo, Buffalo, New York 14214, and the ^¶Margaret M. Dyson Vision Research Institute, Department of Ophthalmology, Cell and Developmental Biology, Weill Medical College of Cornell University, New York, New York 10021

Munc119 (also denoted as RG4) is a mammalian ortholog of the Caenorhabditis elegans protein unc119 and is essential for vision and synaptic transmission at photoreceptor ribbon synapses by unknown molecular mechanisms. Munc119/RG4 is related to the prenyl-binding protein PrBP/ and expressed at high levels in photoreceptor ribbon synapses. Synaptic ribbons are presynaptic specializations in the active zone of these tonically active synapses and contain RIBEYE as a unique and major component. In the present study, we identified Munc119 as a RIBEYE-interacting protein at photoreceptor ribbon synapses using five independent approaches. The PrBP/ homology domain of Munc119 is essential for the interaction with the NADH binding region of RIBEYE(B) domain. But RIBEYE-Munc119 interaction does not depend on NADH binding. A RIBEYE point mutant (RE(B)E844Q) that no longer interacted with Munc119 still bound NADH, arguing that binding of Munc119 and NADH to RIBEYE are independent from each other. Our data indicate that Munc119 is a synaptic ribbon-associated component. We show that Munc119 can be recruited to synaptic ribbons via its interaction with RIBEYE. Our data suggest that the RIBEYE-Munc119 interaction is essential for synaptic transmission at the photoreceptor ribbon synapse.

Received for publication, February 28, 2008 , and in revised form, July 7, 2008.

^* This work was supported by the Sonderforschungsbereich 530 (SFB530) (TPC11) and by HOMFOR (to F. S.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) BC103449.1.

The on-line version of this article (available at http://www.jbc.org) contains supplemental materials and Figs. S1–S6.

¹ Supported by the Sybil Harrington Scholar Award from Research to Prevent Blindness and 5R24EY016662.

² To whom correspondence should be addressed: Dept. of Neuroanatomy, Institute for Anatomy and Cell Biology, Bldg. 61, Saarland University, Medical School Homburg/Saar, 66421 Homburg/Saar. Tel.: 49-6841-1626012; Fax: 49-6841-1626121; E-mail: frank.schmitz{at}uniklinikum-saarland.de.

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