The netrin receptor UNC-40/DCC assembles a postsynaptic scaffold and sets the synaptic content of GABA
Animals
Axon Guidance
/ physiology
Caenorhabditis elegans
/ metabolism
Caenorhabditis elegans Proteins
/ metabolism
Cell Adhesion Molecules
/ metabolism
Cell Adhesion Molecules, Neuronal
/ metabolism
Cytoskeletal Proteins
/ metabolism
Helminth Proteins
/ metabolism
Membrane Proteins
/ metabolism
Nerve Tissue Proteins
/ metabolism
Neuromuscular Junction
/ metabolism
Receptors, Cell Surface
/ metabolism
Receptors, GABA-A
/ metabolism
Synapses
/ physiology
Synaptic Transmission
/ physiology
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
29 05 2020
29 05 2020
Historique:
received:
03
10
2019
accepted:
28
04
2020
entrez:
31
5
2020
pubmed:
31
5
2020
medline:
25
8
2020
Statut:
epublish
Résumé
Increasing evidence indicates that guidance molecules used during development for cellular and axonal navigation also play roles in synapse maturation and homeostasis. In C. elegans the netrin receptor UNC-40/DCC controls the growth of dendritic-like muscle cell extensions towards motoneurons and is required to recruit type A GABA receptors (GABA
Identifiants
pubmed: 32471987
doi: 10.1038/s41467-020-16473-5
pii: 10.1038/s41467-020-16473-5
pmc: PMC7260190
doi:
Substances chimiques
Caenorhabditis elegans Proteins
0
Cell Adhesion Molecules
0
Cell Adhesion Molecules, Neuronal
0
Cytoskeletal Proteins
0
Helminth Proteins
0
Lin-2 protein, C elegans
0
MADD-4 protein, C elegans
0
Membrane Proteins
0
Nerve Tissue Proteins
0
Receptors, Cell Surface
0
Receptors, GABA-A
0
UNC-40 protein, C elegans
0
neuroligin 1
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2674Subventions
Organisme : NIH HHS
ID : P40 OD010440
Pays : United States
Références
Horn, K. E. et al. DCC expression by neurons regulates synaptic plasticity in the adult brain. Cell Rep. 3, 173–185 (2013).
pubmed: 23291093
doi: 10.1016/j.celrep.2012.12.005
Kayser, M. S., Nolt, M. J. & Dalva, M. B. EphB receptors couple dendritic filopodia motility to synapse formation. Neuron 59, 56–69 (2008).
pubmed: 18614029
pmcid: 2617787
doi: 10.1016/j.neuron.2008.05.007
Wang, Q. et al. Neuropilin-2/PlexinA3 receptors associate with GluA1 and mediate Sema3F-dependent homeostatic scaling in cortical neurons. Neuron 96, 1084–1098.e7 (2017).
pubmed: 29154130
pmcid: 5726806
doi: 10.1016/j.neuron.2017.10.029
Poon, V. Y., Choi, S. & Park, M. Growth factors in synaptic function. Front. Synaptic Neurosci. 5, 6 (2013).
pubmed: 24065916
pmcid: 3776238
doi: 10.3389/fnsyn.2013.00006
Hedgecock, E. M., Culotti, J. G. & Hall, D. H. The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4, 61–85 (1990).
pubmed: 2310575
doi: 10.1016/0896-6273(90)90444-K
Chisholm, A. D., Hutter, H., Jin, Y. & Wadsworth, W. G. The genetics of axon guidance and axon regeneration in Caenorhabditis elegans. Genetics 204, 849–882 (2016).
pubmed: 28114100
pmcid: 5105865
doi: 10.1534/genetics.115.186262
Kennedy, T. E., Serafini, T., de la Torre, J. R. & Tessier-Lavigne, M. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78, 425–435 (1994).
pubmed: 8062385
doi: 10.1016/0092-8674(94)90421-9
Serafini, T. et al. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78, 409–424 (1994).
pubmed: 8062384
doi: 10.1016/0092-8674(94)90420-0
Keino-Masu, K. et al. Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 87, 175–185 (1996).
pubmed: 8861902
doi: 10.1016/S0092-8674(00)81336-7
Leonardo, E. D. et al. Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 386, 833–838 (1997).
pubmed: 9126742
doi: 10.1038/386833a0
Boyer, N. P. & Gupton, S. L. Revisiting Netrin-1: One Who Guides (Axons). Front. Cell. Neurosci. 12, (2018).
Hong, K. et al. A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 97, 927–941 (1999).
pubmed: 10399920
doi: 10.1016/S0092-8674(00)80804-1
Dominici, C. et al. Floor plate-derived netrin-1 is dispensable for commissural axon guidance. Nature 545, 350–354 (2017).
pubmed: 28445456
pmcid: 5438598
doi: 10.1038/nature22331
Varadarajan, S. G. et al. Netrin1 produced by neural progenitors, not floor plate cells, is required for axon guidance in the spinal cord. Neuron 94, 790–799.e3 (2017).
pubmed: 28434801
pmcid: 5576449
doi: 10.1016/j.neuron.2017.03.007
Yamauchi, K. et al. Netrin-1 derived from the ventricular zone, but not the floor plate, directs hindbrain commissural axons to the ventral midline. Sci. Rep. 7, 1–12 (2017).
doi: 10.1038/s41598-016-0028-x
Gujar, M. R., Sundararajan, L., Stricker, A. & Lundquist, E. A. Control of growth cone polarity, microtubule accumulation, and protrusion by UNC-6/Netrin and its receptors in Caenorhabditis elegans. Genetics 210, 235–255 (2018).
pubmed: 30045855
pmcid: 6116952
doi: 10.1534/genetics.118.301234
Limerick, G. et al. A Statistically-Oriented Asymmetric Localization (SOAL) model for neuronal outgrowth patterning by Caenorhabditis elegans UNC-5 (UNC5) and UNC-40 (DCC) netrin receptors. Genetics 208, 245–272 (2018).
pubmed: 29092889
doi: 10.1534/genetics.117.300460
Glasgow, S. D. et al. Activity-dependent Netrin-1 secretion drives synaptic insertion of GluA1-containing AMPA receptors in the hippocampus. Cell Rep. 25, 168–182.e6 (2018).
pubmed: 30282026
doi: 10.1016/j.celrep.2018.09.028
Wadsworth, W. G., Bhatt, H. & Hedgecock, E. M. Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 16, 35–46 (1996).
pubmed: 8562088
doi: 10.1016/S0896-6273(00)80021-5
Chan, S. S.-Y. et al. UNC-40, a C. elegans Homolog of DCC (Deleted in Colorectal Cancer), is required in motile cells responding to UNC-6 Netrin cues. Cell 87, 187–195 (1996).
pubmed: 8861903
doi: 10.1016/S0092-8674(00)81337-9
Dixon, S. J. & Roy, P. J. Muscle arm development in Caenorhabditis elegans. Development 132, 3079–3092 (2005).
pubmed: 15930100
doi: 10.1242/dev.01883
Seetharaman, A. et al. MADD-4 Is a secreted cue required for midline-oriented guidance in Caenorhabditis elegans. Dev. Cell 21, 669–680 (2011).
pubmed: 22014523
doi: 10.1016/j.devcel.2011.07.020
Alexander, M. et al. An UNC-40 pathway directs postsynaptic membrane extension in Caenorhabditis elegans. Development 136, 911–922 (2009).
pubmed: 19211675
doi: 10.1242/dev.030759
Colón-Ramos, D. A., Margeta, M. A. & Shen, K. Glia promote local synaptogenesis through UNC-6 (Netrin) signaling in C. elegans. Science 318, 103–106 (2007).
pubmed: 17916735
pmcid: 2741089
doi: 10.1126/science.1143762
Stavoe, A. K. H. & Colón-Ramos, D. A. Netrin instructs synaptic vesicle clustering through Rac GTPase, MIG-10, and the actin cytoskeleton. J. Cell Biol. 197, 75–88 (2012).
pubmed: 22451697
pmcid: 3317799
doi: 10.1083/jcb.201110127
Weinberg, P., Berkseth, M., Zarkower, D. & Hobert, O. Sexually dimorphic unc-6/Netrin expression controls sex-specific maintenance of synaptic connectivity. Curr. Biol. 28, 623–629.e3 (2018).
pubmed: 29429615
pmcid: 5820123
doi: 10.1016/j.cub.2018.01.002
Tu, H., Pinan-Lucarré, B., Ji, T., Jospin, M. & Bessereau, J.-L. C. elegans punctin clusters GABAA receptors via neuroligin binding and UNC-40/DCC recruitment. Neuron 86, 1407–1419 (2015).
pubmed: 26028575
doi: 10.1016/j.neuron.2015.05.013
Pinan-Lucarré, B. et al. C. elegans Punctin specifies cholinergic versus GABAergic identity of postsynaptic domains. Nature 511, 466–470 (2014).
pubmed: 24896188
doi: 10.1038/nature13313
Apte, S. S. A Disintegrin-like and Metalloprotease (Reprolysin-type) with Thrombospondin Type 1 Motif (ADAMTS) superfamily: functions and mechanisms. J. Biol. Chem. 284, 31493–31497 (2009).
pubmed: 19734141
pmcid: 2797218
doi: 10.1074/jbc.R109.052340
Dow, D. J. et al. ADAMTSL3 as a candidate gene for schizophrenia: Gene sequencing and ultra-high density association analysis by imputation. Schizophrenia Res. 127, 28–34 (2011).
doi: 10.1016/j.schres.2010.12.009
Zhou, X. & Bessereau, J.-L. Molecular architecture of genetically-tractable GABA Synapses in C. elegans. Front. Mol. Neurosci. 12, 304 (2019).
pubmed: 31920535
pmcid: 6920096
doi: 10.3389/fnmol.2019.00304
Maro, G. S. et al. MADD-4/punctin and neurexin organize C. elegans GABAergic postsynapses through neuroligin. Neuron 86, 1420–1432 (2015).
pubmed: 26028574
pmcid: 4672740
doi: 10.1016/j.neuron.2015.05.015
Tong, X.-J., Hu, Z., Liu, Y., Anderson, D. & Kaplan, J. M. A network of autism linked genes stabilizes two pools of synaptic GABAA receptors. eLife 4, e09648 (2015).
pubmed: 26575289
pmcid: 4642926
doi: 10.7554/eLife.09648
Gally, C. & Bessereau, J.-L. GABA is dispensable for the formation of junctional GABA receptor clusters in Caenorhabditis elegans. J. Neurosci. 23, 2591–2599 (2003).
pubmed: 12684444
pmcid: 6742079
doi: 10.1523/JNEUROSCI.23-07-02591.2003
Hoskins, R., Hajnal, A. F., Harp, S. A. & Kim, S. K. The C. elegans vulval induction gene lin-2 encodes a member of the MAGUK family of cell junction proteins. Development 122, 97–111 (1996).
pubmed: 8565857
Wu, G.-H., Muthaiyan Shanmugam, M., Bhan, P., Huang, Y.-H. & Wagner, O. I. Identification and characterization of LIN-2(CASK) as a regulator of Kinesin-3 UNC-104(KIF1A) motility and clustering in neurons. Traffic 17, 891–907 (2016).
pubmed: 27172328
doi: 10.1111/tra.12413
Gitai, Z., Yu, T. W., Lundquist, E. A., Tessier-Lavigne, M. & Bargmann, C. I. The netrin receptor UNC-40/DCC stimulates axon attraction and outgrowth through enabled and, in parallel, Rac and UNC-115/AbLIM. Neuron 37, 53–65 (2003).
pubmed: 12526772
doi: 10.1016/S0896-6273(02)01149-2
Gamblin, C. L. et al. Oligomerization of the FERM-FA protein Yurt controls epithelial cell polarity. J. Cell Biol. 217, 3853–3862 (2018).
pubmed: 30082297
pmcid: 6219725
doi: 10.1083/jcb.201803099
Hirano, Y. et al. Structural basis of cargo recognition by the myosin-X MyTH4–FERM domain. EMBO J. 30, 2734–2747 (2011).
pubmed: 21642953
pmcid: 3155308
doi: 10.1038/emboj.2011.177
Wei, Z., Yan, J., Lu, Q., Pan, L. & Zhang, M. Cargo recognition mechanism of myosin X revealed by the structure of its tail MyTH4-FERM tandem in complex with the DCC P3 domain. PNAS 108, 3572–3577 (2011).
pubmed: 21321230
doi: 10.1073/pnas.1016567108
Stein, E., Zou, Y., Poo, M. & Tessier-Lavigne, M. Binding of DCC by Netrin-1 to mediate axon guidance independent of adenosine A2B receptor activation. Science 291, 1976–1982 (2001).
pubmed: 11239160
doi: 10.1126/science.1059391
Chen, C.-H., He, C.-W., Liao, C.-P. & Pan, C.-L. A Wnt-planar polarity pathway instructs neurite branching by restricting F-actin assembly through endosomal signaling. PLoS Genet. 13, (2017).
Wang, X. et al. Transmembrane protein MIG-13 links the Wnt signaling and Hox genes to the cell polarity in neuronal migration. PNAS 110, 11175–11180 (2013).
pubmed: 23784779
doi: 10.1073/pnas.1301849110
Goldman, J. S. et al. Netrin-1 promotes excitatory synaptogenesis between cortical neurons by initiating synapse assembly. J. Neurosci. 33, 17278–17289 (2013).
pubmed: 24174661
pmcid: 6618363
doi: 10.1523/JNEUROSCI.1085-13.2013
Finci, L., Zhang, Y., Meijers, R. & Wang, J.-H. Signaling mechanism of the netrin-1 receptor DCC in axon guidance. Prog. Biophys. Mol. Biol. 118, 153–160 (2015).
pubmed: 25881791
pmcid: 4537816
doi: 10.1016/j.pbiomolbio.2015.04.001
Antoine-Bertrand, J., Ghogha, A., Luangrath, V., Bedford, F. K. & Lamarche-Vane, N. The activation of ezrin–radixin–moesin proteins is regulated by netrin-1 through Src kinase and RhoA/Rho kinase activities and mediates netrin-1–induced axon outgrowth. Mol. Biol. Cell 22, 3734–3746 (2011).
pubmed: 21849478
pmcid: 3183026
doi: 10.1091/mbc.e10-11-0917
Zhuang, B., Su, Y. S. & Sockanathan, S. FARP1 promotes the dendritic growth of spinal motor neuron subtypes through transmembrane Semaphorin6A and PlexinA4 signaling. Neuron 61, 359–372 (2009).
pubmed: 19217374
pmcid: 2654783
doi: 10.1016/j.neuron.2008.12.022
Cheadle, L. & Biederer, T. Activity-dependent regulation of dendritic complexity by semaphorin 3A through Farp1. J. Neurosci. 34, 7999–8009 (2014).
pubmed: 24899721
pmcid: 4044256
doi: 10.1523/JNEUROSCI.3950-13.2014
Toyofuku, T. et al. FARP2 triggers signals for Sema3A-mediated axonal repulsion. Nat. Neurosci. 8, 1712 (2005).
pubmed: 16286926
doi: 10.1038/nn1596
Cheadle, L. & Biederer, T. The novel synaptogenic protein Farp1 links postsynaptic cytoskeletal dynamics and transsynaptic organization. J. Cell Biol. 199, 985–1001 (2012).
pubmed: 23209303
pmcid: 3518221
doi: 10.1083/jcb.201205041
Kuo, Y.-C. et al. Structural analyses of FERM domain-mediated membrane localization of FARP1. Sci. Rep. 8, 10477 (2018).
pubmed: 29992992
pmcid: 6041286
doi: 10.1038/s41598-018-28692-4
Biederer, T. & Südhof, T. C. CASK and protein 4.1 support F-actin nucleation on neurexins. J. Biol. Chem. 276, 47869–47876 (2001).
pubmed: 11604393
doi: 10.1074/jbc.M105287200
Hsueh, Y.-P. et al. Direct interaction of CASK/LIN-2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. J. Cell Biol. 142, 139–151 (1998).
pubmed: 9660869
pmcid: 2133027
doi: 10.1083/jcb.142.1.139
Chen, K. & Featherstone, D. E. Pre and postsynaptic roles for Drosophila CASK. Mol. Cell. Neurosci. 48, 171–182 (2011).
pubmed: 21820054
doi: 10.1016/j.mcn.2011.07.009
Hsueh, Y.-P., Wang, T.-F., Yang, F.-C. & Sheng, M. Nuclear translocation and transcription regulation by the membrane-associated guanylate kinase CASK/LIN-2. Nature 404, 298 (2000).
pubmed: 10749215
doi: 10.1038/35005118
Wang, T.-F. et al. Identification of Tbr-1/CASK complex target genes in neurons. J. Neurochemistry 91, 1483–1492 (2004).
doi: 10.1111/j.1471-4159.2004.02845.x
Bamber, B. A., Beg, A. A., Twyman, R. E. & Jorgensen, E. M. The Caenorhabditis elegans unc-49 locus encodes multiple subunits of a heteromultimeric GABA receptor. J. Neurosci. 19, 5348–5359 (1999).
pubmed: 10377345
pmcid: 6782323
doi: 10.1523/JNEUROSCI.19-13-05348.1999
Fritschy, J.-M., Harvey, R. J. & Schwarz, G. Gephyrin: where do we stand, where do we go? Trends Neurosci. 31, 257–264 (2008).
pubmed: 18403029
doi: 10.1016/j.tins.2008.02.006
Tyagarajan, S. K. & Fritschy, J.-M. Gephyrin: a master regulator of neuronal function? Nat. Rev. Neurosci. 15, 141–156 (2014).
pubmed: 24552784
doi: 10.1038/nrn3670
Yamasaki, T., Hoyos-Ramirez, E., Martenson, J. S., Morimoto-Tomita, M. & Tomita, S. GARLH family proteins stabilize GABAA receptors at synapses. Neuron 93, 1138–1152.e6 (2017).
pubmed: 28279354
pmcid: 5347473
doi: 10.1016/j.neuron.2017.02.023
Davenport, E. C. et al. An essential role for the tetraspanin LHFPL4 in the cell-type-specific targeting and clustering of synaptic GABAA receptors. Cell Rep. 21, 70–83 (2017).
pubmed: 28978485
pmcid: 5640807
doi: 10.1016/j.celrep.2017.09.025
Kneussel, M. et al. Loss of postsynaptic GABAA receptor clustering in gephyrin-deficient mice. J. Neurosci. 19, 9289–9297 (1999).
pubmed: 10531433
pmcid: 6782938
doi: 10.1523/JNEUROSCI.19-21-09289.1999
Lévi, S., Logan, S. M., Tovar, K. R. & Craig, A. M. Gephyrin is critical for glycine receptor clustering but not for the formation of functional GABAergic synapses in hippocampal neurons. J. Neurosci. 24, 207–217 (2004).
pubmed: 14715953
pmcid: 6729579
doi: 10.1523/JNEUROSCI.1661-03.2004
Crestani, F. et al. Trace fear conditioning involves hippocampal α5 GABAA receptors. Proc. Natl Acad. Sci. USA 99, 8980–8985 (2002).
pubmed: 12084936
doi: 10.1073/pnas.142288699
Loebrich, S., Bähring, R., Katsuno, T., Tsukita, S. & Kneussel, M. Activated radixin is essential for GABAA receptor α5 subunit anchoring at the actin cytoskeleton. EMBO J. 25, 987–999 (2006).
pubmed: 16467845
pmcid: 1409722
doi: 10.1038/sj.emboj.7600995
Serwanski, D. R. et al. Synaptic and non-synaptic localization of GABAA receptors containing the α5 subunit in the rat brain. J. Comp. Neurol. 499, 458–470 (2006).
pubmed: 16998906
pmcid: 2749292
doi: 10.1002/cne.21115
Loh, K. H. et al. Proteomic analysis of unbounded cellular compartments: synaptic clefts. Cell 166(1295-1307), e21 (2016).
Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94 (1974).
pubmed: 4366476
pmcid: 1213120
Bindels, D. S. et al. mScarlet: a bright monomeric red fluorescent protein for cellular imaging. Nat. Methods 14, 53–56 (2017).
pubmed: 27869816
doi: 10.1038/nmeth.4074
El Mouridi, S. et al. Reliable CRISPR/Cas9 genome engineering in Caenorhabditis elegans using a single efficient sgRNA and an easily recognizable phenotype. G3 (Bethesda) 7, 1429–1437 (2017).
doi: 10.1534/g3.117.040824
Dickinson, D. J., Pani, A. M., Heppert, J. K., Higgins, C. D. & Goldstein, B. Streamlined genome engineering with a self-excising drug selection cassette. Genetics 200, 1035–1049 (2015).
pubmed: 26044593
pmcid: 4574250
doi: 10.1534/genetics.115.178335
Frøkjær-Jensen, C., Davis, M. W., Ailion, M. & Jorgensen, E. M. Improved Mos1-mediated transgenesis in C. elegans. Nat. Methods 9, 117–118 (2012).
pubmed: 22290181
pmcid: 3725292
doi: 10.1038/nmeth.1865
Frøkjær-Jensen, C. et al. Random and targeted transgene insertion in Caenorhabditis elegans using a modified Mos1 transposon. Nat. Meth 11, 529–534 (2014).
doi: 10.1038/nmeth.2889
Bolte, S. & Cordelières, F. P. A guided tour into subcellular colocalization analysis in light microscopy. J. Microscopy 224, 213–232.
Dunn, K. W., Kamocka, M. M. & McDonald, J. H. A practical guide to evaluating colocalization in biological microscopy. Am. J. Physiol. - Cell Physiol. 300, C723–C742 (2011).
pubmed: 21209361
pmcid: 3074624
doi: 10.1152/ajpcell.00462.2010
Liewald, J. F. et al. Optogenetic analysis of synaptic function. Nat. Methods 5, 895–902 (2008).
pubmed: 18794862
doi: 10.1038/nmeth.1252
Lainé, V., Frøkjær-Jensen, C., Couchoux, H. & Jospin, M. The α1 subunit EGL-19, the α2/δ subunit UNC-36, and the β subunit CCB-1 underlie voltage-dependent calcium currents in Caenorhabditis elegans striated muscle. J. Biol. Chem. 286, 36180–36187 (2011).
pubmed: 21878625
pmcid: 3196126
doi: 10.1074/jbc.M111.256149
Zhou, X. et al. A novel bipartite UNC-101/AP-1 μ1 binding signal mediates KVS-4/Kv2.1 somatodendritic distribution in Caenorhabditis elegans. FEBS Lett. 590, 76–92 (2016).
pubmed: 26762178
doi: 10.1002/1873-3468.12043
Gally, C., Eimer, S., Richmond, J. E. & Bessereau, J.-L. A transmembrane protein required for acetylcholine receptor clustering in Caenorhabditis elegans. Nature 431, 578–582 (2004).
pubmed: 15457263
pmcid: 3781939
doi: 10.1038/nature02893