Molecular Dissection of Neuroligin 2 and Slitrk3 Reveals an Essential Framework for GABAergic Synapse Development

Neuron - Tập 96 - Trang 808-826.e8 - 2017
Jun Li1, Wenyan Han1, Kenneth A. Pelkey2, Jingjing Duan1, Xia Mao1, Ya-Xian Wang3, Michael T. Craig4, Lijin Dong5, Ronald S. Petralia3, Chris J. McBain2, Wei Lu1
1Synapse and Neural Circuit Research Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, 20892, USA
2Program in Developmental Neuroscience, Eunice Kennedy-Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892, USA
3Advanced Imaging Core, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, MD 20892, USA
4Institute of Biomedical and Clinical Sciences, University of Exeter Medical School, Hatherly Laboratories, University of Exeter, Prince of Wales Road, Exeter EX4 4PS, UK
5Genetic Engineering Core, National Eye Institute, National Institutes of Health, Bethesda, MD 20892, USA

Tài liệu tham khảo

Aceti, 2015, Syngap1 haploinsufficiency damages a postnatal critical period of pyramidal cell structural maturation linked to cortical circuit assembly, Biol. Psychiatry, 77, 805, 10.1016/j.biopsych.2014.08.001 Ango, 2004, Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment, Cell, 119, 257, 10.1016/j.cell.2004.10.004 Ashrafi, 2014, Neuronal Ig/Caspr recognition promotes the formation of axoaxonic synapses in mouse spinal cord, Neuron, 81, 120, 10.1016/j.neuron.2013.10.060 Bloodgood, 2013, The activity-dependent transcription factor NPAS4 regulates domain-specific inhibition, Nature, 503, 121, 10.1038/nature12743 Buzsáki, 2012, Mechanisms of gamma oscillations, Annu. Rev. Neurosci., 35, 203, 10.1146/annurev-neuro-062111-150444 Chanda, 2017, Unique versus redundant functions of Neuroligin genes in shaping excitatory and inhibitory synapse properties, J. Neurosci., 37, 6816, 10.1523/JNEUROSCI.0125-17.2017 Cherubini, 2001, Generating diversity at GABAergic synapses, Trends Neurosci., 24, 155, 10.1016/S0166-2236(00)01724-0 Chih, 2005, Control of excitatory and inhibitory synapse formation by neuroligins, Science, 307, 1324, 10.1126/science.1107470 Chubykin, 2007, Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2, Neuron, 54, 919, 10.1016/j.neuron.2007.05.029 Craig, 2007, Neurexin-neuroligin signaling in synapse development, Curr. Opin. Neurobiol., 17, 43, 10.1016/j.conb.2007.01.011 Csicsvari, 1999, Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat, J. Neurosci., 19, 274, 10.1523/JNEUROSCI.19-01-00274.1999 Dalva, 2007, Cell adhesion molecules: signalling functions at the synapse, Nat. Rev. Neurosci., 8, 206, 10.1038/nrn2075 de Wit, 2016, Specification of synaptic connectivity by cell surface interactions, Nat. Rev. Neurosci., 17, 22, 10.1038/nrn.2015.3 Ellender, 2010, Priming of hippocampal population bursts by individual perisomatic-targeting interneurons, J. Neurosci., 30, 5979, 10.1523/JNEUROSCI.3962-09.2010 Fisahn, 1998, Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro, Nature, 394, 186, 10.1038/28179 Futai, 2013, Specific trans-synaptic interaction with inhibitory interneuronal neurexin underlies differential ability of neuroligins to induce functional inhibitory synapses, J. Neurosci., 33, 3612, 10.1523/JNEUROSCI.1811-12.2013 Gabriel, 2014, Brain slice biotinylation: an ex vivo approach to measure region-specific plasma membrane protein trafficking in adult neurons, J. Vis. Exp., 10.3791/51240 Giannone, 2013, Neurexin-1β binding to neuroligin-1 triggers the preferential recruitment of PSD-95 versus gephyrin through tyrosine phosphorylation of neuroligin-1, Cell Rep., 3, 1996, 10.1016/j.celrep.2013.05.013 Graf, 2004, Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins, Cell, 119, 1013, 10.1016/j.cell.2004.11.035 Gu, 2016, An NMDA receptor-dependent mechanism underlies inhibitory synapse development, Cell Rep., 14, 471, 10.1016/j.celrep.2015.12.061 Huang, 2008, GABA and neuroligin signaling: linking synaptic activity and adhesion in inhibitory synapse development, Curr. Opin. Neurobiol., 18, 77, 10.1016/j.conb.2008.05.008 Kins, 2000, Collybistin, a newly identified brain-specific GEF, induces submembrane clustering of gephyrin, Nat. Neurosci., 3, 22, 10.1038/71096 Klausberger, 2008, Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations, Science, 321, 53, 10.1126/science.1149381 Ko, 2015, The balancing act of GABAergic synapse organizers, Trends Mol. Med., 21, 256, 10.1016/j.molmed.2015.01.004 Krueger-Burg, 2017, Organizers of inhibitory synapses come of age, Curr. Opin. Neurobiol., 45, 66, 10.1016/j.conb.2017.04.003 Kubota, 2016, The diversity of cortical inhibitory synapses, Front. Neural Circuits, 10, 27, 10.3389/fncir.2016.00027 Kuzirian, 2011, Emerging themes in GABAergic synapse development, Prog. Neurobiol., 95, 68, 10.1016/j.pneurobio.2011.07.002 Kwon, 2012, Neuroligin-1-dependent competition regulates cortical synaptogenesis and synapse number, Nat. Neurosci., 15, 1667, 10.1038/nn.3256 Liang, 2015, Conditional knockout of Nlgn2 in the adult medial prefrontal cortex (mPFC) induces delayed loss of inhibitory synapses, Mol. Psychiatry, 20, 793, 10.1038/mp.2015.82 Lu, 2009, Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach, Neuron, 62, 254, 10.1016/j.neuron.2009.02.027 Lu, 2017, Regulation of GABAergic synapse development by postsynaptic membrane proteins, Brain Res. Bull., 129, 30, 10.1016/j.brainresbull.2016.07.004 Mann, 2005, Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro, Neuron, 45, 105, 10.1016/j.neuron.2004.12.016 McAllister, 2007, Dynamic aspects of CNS synapse formation, Annu. Rev. Neurosci., 30, 425, 10.1146/annurev.neuro.29.051605.112830 Missler, 2012, Synaptic cell adhesion, Cold Spring Harb. Perspect. Biol., 4, a005694, 10.1101/cshperspect.a005694 Nguyen, 2016, Distinct roles for extracellular and intracellular domains in neuroligin function at inhibitory synapses, eLife, 5, 10.7554/eLife.19236 Pang, 2010, Calmodulin controls synaptic strength via presynaptic activation of calmodulin kinase II, J. Neurosci., 30, 4132, 10.1523/JNEUROSCI.3129-09.2010 Panzanelli, 2017, Differential role of GABAA receptors and neuroligin 2 for perisomatic GABAergic synapse formation in the hippocampus, Brain Struct. Funct., 10.1007/s00429-017-1462-7 Papadopoulos, 2007, Impaired GABAergic transmission and altered hippocampal synaptic plasticity in collybistin-deficient mice, EMBO J., 26, 3888, 10.1038/sj.emboj.7601819 Papadopoulos, 2008, Collybistin is required for both the formation and maintenance of GABAergic postsynapses in the hippocampus, Mol. Cell. Neurosci., 39, 161, 10.1016/j.mcn.2008.06.006 Pelkey, 2015, Pentraxins coordinate excitatory synapse maturation and circuit integration of parvalbumin interneurons, Neuron, 85, 1257, 10.1016/j.neuron.2015.02.020 Poulopoulos, 2009, Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin, Neuron, 63, 628, 10.1016/j.neuron.2009.08.023 Poulopoulos, 2012, Homodimerization and isoform-specific heterodimerization of neuroligins, Biochem. J., 446, 321, 10.1042/BJ20120808 Ramamoorthi, 2011, The contribution of GABAergic dysfunction to neurodevelopmental disorders, Trends Mol. Med., 17, 452, 10.1016/j.molmed.2011.03.003 Sanes, 2009, Many paths to synaptic specificity, Annu. Rev. Cell Dev. Biol., 25, 161, 10.1146/annurev.cellbio.24.110707.175402 Sassoè-Pognetto, 2011, Understanding the molecular diversity of GABAergic synapses, Front. Cell. Neurosci., 5, 4, 10.3389/fncel.2011.00004 Scheiffele, 2000, Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons, Cell, 101, 657, 10.1016/S0092-8674(00)80877-6 Shen, 2010, Genetics and cell biology of building specific synaptic connectivity, Annu. Rev. Neurosci., 33, 473, 10.1146/annurev.neuro.051508.135302 Shipman, 2011, Functional dependence of neuroligin on a new non-PDZ intracellular domain, Nat. Neurosci., 14, 718, 10.1038/nn.2825 Siddiqui, 2011, Synaptic organizing complexes, Curr. Opin. Neurobiol., 21, 132, 10.1016/j.conb.2010.08.016 Soykan, 2014, A conformational switch in collybistin determines the differentiation of inhibitory postsynapses, EMBO J., 33, 2113, 10.15252/embj.201488143 Südhof, 2008, Neuroligins and neurexins link synaptic function to cognitive disease, Nature, 455, 903, 10.1038/nature07456 Takahashi, 2012, Selective control of inhibitory synapse development by Slitrk3-PTPdelta trans-synaptic interaction, Nat. Neurosci., 15, 389, 10.1038/nn.3040 Tretter, 2012, Gephyrin, the enigmatic organizer at GABAergic synapses, Front. Cell. Neurosci., 6, 23, 10.3389/fncel.2012.00023 Tyagarajan, 2014, Gephyrin: a master regulator of neuronal function?, Nat. Rev. Neurosci., 15, 141, 10.1038/nrn3670 Varoqueaux, 2004, Neuroligin 2 is exclusively localized to inhibitory synapses, Eur. J. Cell Biol., 83, 449, 10.1078/0171-9335-00410 Varoqueaux, 2006, Neuroligins determine synapse maturation and function, Neuron, 51, 741, 10.1016/j.neuron.2006.09.003 Waites, 2005, Mechanisms of vertebrate synaptogenesis, Annu. Rev. Neurosci., 28, 251, 10.1146/annurev.neuro.27.070203.144336 Yamasaki, 2017, GARLH family proteins stabilize GABAA receptors at synapses, Neuron, 93, 1138, 10.1016/j.neuron.2017.02.023 Yim, 2013, Slitrks control excitatory and inhibitory synapse formation with LAR receptor protein tyrosine phosphatases, Proc. Natl. Acad. Sci. USA, 110, 4057, 10.1073/pnas.1209881110 Yoshida, 2011, IL-1 receptor accessory protein-like 1 associated with mental retardation and autism mediates synapse formation by trans-synaptic interaction with protein tyrosine phosphatase δ, J. Neurosci., 31, 13485, 10.1523/JNEUROSCI.2136-11.2011 Zhang, 2015, Neuroligins sculpt cerebellar purkinje-cell circuits by differential control of distinct classes of synapses, Neuron, 87, 781, 10.1016/j.neuron.2015.07.020