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Wu, Xiaoting; Morishita, Wade K.; Riley, Ashley M.; Hale, William D.; Südhof, Thomas C.; Malenka, Robert C.
Neuron (Cambridge, Mass.), 05/2019, Volume: 102, Issue: 3Journal Article
Neuroligins, postsynaptic cell adhesion molecules that are linked to neuropsychiatric disorders, are extensively studied, but fundamental questions about their functions remain. Using in vivo replacement strategies in quadruple conditional knockout mice of all neuroligins to avoid heterodimerization artifacts, we show, in hippocampal CA1 pyramidal neurons, that neuroligin-1 performs two key functions in excitatory synapses by distinct molecular mechanisms. N-methyl-D-aspartate (NMDA) receptor-dependent LTP requires trans-synaptic binding of postsynaptic neuroligin-1 to presynaptic β-neurexins but not the cytoplasmic sequences of neuroligins. In contrast, postsynaptic NMDA receptor (NMDAR)-mediated responses involve a neurexin-independent mechanism that requires the neuroligin-1 cytoplasmic sequences. Strikingly, deletion of neuroligins blocked the spine expansion associated with LTP, as monitored by two-photon imaging; this block involved a mechanism identical to that of the role of neuroligin-1 in NMDAR-dependent LTP. Our data suggest that neuroligin-1 performs two mechanistically distinct signaling functions and that neurolign-1-mediated trans-synaptic cell adhesion signaling critically regulates LTP. •Nlgn1 extracellular domain is sufficient to rescue LTP loss in cells lacking Nlgns•Nlgn1 intracellular domain is crucial for basal NMDAR-mediated transmission•Binding of Nlgn1 to presynaptic β-Nrxns is essential for LTP•Spine growth during LTP also requires Nlgn1 binding to β-Nrnxs At excitatory synapses on CA1 pyramidal neurons lacking neuroligins, Nlgn1 rescues impairments in functional and structural LTP and in NMDA receptor-mediated synaptic transmission. Structure-function rescue experiments reveal that Nlgn1 plays mechanistically distinct roles in LTP and basal NMDA receptor-mediated transmission.
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