Splicing-Dependent Trans-synaptic SALM3–LAR-RPTP Interactions Regulate Excitatory Synapse Development and Locomotion

Ackley, 2005, The two isoforms of the Caenorhabditis elegans leukocyte-common antigen related receptor tyrosine phosphatase PTP-3 function independently in axon guidance and synapse formation, J. Neurosci., 25, 7517, 10.1523/JNEUROSCI.2010-05.2005 Biederer, 2008, Signaling by synaptogenic molecules, Curr. Opin. Neurobiol., 18, 261, 10.1016/j.conb.2008.07.014 Blundell, 2010, Neuroligin-1 deletion results in impaired spatial memory and increased repetitive behavior, J. Neurosci., 30, 2115, 10.1523/JNEUROSCI.4517-09.2010 Dalva, 2007, Cell adhesion molecules: signalling functions at the synapse, Nat. Rev. Neurosci., 8, 206, 10.1038/nrn2075 de Bruijn, 2010, Severe progressive autism associated with two de novo changes: A 2.6-Mb 2q31.1 deletion and a balanced t(14;21)(q21.1;p11.2) translocation with long-range epigenetic silencing of LRFN5 expression, Mol. Syndromol., 1, 46, 10.1159/000280290 de Wit, 2014, Control of neural circuit formation by leucine-rich repeat proteins, Trends Neurosci., 37, 539, 10.1016/j.tins.2014.07.004 de Wit, 2011, Role of leucine-rich repeat proteins in the development and function of neural circuits, Annu. Rev. Cell Dev. Biol., 27, 697, 10.1146/annurev-cellbio-092910-154111 Deacon, 2006, T-maze alternation in the rodent, Nat. Protoc., 1, 7, 10.1038/nprot.2006.2 Dix, 1999, Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition, Behav. Brain Res., 99, 191, 10.1016/S0166-4328(98)00079-5 Dunah, 2005, LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses, Nat. Neurosci., 8, 458, 10.1038/nn1416 Elia, 2010, Rare structural variants found in attention-deficit hyperactivity disorder are preferentially associated with neurodevelopmental genes, Mol. Psychiatry, 15, 637, 10.1038/mp.2009.57 Ennaceur, 1988, A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data, Behav. Brain Res., 31, 47, 10.1016/0166-4328(88)90157-X Gambino, 2009, IL1RAPL1 controls inhibitory networks during cerebellar development in mice, Eur. J. Neurosci., 30, 1476, 10.1111/j.1460-9568.2009.06975.x Han, 2010, Regulation of dendritic spines, spatial memory, and embryonic development by the TANC family of PSD-95-interacting proteins, J. Neurosci., 30, 15102, 10.1523/JNEUROSCI.3128-10.2010 Hoogenraad, 2007, Liprinalpha1 degradation by calcium/calmodulin-dependent protein kinase II regulates LAR receptor tyrosine phosphatase distribution and dendrite development, Dev. Cell, 12, 587, 10.1016/j.devcel.2007.02.006 Houbaert, 2013, Target-specific vulnerability of excitatory synapses leads to deficits in associative memory in a model of intellectual disorder, J. Neurosci., 33, 13805, 10.1523/JNEUROSCI.1457-13.2013 Jedlicka, 2015, Neuroligin-1 regulates excitatory synaptic transmission, LTP and EPSP-spike coupling in the dentate gyrus in vivo, Brain Struct. Funct., 220, 47, 10.1007/s00429-013-0636-1 Ji, 2007, Hippocampal involvement in contextual modulation of fear extinction, Hippocampus, 17, 749, 10.1002/hipo.20331 Johnson, 2003, Receptor protein tyrosine phosphatases in nervous system development, Physiol. Rev., 83, 1, 10.1152/physrev.00016.2002 Jung, 2010, Input-specific synaptic plasticity in the amygdala is regulated by neuroligin-1 via postsynaptic NMDA receptors, Proc. Natl. Acad. Sci. USA, 107, 4710, 10.1073/pnas.1001084107 Kim, 2008, Neuroligin-1 is required for normal expression of LTP and associative fear memory in the amygdala of adult animals, Proc. Natl. Acad. Sci. USA, 105, 9087, 10.1073/pnas.0803448105 Ko, 2006, SALM synaptic cell adhesion-like molecules regulate the differentiation of excitatory synapses, Neuron, 50, 233, 10.1016/j.neuron.2006.04.005 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 Kwon, 2010, Trans-synaptic adhesions between netrin-G ligand-3 (NGL-3) and receptor tyrosine phosphatases LAR, protein-tyrosine phosphatase delta (PTPdelta), and PTPsigma via specific domains regulate excitatory synapse formation, J. Biol. Chem., 285, 13966, 10.1074/jbc.M109.061127 Lee, 2014, Long-term depression-inducing stimuli promote cleavage of the synaptic adhesion molecule NGL-3 through NMDA receptors, matrix metalloproteinases and presenilin/γ-secretase, Philos. Trans. R. Soc. Lond. B Biol. Sci., 369, 20130158, 10.1098/rstb.2013.0158 Lisman, 2011, A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP, Trends Neurosci., 34, 536, 10.1016/j.tins.2011.07.006 Mah, 2010, Selected SALM (synaptic adhesion-like molecule) family proteins regulate synapse formation, J. Neurosci., 30, 5559, 10.1523/JNEUROSCI.4839-09.2010 Malhotra, 2011, High frequencies of de novo CNVs in bipolar disorder and schizophrenia, Neuron, 72, 951, 10.1016/j.neuron.2011.11.007 Mander, 2005, Knock-down of LAR protein tyrosine phosphatase induces insulin resistance, FEBS Lett., 579, 3024, 10.1016/j.febslet.2005.04.057 Mignogna, 2010, Brain distribution of genes related to changes in locomotor activity, Physiol. Behav., 99, 618, 10.1016/j.physbeh.2010.01.026 Mikhail, 2011, Clinically relevant single gene or intragenic deletions encompassing critical neurodevelopmental genes in patients with developmental delay, mental retardation, and/or autism spectrum disorders, Am. J. Med. Genet. A., 155A, 2386, 10.1002/ajmg.a.34177 Missler, 2012, Synaptic cell adhesion, Cold Spring Harb. Perspect. Biol., 4, a005694, 10.1101/cshperspect.a005694 Morimura, 2006, Comparative analysis of structure, expression and PSD95-binding capacity of Lrfn, a novel family of neuronal transmembrane proteins, Gene, 380, 72, 10.1016/j.gene.2006.05.014 Morris, 1984, Developments of a water-maze procedure for studying spatial learning in the rat, J. Neurosci. Methods, 11, 47, 10.1016/0165-0270(84)90007-4 Nam, 2011, The SALM/Lrfn family of leucine-rich repeat-containing cell adhesion molecules, Semin. Cell Dev. Biol., 22, 492, 10.1016/j.semcdb.2011.06.005 Pavlowsky, 2010, A postsynaptic signaling pathway that may account for the cognitive defect due to IL1RAPL1 mutation, Curr. Biol., 20, 103, 10.1016/j.cub.2009.12.030 Phillips, 1992, Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning, Behav. Neurosci., 106, 274, 10.1037/0735-7044.106.2.274 Pinto, 2010, Functional impact of global rare copy number variation in autism spectrum disorders, Nature, 466, 368, 10.1038/nature09146 2014, Biological insights from 108 schizophrenia-associated genetic loci, Nature, 511, 421, 10.1038/nature13595 Schormair, 2008, PTPRD (protein tyrosine phosphatase receptor type delta) is associated with restless legs syndrome, Nat. Genet., 40, 946, 10.1038/ng.190 Seabold, 2008, The SALM family of adhesion-like molecules forms heteromeric and homomeric complexes, J. Biol. Chem., 283, 8395, 10.1074/jbc.M709456200 Shen, 2010, Genetics and cell biology of building specific synaptic connectivity, Annu. Rev. Neurosci., 33, 473, 10.1146/annurev.neuro.051508.135302 Shipman, 2012, A subtype-specific function for the extracellular domain of neuroligin 1 in hippocampal LTP, Neuron, 76, 309, 10.1016/j.neuron.2012.07.024 Shmelkov, 2010, Slitrk5 deficiency impairs corticostriatal circuitry and leads to obsessive-compulsive-like behaviors in mice, Nat. Med., 16, 598, 10.1038/nm.2125 Siddiqui, 2011, Synaptic organizing complexes, Curr. Opin. Neurobiol., 21, 132, 10.1016/j.conb.2010.08.016 Smith, 2009, A central nervous system-restricted isoform of the interleukin-1 receptor accessory protein modulates neuronal responses to interleukin-1, Immunity, 30, 817, 10.1016/j.immuni.2009.03.020 Soler-Llavina, 2013, Leucine-rich repeat transmembrane proteins are essential for maintenance of long-term potentiation, Neuron, 79, 439, 10.1016/j.neuron.2013.06.007 Song, 2013, Presynaptic proteoglycans: sweet organizers of synapse development, Neuron, 79, 609, 10.1016/j.neuron.2013.07.048 Stryker, 2007, LAR, liprin alpha and the regulation of active zone morphogenesis, J. Cell Sci., 120, 3723, 10.1242/jcs.03491 Südhof, 2008, Neuroligins and neurexins link synaptic function to cognitive disease, Nature, 455, 903, 10.1038/nature07456 Takahashi, 2013, Protein tyrosine phosphatases PTPδ, PTPσ, and LAR: presynaptic hubs for synapse organization, Trends Neurosci., 36, 522, 10.1016/j.tins.2013.06.002 Takahashi, 2011, Postsynaptic TrkC and presynaptic PTPσ function as a bidirectional excitatory synaptic organizing complex, Neuron, 69, 287, 10.1016/j.neuron.2010.12.024 Takahashi, 2012, Selective control of inhibitory synapse development by Slitrk3-PTPδ trans-synaptic interaction, Nat. Neurosci., 15, 389, 10.1038/nn.3040 Tessarollo, 1997, Targeted deletion of all isoforms of the trkC gene suggests the use of alternate receptors by its ligand neurotrophin-3 in neuronal development and implicates trkC in normal cardiogenesis, Proc. Natl. Acad. Sci. USA, 94, 14776, 10.1073/pnas.94.26.14776 Um, 2013, LAR-RPTPs: synaptic adhesion molecules that shape synapse development, Trends Cell Biol., 23, 465, 10.1016/j.tcb.2013.07.004 Um, 2014, Structural basis for LAR-RPTP/Slitrk complex-mediated synaptic adhesion, Nat. Commun., 5, 5423, 10.1038/ncomms6423 Valnegri, 2011, The X-linked intellectual disability protein IL1RAPL1 regulates excitatory synapse formation by binding PTPδ and RhoGAP2, Hum. Mol. Genet., 20, 4797, 10.1093/hmg/ddr418 Valnegri, 2012, Synaptic dysfunction and intellectual disability, Adv. Exp. Med. Biol., 970, 433, 10.1007/978-3-7091-0932-8_19 Viggiano, 2008, The hyperactive syndrome: metanalysis of genetic alterations, pharmacological treatments and brain lesions which increase locomotor activity, Behav. Brain Res., 194, 1, 10.1016/j.bbr.2008.06.033 Voineagu, 2013, Current progress and challenges in the search for autism biomarkers, Dis. Markers, 35, 55, 10.1155/2013/476276 Wang, 2006, A novel family of adhesion-like molecules that interacts with the NMDA receptor, J. Neurosci., 26, 2174, 10.1523/JNEUROSCI.3799-05.2006 Wang, 2009, Common genetic variants on 5p14.1 associate with autism spectrum disorders, Nature, 459, 528, 10.1038/nature07999 Woo, 2009, Trans-synaptic adhesion between NGL-3 and LAR regulates the formation of excitatory synapses, Nat. Neurosci., 12, 428, 10.1038/nn.2279 Xu, 2009, Elucidating the genetic architecture of familial schizophrenia using rare copy number variant and linkage scans, Proc. Natl. Acad. Sci. USA, 106, 16746, 10.1073/pnas.0908584106 Yamagata, 2003, Synaptic adhesion molecules, Curr. Opin. Cell Biol., 15, 621, 10.1016/S0955-0674(03)00107-8 Yamagata, 2015, Structure of Slitrk2-PTPδ complex reveals mechanisms for splicing-dependent trans-synaptic adhesion, Sci. Rep., 5, 9686, 10.1038/srep09686 Yamagata, 2015, Mechanisms of splicing-dependent trans-synaptic adhesion by PTPδ-IL1RAPL1/IL-1RAcP for synaptic differentiation, Nat. Commun., 6, 6926, 10.1038/ncomms7926 Yang, 2011, Family-based and population-based association studies validate PTPRD as a risk factor for restless legs syndrome, Mov. Disord., 26, 516, 10.1002/mds.23459 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 Yoshida, 2012, Interleukin-1 receptor accessory protein organizes neuronal synaptogenesis as a cell adhesion molecule, J. Neurosci., 32, 2588, 10.1523/JNEUROSCI.4637-11.2012 Yuzaki, 2011, Cbln1 and its family proteins in synapse formation and maintenance, Curr. Opin. Neurobiol., 21, 215, 10.1016/j.conb.2011.01.010