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The Journal of Neuroscience, March 14, 2007, 27(11):2815-2824; doi:10.1523/JNEUROSCI.0032-07.2007

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Cellular/Molecular
Silencing of Neuroligin Function by Postsynaptic Neurexins

Hiroki Taniguchi,¹ Leora Gollan,¹ Francisco G. Scholl,¹ Veeravan Mahadomrongkul,² Elizabeth Dobler,² Nicolas Limthong,¹ Morgen Peck,¹ Chiye Aoki,² and Peter Scheiffele¹

¹Department of Physiology and Cellular Biophysics, Center for Neurobiology and Behavior, Columbia University, Physicians and Surgeons 11-511, New York, New York 10032, and ²Center for Neural Science, New York University, New York, New York 10003

Correspondence should be addressed to Peter Scheiffele, Columbia University, Department of Physiology and Cellular Biophysics, 630 West 168th Street, Physicians and Surgeons 11-511, New York, NY 10032. Email: ps2018{at}columbia.edu

The formation of neuronal circuits during development involves a combination of synapse stabilization and elimination events. Synaptic adhesion molecules are thought to play an important role in synaptogenesis, and several trans-synaptic adhesion systems that promote the formation and maturation of synapses have been identified. The neuroligin–neurexin complex is a heterophilic adhesion system that promotes assembly and maturation of synapses through bidirectional signaling. In this protein complex, postsynaptic neuroligins are thought to interact trans-synaptically with presynaptic neurexins. However, the subcellular localization of neurexins has not been determined. Using immunoelectron microscopy, we found that endogenous neurexins and epitope-tagged neurexin-1ß are localized to axons and presynaptic terminals in vivo. Unexpectedly, neurexins are also abundant in the postsynaptic density. cis-expression of neurexin-1ß with neuroligin-1 inhibits trans-binding to recombinant neurexins, blocks the synaptogenic activity of neuroligin-1, and reduces the density of presynaptic terminals in cultured hippocampal neurons. Our results demonstrate that the function of neurexin proteins is more diverse than previously anticipated and suggest that postsynaptic cis-interactions might provide a novel mechanism for silencing the activity of a synaptic adhesion complex.

Key words: synapse formation; hippocampus; adhesion; neuroligin; neurexin; hippocampal neurons

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Received June 7, 2006; revised Feb. 2, 2007; accepted Feb. 2, 2007.

Correspondence should be addressed to Peter Scheiffele, Columbia University, Department of Physiology and Cellular Biophysics, 630 West 168th Street, Physicians and Surgeons 11-511, New York, NY 10032. Email: ps2018{at}columbia.edu

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