Synapse organizers as molecular codes for synaptic plasticity

Trends in Neurosciences - Tập 46 - Trang 971-985 - 2023
Steven A. Connor1, Tabrez J. Siddiqui2,3,4,5
1Department of Biology, York University, Toronto, ON, M3J 1P3, Canada
2PrairieNeuro Research Centre, Kleysen Institute for Advanced Medicine, Health Sciences Centre, Winnipeg, MB R3E 0Z3, Canada
3Department of Physiology and Pathophysiology, University of Manitoba, Winnipeg, MB R3E 0J9, Canada
4The Children’s Hospital Research Institute of Manitoba, Winnipeg, MB R3E 3P4, Canada
5Program in Biomedical Engineering, University of Manitoba, Winnipeg, MB Canada

Tài liệu tham khảo

Sudhof, 2018, Towards an understanding of synapse formation, Neuron, 100, 276, 10.1016/j.neuron.2018.09.040

Gomez, 2021, Neurexins: molecular codes for shaping neuronal synapses, Nat. Rev. Neurosci., 22, 137, 10.1038/s41583-020-00415-7

Sudhof, 2017, Synaptic neurexin complexes: a molecular code for the logic of neural circuits, Cell, 171, 745, 10.1016/j.cell.2017.10.024

Craig, 2007, Neurexin-neuroligin signaling in synapse development, Curr. Opin. Neurobiol., 17, 43, 10.1016/j.conb.2007.01.011

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

Bemben, 2015, The cellular and molecular landscape of neuroligins, Trends Neurosci., 38, 496, 10.1016/j.tins.2015.06.004

Roppongi, 2017, Role of LRRTMs in synapse development and plasticity, Neurosci. Res., 116, 18, 10.1016/j.neures.2016.10.003

Uemura, 2010, Trans-synaptic interaction of GluRδ2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum, Cell, 141, 1068, 10.1016/j.cell.2010.04.035

Seigneur, 2018, Genetic ablation of all cerebellins reveals synapse organizer functions in multiple regions throughout the brain, J. Neurosci., 38, 4774, 10.1523/JNEUROSCI.0360-18.2018

Kakegawa, 2009, The N-terminal domain of GluD2 (GluRδ2) recruits presynaptic terminals and regulates synaptogenesis in the cerebellum in vivo, J. Neurosci., 29, 5738, 10.1523/JNEUROSCI.6013-08.2009

Matsuda, 2010, Cbln1 is a ligand for an orphan glutamate receptor delta2, a bidirectional synapse organizer, Science, 328, 363, 10.1126/science.1185152

Pettem, 2013, The specific alpha-neurexin interactor calsyntenin-3 promotes excitatory and inhibitory synapse development, Neuron, 80, 113, 10.1016/j.neuron.2013.07.016

Connor, 2019, Pumping the brakes: suppression of synapse development by MDGA-neuroligin interactions, Curr. Opin. Neurobiol., 57, 71, 10.1016/j.conb.2019.01.002

Pettem, 2013, Interaction between autism-linked MDGAs and neuroligins suppresses inhibitory synapse development, J. Cell Biol., 200, 321, 10.1083/jcb.201206028

Lie, 2016, SALM4 suppresses excitatory synapse development by cis-inhibiting trans-synaptic SALM3-LAR adhesion, Nat. Commun., 7, 12328, 10.1038/ncomms12328

Mah, 2010, Selected SALM (synaptic adhesion-like molecule) family proteins regulate synapse formation, J. Neurosci., 30, 5559, 10.1523/JNEUROSCI.4839-09.2010

Steffen, 2021, The gamma-protocadherins interact physically and functionally with neuroligin-2 to negatively regulate inhibitory synapse density and are required for normal social interaction, Mol. Neurobiol., 58, 2574, 10.1007/s12035-020-02263-z

Molumby, 2017, γ-Protocadherins interact with neuroligin-1 and negatively regulate dendritic spine morphogenesis, Cell Rep., 18, 2702, 10.1016/j.celrep.2017.02.060

Lin, 2023, Neurexin-2: an inhibitory neurexin that restricts excitatory synapse formation in the hippocampus, Sci. Adv., 9, 10.1126/sciadv.add8856

Vieira, 2021, The role of NMDA receptor and neuroligin rare variants in synaptic dysfunction underlying neurodevelopmental disorders, Curr. Opin. Neurobiol., 69, 93, 10.1016/j.conb.2021.03.001

Sudhof, 2008, Neuroligins and neurexins link synaptic function to cognitive disease, Nature, 455, 903, 10.1038/nature07456

Hu, 2019, Genetic insights and neurobiological implications from NRXN1 in neuropsychiatric disorders, Mol. Psychiatry, 24, 1400, 10.1038/s41380-019-0438-9

Bourgeron, 2015, From the genetic architecture to synaptic plasticity in autism spectrum disorder, Nat. Rev. Neurosci., 16, 551, 10.1038/nrn3992

Malenka, 2004, LTP and LTD: an embarrassment of riches, Neuron, 44, 5, 10.1016/j.neuron.2004.09.012

Bliss, 1993, A synaptic model of memory: long-term potentiation in the hippocampus, Nature, 361, 31, 10.1038/361031a0

Pinar, 2017, Revisiting the flip side: long-term depression of synaptic efficacy in the hippocampus, Neurosci. Biobehav. Rev., 80, 394, 10.1016/j.neubiorev.2017.06.001

Collingridge, 2010, Long-term depression in the CNS, Nat. Rev. Neurosci., 11, 459, 10.1038/nrn2867

Howard, 2010, The role of SAP97 in synaptic glutamate receptor dynamics, Proc. Natl. Acad. Sci. U. S. A., 107, 3805, 10.1073/pnas.0914422107

Nicoll, 2017, A brief history of long-term potentiation, Neuron, 93, 281, 10.1016/j.neuron.2016.12.015

Getz, 2022, High-resolution imaging and manipulation of endogenous AMPA receptor surface mobility during synaptic plasticity and learning, Sci. Adv., 8, 10.1126/sciadv.abm5298

Whitlock, 2006, Learning induces long-term potentiation in the hippocampus, Science, 313, 1093, 10.1126/science.1128134

Lisman, 2018, Memory formation depends on both synapse-specific modifications of synaptic strength and cell-specific increases in excitability, Nat. Neurosci., 21, 309, 10.1038/s41593-018-0076-6

Liakath-Ali, 2022, Transsynaptic cerebellin 4-neogenin 1 signaling mediates LTP in the mouse dentate gyrus, Proc. Natl. Acad. Sci. U. S. A., 119, 10.1073/pnas.2123421119

Sudhof, 2023, Cerebellin-neurexin complexes instructing synapse properties, Curr. Opin. Neurobiol., 18

Kakegawa, 2011, D-serine regulates cerebellar LTD and motor coordination through the delta2 glutamate receptor, Nat. Neurosci., 14, 10.1038/nn.2791

Uetani, 2000, Impaired learning with enhanced hippocampal long-term potentiation in PTPdelta-deficient mice, EMBO J., 19, 2775, 10.1093/emboj/19.12.2775

Lee, 2014, Long-term depression-inducing stimuli promote cleavage of the synaptic adhesion molecule NGL-3 through NMDA receptors, matrix metalloproteinases and presenilin/gamma-secretase, Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci., 369, 10.1098/rstb.2013.0158

Regan, 2021, A novel role for the ADHD risk gene latrophilin-3 in learning and memory in Lphn3 knockout rats, Neurobiol. Dis., 158, 10.1016/j.nbd.2021.105456

Ribic, 2019, Synapse-selective control of cortical maturation and plasticity by parvalbumin-autonomous action of SynCAM 1, Cell Rep., 26, 381, 10.1016/j.celrep.2018.12.069

Robbins, 2010, SynCAM 1 adhesion dynamically regulates synapse number and impacts plasticity and learning, Neuron, 68, 894, 10.1016/j.neuron.2010.11.003

Morimura, 2017, Autism-like behaviours and enhanced memory formation and synaptic plasticity in Lrfn2/SALM1-deficient mice, Nat. Commun., 8, 15800, 10.1038/ncomms15800

Li, 2015, Splicing-dependent trans-synaptic SALM3-LAR-RPTP interactions regulate excitatory synapse development and locomotion, Cell Rep., 12, 1618, 10.1016/j.celrep.2015.08.002

Kakegawa, 2015, Anterograde C1ql1 signaling is required in order to determine and maintain a single-winner climbing fiber in the mouse cerebellum, Neuron, 85, 316, 10.1016/j.neuron.2014.12.020

Basu, 2017, Heterophilic type II cadherins are required for high-magnitude synaptic potentiation in the hippocampus, Neuron, 96, 160, 10.1016/j.neuron.2017.09.009

Bozdagi, 2000, Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation, Neuron, 28, 245, 10.1016/S0896-6273(00)00100-8

Tang, 1998, A role for the cadherin family of cell adhesion molecules in hippocampal long-term potentiation, Neuron, 20, 1165, 10.1016/S0896-6273(00)80497-3

Ushkaryov, 1992, Neurexins: synaptic cell surface proteins related to the α-latrotoxin receptor and laminin, Science, 257, 50, 10.1126/science.1621094

Treutlein, 2014, Cartography of neurexin alternative splicing mapped by single-molecule long-read mRNA sequencing, Proc. Natl. Acad. Sci. U. S. A., 111, E1291, 10.1073/pnas.1403244111

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

Traunmuller, 2016, Control of neuronal synapse specification by a highly dedicated alternative splicing program, Science, 352, 982, 10.1126/science.aaf2397

Schreiner, 2014, Targeted combinatorial alternative splicing generates brain region-specific repertoires of neurexins, Neuron, 84, 386, 10.1016/j.neuron.2014.09.011

Chen, 2017, Conditional deletion of all neurexins defines diversity of essential synaptic organizer functions for neurexins, Neuron, 94, 611, 10.1016/j.neuron.2017.04.011

Missler, 2003, α-neurexins couple Ca2+ channels to synaptic vesicle exocytosis, Nature, 423, 939, 10.1038/nature01755

Anderson, 2015, β-Neurexins control neural circuits by regulating synaptic endocannabinoid signaling, Cell, 162, 593, 10.1016/j.cell.2015.06.056

Ko, 2009, LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation, Neuron, 64, 791, 10.1016/j.neuron.2009.12.012

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

Boucard, 2012, High affinity neurexin binding to cell adhesion G-protein-coupled receptor CIRL1/latrophilin-1 produces an intercellular adhesion complex, J. Biol. Chem., 287, 9399, 10.1074/jbc.M111.318659

Aoto, 2013, Presynaptic neurexin-3 alternative splicing trans-synaptically controls postsynaptic AMPA receptor trafficking, Cell, 154, 75, 10.1016/j.cell.2013.05.060

Roppongi, 2020, LRRTMs organize synapses through differential engagement of neurexin and PTPsigma, Neuron, 106, 108, 10.1016/j.neuron.2020.01.003

Zhang, 2018, Heparan sulfate organizes neuronal synapses through neurexin partnerships, Cell, 174, 1450, 10.1016/j.cell.2018.07.002

Poulopoulos, 2012, Homodimerization and isoform-specific heterodimerization of neuroligins, Biochem. J., 446, 321, 10.1042/BJ20120808

Graf, 2004, Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins, Cell, 119, 1013, 10.1016/j.cell.2004.11.035

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

Budreck, 2007, Neuroligin-3 is a neuronal adhesion protein at GABAergic and glutamatergic synapses, Eur. J. Neurosci., 26, 1738, 10.1111/j.1460-9568.2007.05842.x

Dahlhaus, 2010, Overexpression of the cell adhesion protein neuroligin-1 induces learning deficits and impairs synaptic plasticity by altering the ratio of excitation to inhibition in the hippocampus, Hippocampus, 20, 305, 10.1002/hipo.20630

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. U. S. A., 105, 9087, 10.1073/pnas.0803448105

Jung, 2010, Input-specific synaptic plasticity in the amygdala is regulated by neuroligin-1 via postsynaptic NMDA receptors, Proc. Natl. Acad. Sci. U. S. A., 107, 4710, 10.1073/pnas.1001084107

Blundell, 2010, Neuroligin-1 deletion results in impaired spatial memory and increased repetitive behavior, J. Neurosci., 30, 2115, 10.1523/JNEUROSCI.4517-09.2010

Shipman, 2012, A subtype-specific function for the extracellular domain of neuroligin 1 in hippocampal LTP, Neuron, 76, 10.1016/j.neuron.2012.07.024

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

Jedlicka, 2018, Synaptic plasticity and excitation-inhibition balance in the dentate gyrus: insights from in vivo recordings in neuroligin-1, neuroligin-2, and collybistin knockouts, Neural Plast., 2018, 10.1155/2018/6015753

Jiang, 2017, 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

Bemben, 2014, CaMKII phosphorylation of neuroligin-1 regulates excitatory synapses, Nat. Neurosci., 17, 56, 10.1038/nn.3601

Letellier, 2018, A unique intracellular tyrosine in neuroligin-1 regulates AMPA receptor recruitment during synapse differentiation and potentiation, Nat. Commun., 9, 3979, 10.1038/s41467-018-06220-2

Dang, 2018, Regulation of hippocampal long term depression by Neuroligin 1, Neuropharmacology, 143, 205, 10.1016/j.neuropharm.2018.09.035

Dolen, 2007, Correction of fragile X syndrome in mice, Neuron, 56, 955, 10.1016/j.neuron.2007.12.001

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

Etherton, 2011, Autism-linked neuroligin-3 R451C mutation differentially alters hippocampal and cortical synaptic function, Proc. Natl. Acad. Sci. U. S. A., 108, 13764, 10.1073/pnas.1111093108

Martella, 2018, The neurobiological bases of autism spectrum disorders: the R451C-neuroligin 3 mutation hampers the expression of long-term synaptic depression in the dorsal striatum, Eur. J. Neurosci., 47, 701, 10.1111/ejn.13705

Wu, 2019, Neuroligin-1 signaling controls LTP and NMDA receptors by distinct molecular pathways, Neuron, 102, 621, 10.1016/j.neuron.2019.02.013

Laurén, 2003, A novel gene family encoding leucine-rich repeat transmembrane proteins differentially expressed in the nervous system, Genomics, 81, 411, 10.1016/S0888-7543(03)00030-2

de Wit, 2009, LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation, Neuron, 64, 799, 10.1016/j.neuron.2009.12.019

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

Soler-Llavina, 2011, The neurexin ligands, neuroligins and leucine-rich repeat transmembrane proteins, perform convergent and divergent synaptic functions in vivo, Proc. Natl. Acad. Sci. U. S. A., 108, 16502, 10.1073/pnas.1114028108

Dhume, 2022, Distinct but overlapping roles of LRRTM1 and LRRTM2 in developing and mature hippocampal circuits, eLife, 11, 10.7554/eLife.64742

Bhouri, 2018, Deletion of LRRTM1 and LRRTM2 in adult mice impairs basal AMPA receptor transmission and LTP in hippocampal CA1 pyramidal neurons, Proc. Natl. Acad. Sci. U. S. A., 115, E5382, 10.1073/pnas.1803280115

Schwenk, 2012, High-resolution proteomics unravel architecture and molecular diversity of native AMPA receptor complexes, Neuron, 74, 10.1016/j.neuron.2012.03.034

Siddiqui, 2013, An LRRTM4-HSPG complex mediates excitatory synapse development on dentate gyrus granule cells, Neuron, 79, 680, 10.1016/j.neuron.2013.06.029

Karimi, 2021, Schizophrenia-associated LRRTM1 regulates cognitive behavior through controlling synaptic function in the mediodorsal thalamus, Mol. Psychiatry, 26, 6912, 10.1038/s41380-021-01146-6

Um, 2016, LRRTM3 regulates excitatory synapse development through alternative splicing and neurexin binding, Cell Rep., 14, 808, 10.1016/j.celrep.2015.12.081

Ramsey, 2021, Subsynaptic positioning of AMPARs by LRRTM2 controls synaptic strength, Sci. Adv., 7, 10.1126/sciadv.abf3126

Nozawa, 2022, In vivo nanoscopic landscape of neurexin ligands underlying anterograde synapse specification, Neuron, 110, 3168, 10.1016/j.neuron.2022.07.027

Linhoff, 2009, An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers, Neuron, 61, 734, 10.1016/j.neuron.2009.01.017

Takashima, 2011, Impaired cognitive function and altered hippocampal synapse morphology in mice lacking Lrrtm1, a gene associated with schizophrenia, PLoS One, 6, 10.1371/journal.pone.0022716

Schroeder, 2018, A modular organization of LRR protein-mediated synaptic adhesion defines synapse identity, Neuron, 99, 329, 10.1016/j.neuron.2018.06.026

Elegheert, 2017, Structural mechanism for modulation of synaptic neuroligin-neurexin signaling by MDGA proteins, Neuron, 95, 896, 10.1016/j.neuron.2017.07.040

Gangwar, 2017, Molecular mechanism of MDGA1: regulation of neuroligin 2:neurexin trans-synaptic bridges, Neuron, 94, 1132, 10.1016/j.neuron.2017.06.009

Kim, 2017, Structural insights into modulation of neurexin-neuroligin trans-synaptic adhesion by MDGA1/neuroligin-2 complex, Neuron, 94, 1121, 10.1016/j.neuron.2017.05.034

Litwack, 2004, Identification and characterization of two novel brain-derived immunoglobulin superfamily members with a unique structural organization, Mol. Cell. Neurosci., 25, 263, 10.1016/j.mcn.2003.10.016

Connor, 2016, Altered cortical dynamics and cognitive function upon haploinsufficiency of the autism-linked excitatory synaptic suppressor MDGA2, Neuron, 91, 1052, 10.1016/j.neuron.2016.08.016

Connor, 2017, Loss of synapse repressor MDGA1 enhances perisomatic inhibition, confers resistance to network excitation, and impairs cognitive function, Cell Rep., 21, 3637, 10.1016/j.celrep.2017.11.109

Toledo, 2022, MDGAs are fast-diffusing molecules that delay excitatory synapse development by altering neuroligin behavior, eLife, 11, 10.7554/eLife.75233

Loh, 2016, Proteomic analysis of unbounded cellular compartments: synaptic clefts, Cell, 166, 1295, 10.1016/j.cell.2016.07.041

Opazo, 2012, Regulation of AMPA receptor surface diffusion by PSD-95 slots, Curr. Opin. Neurobiol., 22, 453, 10.1016/j.conb.2011.10.010

Bemben, 2023, Contrasting synaptic roles of MDGA1 and MDGA2, bioRxiv

Shipman, 2012, Dimerization of postsynaptic neuroligin drives synaptic assembly via transsynaptic clustering of neurexin, Proc. Natl. Acad. Sci. U. S. A., 109, 19432, 10.1073/pnas.1217633109

Li, 2017, Molecular dissection of neuroligin 2 and Slitrk3 reveals an essential framework for GABAergic synapse development, Neuron, 96, 808, 10.1016/j.neuron.2017.10.003

de Arce, 2023, Concerted roles of LRRTM1 and SynCAM 1 in organizing prefrontal cortex synapses and cognitive functions, Nat. Commun., 14, 459, 10.1038/s41467-023-36042-w

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