β-Neurexins Control Neural Circuits by Regulating Synaptic Endocannabinoid Signaling

Aoto, 2013, Presynaptic neurexin-3 alternative splicing trans-synaptically controls postsynaptic AMPA receptor trafficking, Cell, 154, 75, 10.1016/j.cell.2013.05.060 Aoto, 2015, Distinct circuit-dependent functions of presynaptic neurexin-3 at GABAergic and glutamatergic synapses, Nat. Neurosci., 18, 997, 10.1038/nn.4037 Bang, 2013, A matter of balance: role of neurexin and neuroligin at the synapse, Neurochem. Res., 38, 1174, 10.1007/s11064-013-1029-9 Behr, 2009, Synaptic plasticity in the subiculum, Prog. Neurobiol., 89, 334, 10.1016/j.pneurobio.2009.09.002 Boucard, 2005, A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins, Neuron, 48, 229, 10.1016/j.neuron.2005.08.026 Brown, 2004, Endocannabinoids inhibit transmission at granule cell to Purkinje cell synapses by modulating three types of presynaptic calcium channels, J. Neurosci., 24, 5623, 10.1523/JNEUROSCI.0918-04.2004 Castillo, 2012, Endocannabinoid signaling and synaptic function, Neuron, 76, 70, 10.1016/j.neuron.2012.09.020 Chih, 2006, Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex, Neuron, 51, 171, 10.1016/j.neuron.2006.06.005 Clarke, 2014, Balance within the neurexin trans-synaptic connexus stabilizes behavioral control, Front. Hum. Neurosci., 8, 52, 10.3389/fnhum.2014.00052 Comoletti, 2006, Gene selection, alternative splicing, and post-translational processing regulate neuroligin selectivity for β-neurexins, Biochemistry, 45, 12816, 10.1021/bi0614131 de Wit, 2009, LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation, Neuron, 64, 799, 10.1016/j.neuron.2009.12.019 Di Marzo, 2004, The endocannabinoid system and its therapeutic exploitation, Nat. Rev. Drug Discov., 3, 771, 10.1038/nrd1495 Fanselow, 2010, Are the dorsal and ventral hippocampus functionally distinct structures?, Neuron, 65, 7, 10.1016/j.neuron.2009.11.031 Földy, 2013, Autism-associated neuroligin-3 mutations commonly disrupt tonic endocannabinoid signaling, Neuron, 78, 498, 10.1016/j.neuron.2013.02.036 Fowler, 2001, A force-plate actometer for quantitating rodent behaviors: illustrative data on locomotion, rotation, spatial patterning, stereotypies, and tremor, J. Neurosci. Methods, 107, 107, 10.1016/S0165-0270(01)00359-4 Freund, 2003, Role of endogenous cannabinoids in synaptic signaling, Physiol. Rev., 83, 1017, 10.1152/physrev.00004.2003 Graves, 2012, Hippocampal pyramidal neurons comprise two distinct cell types that are countermodulated by metabotropic receptors, Neuron, 76, 776, 10.1016/j.neuron.2012.09.036 Hajos, 2001, Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus, Neuroscience, 106, 1, 10.1016/S0306-4522(01)00287-1 Han, 2012, Acute cannabinoids impair working memory through astroglial CB1 receptor modulation of hippocampal LTD, Cell, 148, 1039, 10.1016/j.cell.2012.01.037 Hessler, 1993, The probability of transmitter release at a mammalian central synapse, Nature, 366, 569, 10.1038/366569a0 Ichtchenko, 1995, Neuroligin 1: a splice site-specific ligand for beta-neurexins, Cell, 81, 435, 10.1016/0092-8674(95)90396-8 Kaeser, 2014, Molecular mechanisms for synchronous, asynchronous, and spontaneous neurotransmitter release, Annu. Rev. Physiol., 76, 333, 10.1146/annurev-physiol-021113-170338 Kaeser, 2011, RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction, Cell, 144, 282, 10.1016/j.cell.2010.12.029 Kano, 2009, Endocannabinoid-mediated control of synaptic transmission, Physiol. Rev., 89, 309, 10.1152/physrev.00019.2008 Katona, 2008, Endocannabinoid signaling as a synaptic circuit breaker in neurological disease, Nat. Med., 14, 923, 10.1038/nm.f.1869 Katona, 2006, Molecular composition of the endocannabinoid system at glutamatergic synapses, J. Neurosci., 26, 5628, 10.1523/JNEUROSCI.0309-06.2006 Kawamura, 2006, The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum, J. Neurosci., 26, 2991, 10.1523/JNEUROSCI.4872-05.2006 Ko, 2009, LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation, Neuron, 64, 791, 10.1016/j.neuron.2009.12.012 Kreitzer, 2001, Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells, Neuron, 29, 717, 10.1016/S0896-6273(01)00246-X Krueger, 2012, The role of neurexins and neuroligins in the formation, maturation, and function of vertebrate synapses, Curr. Opin. Neurobiol., 22, 412, 10.1016/j.conb.2012.02.012 Matsuda, 2011, Cbln family proteins promote synapse formation by regulating distinct neurexin signaling pathways in various brain regions, Eur. J. Neurosci., 33, 1447, 10.1111/j.1460-9568.2011.07638.x Melis, 2014, Interplay between synaptic endocannabinoid signaling and metaplasticity in neuronal circuit function and dysfunction, Eur. J. Neurosci., 39, 1189, 10.1111/ejn.12501 Missler, 2003, α-neurexins couple Ca2+ channels to synaptic vesicle exocytosis, Nature, 423, 939, 10.1038/nature01755 Murataeva, 2014, Parsing the players: 2-arachidonoylglycerol synthesis and degradation in the CNS, Br. J. Pharmacol., 171, 1379, 10.1111/bph.12411 Ohno-Shosaku, 2002, Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses, J. Neurosci., 22, 3864, 10.1523/JNEUROSCI.22-10-03864.2002 Peterfi, 2012, Endocannabinoid-mediated long-term depression of afferent excitatory synapses in hippocampal pyramidal cells and GABAergic interneurons, J. Neurosci., 32, 14448, 10.1523/JNEUROSCI.1676-12.2012 Petrenko, 1996, Structure and evolution of neurexophilin, J. Neurosci., 16, 4360, 10.1523/JNEUROSCI.16-14-04360.1996 Rosenmund, 1993, Nonuniform probability of glutamate release at a hippocampal synapse, Science, 262, 754, 10.1126/science.7901909 Rowen, 2002, Analysis of the human neurexin genes: alternative splicing and the generation of protein diversity, Genomics, 79, 587, 10.1006/geno.2002.6734 Siddiqui, 2010, LRRTMs and neuroligins bind neurexins with a differential code to cooperate in glutamate synapse development, J. Neurosci., 30, 7495, 10.1523/JNEUROSCI.0470-10.2010 Staff, 2000, Resting and active properties of pyramidal neurons in subiculum and CA1 of rat hippocampus, J. Neurophysiol., 84, 2398, 10.1152/jn.2000.84.5.2398 Südhof, 2008, Neuroligins and neurexins link synaptic function to cognitive disease, Nature, 455, 903, 10.1038/nature07456 Szabó, 2014, Presynaptic calcium channel inhibition underlies CB1 cannabinoid receptor-mediated suppression of GABA release, J. Neurosci., 34, 7958, 10.1523/JNEUROSCI.0247-14.2014 Tabuchi, 2002, Structure and evolution of neurexin genes: insight into the mechanism of alternative splicing, Genomics, 79, 849, 10.1006/geno.2002.6780 Takahashi, 2006, The CB1 cannabinoid receptor mediates glutamatergic synaptic suppression in the hippocampus, Neuroscience, 139, 795, 10.1016/j.neuroscience.2006.01.024 Treutlein, 2014, Cartography of neurexin alternative splicing mapped by single-molecule long-read mRNA sequencing, Proc. Natl. Acad. Sci. USA, 111, E1291, 10.1073/pnas.1403244111 Twitchell, 1997, Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons, J. Neurophysiol., 78, 43, 10.1152/jn.1997.78.1.43 Uemura, 2010, Trans-synaptic interaction of GluRdelta2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum, Cell, 141, 1068, 10.1016/j.cell.2010.04.035 Ullrich, 1995, Cartography of neurexins: more than 1000 isoforms generated by alternative splicing and expressed in distinct subsets of neurons, Neuron, 14, 497, 10.1016/0896-6273(95)90306-2 Ushkaryov, 1992, Neurexins: synaptic cell surface proteins related to the alpha-latrotoxin receptor and laminin, Science, 257, 50, 10.1126/science.1621094 Ushkaryov, 1994, Conserved domain structure of beta-neurexins. Unusual cleaved signal sequences in receptor-like neuronal cell-surface proteins, J. Biol. Chem., 269, 11987, 10.1016/S0021-9258(17)32671-6 van Welie, 2006, Different levels of Ih determine distinct temporal integration in bursting and regular-spiking neurons in rat subiculum, J. Physiol., 576, 203, 10.1113/jphysiol.2006.113944 Wozny, 2008, Differential cAMP signaling at hippocampal output synapses, J. Neurosci., 28, 14358, 10.1523/JNEUROSCI.4973-08.2008 Xu, 2009, Synaptotagmin-1 functions as a Ca2+ sensor for spontaneous release, Nat. Neurosci., 12, 759, 10.1038/nn.2320 Xu, 2012, Distinct neuronal coding schemes in memory revealed by selective erasure of fast synchronous synaptic transmission, Neuron, 73, 990, 10.1016/j.neuron.2011.12.036