γ-Protocadherins Interact with Neuroligin-1 and Negatively Regulate Dendritic Spine Morphogenesis

Cell Reports - Tập 18 - Trang 2702-2714 - 2017
Michael J. Molumby1,2, Rachel M. Anderson3, Dillan J. Newbold2, Norah K. Koblesky2, Andrew M. Garrett2, Dietmar Schreiner2, Jason J. Radley3, Joshua A. Weiner1,2,4
1Graduate Program in Genetics, The University of Iowa, Iowa City, IA 52242, USA
2Department of Biology, The University of Iowa, Iowa City, IA 52242, USA
3Department of Psychological and Brain Sciences, The University of Iowa, Iowa City, IA, 52242, USA
4Department of Psychiatry, The University of Iowa, Iowa City, IA 52242, USA

Tài liệu tham khảo

Alvarez, 2006, Retraction of synapses and dendritic spines induced by off-target effects of RNA interference, J. Neurosci., 26, 7820, 10.1523/JNEUROSCI.1957-06.2006 Anderson, 2014, Adrenocortical status predicts the degree of age-related deficits in prefrontal structural plasticity and working memory, J. Neurosci., 34, 8387, 10.1523/JNEUROSCI.1385-14.2014 Bemben, 2014, CaMKII phosphorylation of neuroligin-1 regulates excitatory synapses, Nat. Neurosci., 17, 56, 10.1038/nn.3601 Biederer, 2007, Mixed-culture assays for analyzing neuronal synapse formation, Nat. Protoc., 2, 670, 10.1038/nprot.2007.92 Bloss, 2011, Evidence for reduced experience-dependent dendritic spine plasticity in the aging prefrontal cortex, J. Neurosci., 31, 7831, 10.1523/JNEUROSCI.0839-11.2011 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 Boyer, 1998, Comparison of hippocampal dendritic spines in culture and in brain, J. Neurosci., 18, 5294, 10.1523/JNEUROSCI.18-14-05294.1998 Chen, 2010, Neurexin-neuroligin cell adhesion complexes contribute to synaptotropic dendritogenesis via growth stabilization mechanisms in vivo, Neuron., 67, 967, 10.1016/j.neuron.2010.08.016 Chih, 2005, Control of excitatory and inhibitory synapse formation by neuroligins, Science, 307, 1324, 10.1126/science.1107470 Chih, 2006, Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex, Neuron, 51, 171, 10.1016/j.neuron.2006.06.005 Chubykin, 2005, Dissection of synapse induction by neuroligins: Effect of a neuroligin mutation associated with autism, J. Biol. Chem., 280, 22365, 10.1074/jbc.M410723200 Cline, 2008, The regulation of dendritic arbor development and plasticity by glutamatergic synaptic input: A review of the synaptotrophic hypothesis, J. Physiol., 586, 1509, 10.1113/jphysiol.2007.150029 Comoletti, 2003, Characterization of the interaction of a recombinant soluble neuroligin-1 with neurexin-1beta, J. Biol. Chem., 278, 50497, 10.1074/jbc.M306803200 Dailey, 1996, The dynamics of dendritic structure in developing hippocampal slices, J. Neurosci., 16, 2983, 10.1523/JNEUROSCI.16-09-02983.1996 de Wit, 2016, Specification of synaptic connectivity by cell surface interactions, Nat. Rev. Neurosci., 17, 22, 10.1038/nrn.2015.3 Dean, 2003, Neurexin mediates the assembly of presynaptic terminals, Nat. Neurosci., 6, 708, 10.1038/nn1074 Feng, 2000, Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP, Neuron, 28, 41, 10.1016/S0896-6273(00)00084-2 Fernández-Monreal, 2009, Gamma-protocadherin homophilic interaction and intracellular trafficking is controlled by the cytoplasmic domain in neurons, Mol. Cell. Neurosci., 40, 344, 10.1016/j.mcn.2008.12.002 Fernández-Monreal, 2010, γ-protocadherins are enriched and transported in specialized vesicles associated with the secretory pathway in neurons, Eur. J. Neurosci., 32, 921, 10.1111/j.1460-9568.2010.07386.x Fiala, 1998, Synaptogenesis via dendritic filopodia in developing hippocampal area CA1, J. Neurosci., 18, 8900, 10.1523/JNEUROSCI.18-21-08900.1998 Garrett, 2009, Control of CNS synapse development by gamma-protocadherin-mediated astrocyte-neuron contact, J. Neurosci., 29, 11723, 10.1523/JNEUROSCI.2818-09.2009 Garrett, 2012, γ-protocadherins control cortical dendrite arborization by regulating the activity of a FAK/PKC/MARCKS signaling pathway, Neuron, 74, 269, 10.1016/j.neuron.2012.01.028 Gorski, 2002, Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage, J. Neurosci., 22, 6309, 10.1523/JNEUROSCI.22-15-06309.2002 Han, 2010, Proteomics analysis reveals overlapping functions of clustered protocadherins, Mol. Cell. Proteomics, 9, 71, 10.1074/mcp.M900343-MCP200 Holtmaat, 2005, Transient and persistent dendritic spines in the neocortex in vivo, Neuron, 45, 279, 10.1016/j.neuron.2005.01.003 Ichtchenko, 1995, Neuroligin 1: A splice site-specific ligand for beta-neurexins, Cell, 81, 435, 10.1016/0092-8674(95)90396-8 Ichtchenko, 1996, Structures, alternative splicing, and neurexin binding of multiple neuroligins, J. Biol. Chem., 271, 2676, 10.1074/jbc.271.5.2676 Jiang, 2016, Conditional ablation of neuroligin-1 in CA1 pyramidal neurons blocks LTP by a cell-autonomous NMDA receptor-independent mechanism, Mol. Psychiatry, 22, 375, 10.1038/mp.2016.80 Kaneko, 2006, Allelic gene regulation of Pcdh-alpha and Pcdh-gamma clusters involving both monoallelic and biallelic expression in single Purkinje cells, J. Biol. Chem., 281, 30551, 10.1074/jbc.M605677200 Keeler, 2015, Protocadherins branch out: Multiple roles in dendrite development, Cell Adh Migr., 9, 214, 10.1080/19336918.2014.1000069 Keeler, 2015, Protein kinase C phosphorylation of a γ-protocadherin C-terminal lipid binding domain regulates focal adhesion kinase inhibition and dendrite arborization, J. Biol. Chem., 290, 20674, 10.1074/jbc.M115.642306 Knott, 2006, Spine growth precedes synapse formation in the adult neocortex in vivo, Nat. Neurosci., 9, 1117, 10.1038/nn1747 Ko, 2009, Neuroligin-1 performs neurexin-dependent and neurexin-independent functions in synapse validation, EMBO J., 28, 3244, 10.1038/emboj.2009.249 Kostadinov, 2015, Protocadherin-dependent dendritic self-avoidance regulates neural connectivity and circuit function, eLife, 10.7554/eLife.08964 Kwon, 2012, Neuroligin-1-dependent competition regulates cortical synaptogenesis and synapse number, Nat. Neurosci., 15, 1667, 10.1038/nn.3256 Ledderose, 2013, Maturation of postnatally generated olfactory bulb granule cells depends on functional γ-protocadherin expression, Sci. Rep., 3, 1514, 10.1038/srep01514 Lefebvre, 2012, Protocadherins mediate dendritic self-avoidance in the mammalian nervous system, Nature, 488, 517, 10.1038/nature11305 Lobas, 2012, Molecular heterogeneity in the choroid plexus epithelium: The 22-member γ-protocadherin family is differentially expressed, apically localized, and implicated in CSF regulation, J. Neurochem., 120, 913 Mah, 2016, The clustered protocadherins, 195 Mah, 2016, The γ-Protocadherin-C3 isoform inhibits canonical Wnt signalling by binding to and stabilizing Axin1 at the membrane, Sci. Rep., 6, 31665, 10.1038/srep31665 Matsuzaki, 2004, Structural basis of long-term potentiation in single dendritic spines, Nature, 429, 761, 10.1038/nature02617 Molumby, 2016, Homophilic protocadherin cell-cell interactions promote dendrite complexity, Cell Rep., 15, 1037, 10.1016/j.celrep.2016.03.093 Petrak, 2005, Synaptogenesis on mature hippocampal dendrites occurs via filopodia and immature spines during blocked synaptic transmission, J. Comp. Neurol., 484, 183, 10.1002/cne.20468 Pettem, 2013, Interaction between autism-linked MDGAs and neuroligins suppresses inhibitory synapse development, J. Cell Biol., 200, 321, 10.1083/jcb.201206028 Phillips, 2003, Gamma-protocadherins are targeted to subsets of synapses and intracellular organelles in neurons, J. Neurosci., 23, 5096, 10.1523/JNEUROSCI.23-12-05096.2003 Prasad, 2008, A differential developmental pattern of spinal interneuron apoptosis during synaptogenesis: Insights from genetic analyses of the protocadherin-gamma gene cluster, Development, 135, 4153, 10.1242/dev.026807 Radley, 2008, Repeated stress alters dendritic spine morphology in the rat medial prefrontal cortex, J. Comp. Neurol., 507, 1141, 10.1002/cne.21588 Radley, 2013, Chronic stress-induced alterations of dendritic spine subtypes predict functional decrements in an hypothalamo-pituitary-adrenal-inhibitory prefrontal circuit, J. Neurosci., 33, 14379, 10.1523/JNEUROSCI.0287-13.2013 Rodriguez, 2008, Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images, PLoS ONE, 3, e1997, 10.1371/journal.pone.0001997 Rubinstein, 2015, Molecular logic of neuronal self-recognition through protocadherin domain interactions, Cell, 163, 629, 10.1016/j.cell.2015.09.026 Scheiffele, 2000, Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons, Cell, 101, 657, 10.1016/S0092-8674(00)80877-6 Schreiner, 2010, Combinatorial homophilic interaction between gamma-protocadherin multimers greatly expands the molecular diversity of cell adhesion, Proc. Natl. Acad. Sci. USA, 107, 14893, 10.1073/pnas.1004526107 Song, 1999, Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses, Proc. Natl. Acad. Sci. USA, 96, 1100, 10.1073/pnas.96.3.1100 Südhof, 2008, Neuroligins and neurexins link synaptic function to cognitive disease, Nature, 455, 903, 10.1038/nature07456 Suo, 2012, Protocadherin clusters and cell adhesion kinase regulate dendrite complexity through Rho GTPase, J. Mol. Cell Biol., 4, 362, 10.1093/jmcb/mjs034 Thu, 2014, Single-cell identity generated by combinatorial homophilic interactions between α, β, and γ protocadherins, Cell, 158, 1045, 10.1016/j.cell.2014.07.012 Varoqueaux, 2006, Neuroligins determine synapse maturation and function, Neuron, 51, 741, 10.1016/j.neuron.2006.09.003 Vaughn, 1989, Fine structure of synaptogenesis in the vertebrate central nervous system, Synapse, 3, 255, 10.1002/syn.890030312 Wang, 2002, Gamma protocadherins are required for survival of spinal interneurons, Neuron, 36, 843, 10.1016/S0896-6273(02)01090-5 Weiner, 2005, Gamma protocadherins are required for synaptic development in the spinal cord, Proc. Natl. Acad. Sci. USA, 102, 8, 10.1073/pnas.0407931101 Woo, 2013, The adhesion protein IgSF9b is coupled to neuroligin 2 via S-SCAM to promote inhibitory synapse development, J. Cell Biol., 201, 929, 10.1083/jcb.201209132 Wu, 1999, A striking organization of a large family of human neural cadherin-like cell adhesion genes, Cell, 97, 779, 10.1016/S0092-8674(00)80789-8 Yagi, 2012, Molecular codes for neuronal individuality and cell assembly in the brain, Front. Mol. Neurosci., 5, 45, 10.3389/fnmol.2012.00045