XPresynaptic neurexin-3 alternative splicing trans-synaptically controls postsynaptic AMPA receptor trafficking

Cell

Volumn 154, Issue 1, 2013, Pages 75-

  Aoto, Jason ^a   Martinelli, David C ^a   Malenka, Robert C ^a   Tabuchi, Katsuhiko ^a,b   Südhof, Thomas C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUREXIN; NEUREXIN 3; NEUROLIGIN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC RECOMBINATION; MOUSE; NONHUMAN; PHENOTYPE; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION;

MUS;

EID: 84879970825     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.05.060     Document Type: Article

References (60)

1. J. Aoto, C.I. Nam, M.M. Poon, P. Ting, and L. Chen Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity Neuron 60 2008 308 320
2. Y.C. Chen, Y.Q. Lin, S. Banerjee, K. Venken, J. Li, A. Ismat, K. Chen, L. Duraine, H.J. Bellen, and M.A. Bhat Drosophila neuroligin 2 is required presynaptically and postsynaptically for proper synaptic differentiation and synaptic transmission J. Neurosci. 32 2012 16018 16030
3. B. Chih, L. Gollan, and P. Scheiffele Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex Neuron 51 2006 171 178
4. A.A. Chubykin, D. Atasoy, M.R. Etherton, N. Brose, E.T. Kavalali, J.R. Gibson, and T.C. Südhof Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2 Neuron 54 2007 919 931
5. D. Comoletti, R.E. Flynn, A.A. Boucard, B. Demeler, V. Schirf, J. Shi, L.L. Jennings, H.R. Newlin, T.C. Südhof, and P. Taylor Gene selection, alternative splicing, and post-translational processing regulate neuroligin selectivity for β-neurexins Biochemistry 45 2006 12816 12827
6. A.M. Craig, and Y. Kang Neurexin-neuroligin signaling in synapse development Curr. Opin. Neurobiol. 17 2007 43 52
7. J. de Wit, E. Sylwestrak, M.L. O'Sullivan, S. Otto, K. Tiglio, J.N. Savas, J.R. Yates 3rd, D. Comoletti, P. Taylor, and A. Ghosh LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation Neuron 64 2009 799 806
8. M.R. Etherton, K. Tabuchi, M. Sharma, J. Ko, and T.C. Südhof An autism-associated point mutation in the neuroligin cytoplasmic tail selectively impairs AMPA receptor-mediated synaptic transmission in hippocampus EMBO J. 30 2011 2908 2919
9. N.L. Heard-Costa, M.C. Zillikens, K.L. Monda, A. Johansson, T.B. Harris, M. Fu, T. Haritunians, M.F. Feitosa, T. Aspelund, and G. Eiriksdottir NRXN3 is a novel locus for waist circumference: a genome-wide association study from the CHARGE Consortium PLoS Genet. 5 2009 e1000539
10. A. Hishimoto, Q.R. Liu, T. Drgon, O. Pletnikova, D. Walther, X.G. Zhu, J.C. Troncoso, and G.R. Uhl Neurexin 3 polymorphisms are associated with alcohol dependence and altered expression of specific isoforms Hum. Mol. Genet. 16 2007 2880 2891
11. Z. Hu, S. Hom, T. Kudze, X.J. Tong, S. Choi, G. Aramuni, W. Zhang, and J.M. Kaplan Neurexin and neuroligin mediate retrograde synaptic inhibition in C. elegans Science 337 2012 980 984
12. K. Ichtchenko, Y. Hata, T. Nguyen, B. Ullrich, M. Missler, C. Moomaw, and T.C. Südhof Neuroligin 1: a splice site-specific ligand for β-neurexins Cell 81 1995 435 443
13. T. Iijima, K. Wu, H. Witte, Y. Hanno-Iijima, T. Glatter, S. Richard, and P. Scheiffele SAM68 regulates neuronal activity-dependent alternative splicing of neurexin-1 Cell 147 2011 1601 1614
14. 2+ channels to presynaptic active zones via a direct PDZ-domain interaction Cell 144 2011 282 295
15. G. Kattenstroth, E. Tantalaki, T.C. Südhof, K. Gottmann, and M. Missler Postsynaptic N-methyl-D-aspartate receptor function requires α-neurexins Proc. Natl. Acad. Sci. USA 101 2004 2607 2612
16. G.A. Kerchner, and R.A. Nicoll Silent synapses and the emergence of a postsynaptic mechanism for LTP Nat. Rev. Neurosci. 9 2008 813 825
17. J. Ko, M.V. Fuccillo, R.C. Malenka, and T.C. Südhof LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation Neuron 64 2009 791 798
18. H.J. Koester, and D. Johnston Target cell-dependent normalization of transmitter release at neocortical synapses Science 308 2005 863 866
19. D.D. Krueger, L.P. Tuffy, T. Papadopoulos, and N. Brose The role of neurexins and neuroligins in the formation, maturation, and function of vertebrate synapses Curr. Opin. Neurobiol. 22 2012 412 422
20. H.M. Lachman, C.S. Fann, M. Bartzis, O.V. Evgrafov, R.N. Rosenthal, E.V. Nunes, C. Miner, M. Santana, J. Gaffney, and A. Riddick Genomewide suggestive linkage of opioid dependence to chromosome 14q Hum. Mol. Genet. 16 2007 1327 1334
21. K. Lee, Y. Kim, S.J. Lee, Y. Qiang, D. Lee, H.W. Lee, H. Kim, H.S. Je, T.C. Südhof, and J. Ko MDGAs interact selectively with neuroligin-2 but not other neuroligins to regulate inhibitory synapse development Proc. Natl. Acad. Sci. USA 110 2013 336 341
22. J.W. Lin, W. Ju, K. Foster, S.H. Lee, G. Ahmadian, M. Wyszynski, Y.T. Wang, and M. Sheng Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization Nat. Neurosci. 3 2000 1282 1290
23. K. Matsuda, and M. Yuzaki Cbln family proteins promote synapse formation by regulating distinct neurexin signaling pathways in various brain regions Eur. J. Neurosci. 33 2011 1447 1461
24. L. Menendez de la Prida, F. Suarez, and M.A. Pozo Electrophysiological and morphological diversity of neurons from the rat subicular complex in vitro Hippocampus 13 2003 728 744
25. 2+ channels to synaptic vesicle exocytosis Nature 423 2003 939 948
26. S. O'Mara The subiculum: what it does, what it might do, and what neuroanatomy has yet to tell us J. Anat. 207 2005 271 282
27. A.C. Reichelt, R.J. Rodgers, and S.J. Clapcote The role of neurexins in schizophrenia and autistic spectrum disorder Neuropharmacology 62 2012 1519 1526
28. M. Resnick, A. Segall, G.R. G, Z. Lupowitz, and N. Zisapel Alternative splicing of neurexins: a role for neuronal polypyrimidine tract binding protein Neurosci. Lett. 439 2008 235 240
29. A. Reyes, R. Lujan, A. Rozov, N. Burnashev, P. Somogyi, and B. Sakmann Target-cell-specific facilitation and depression in neocortical circuits Nat. Neurosci. 1 1998 279 285
30. L. Rowen, J. Young, B. Birditt, A. Kaur, A. Madan, D.L. Philipps, S. Qin, P. Minx, R.K. Wilson, L. Hood, and B.R. Graveley Analysis of the human neurexin genes: alternative splicing and the generation of protein diversity Genomics 79 2002 587 597
31. G. Rozic, Z. Lupowitz, and N. Zisapel Exonal elements and factors involved in the depolarization-induced alternative splicing of neurexin 2 J. Mol. Neurosci. 50 2012 221 233
32. E. Schnell, A.L. Bensen, E.K. Washburn, and G.L. Westbrook Neuroligin-1 overexpression in newborn granule cells in vivo PLoS ONE 7 2012 e48045
33. J. Schwenk, N. Harmel, A. Brechet, G. Zolles, H. Berkefeld, C.S. Müller, W. Bildl, D. Baehrens, B. Hüber, and A. Kulik High-resolution proteomics unravel architecture and molecular diversity of native AMPA receptor complexes Neuron 74 2012 621 633
34. M. Shapiro-Reznik, A. Jilg, H. Lerner, D.J. Earnest, and N. Zisapel Diurnal rhythms in neurexins transcripts and inhibitory/excitatory synapse scaffold proteins in the biological clock PLoS ONE 7 2012 e37894
35. T.J. Siddiqui, R. Pancaroglu, Y. Kang, A. Rooyakkers, and A.M. Craig LRRTMs and neuroligins bind neurexins with a differential code to cooperate in glutamate synapse development J. Neurosci. 30 2010 7495 7506
36. G.J. Soler-Llavina, M.V. Fuccillo, J. Ko, T.C. Südhof, and R.C. Malenka The neurexin ligands, neuroligins and leucine-rich repeat transmembrane proteins, perform convergent and divergent synaptic functions in vivo Proc. Natl. Acad. Sci. USA 108 2011 16502 16509
37. G.J. Soler-Llavina, P. Arstikaitis, W. Morishita, M. Ahmad, T.C. Südhof, and R.C. Malenka Leucine-Rich Repeat Transmembrane Proteins Are Essential for Maintenance of Long-term Potentiation Neuron 2013 10.1016/j.neuron.2013.06.007 Published online August 7, 2013
38. N.P. Staff, H.Y. Jung, T. Thiagarajan, M. Yao, and N. Spruston Resting and active properties of pyramidal neurons in subiculum and CA1 of rat hippocampus J. Neurophysiol. 84 2000 2398 2408
39. T.C. Südhof Neuroligins and neurexins link synaptic function to cognitive disease Nature 455 2008 903 911
40. S. Sugita, M. Khvochtev, and T.C. Südhof Neurexins are functional α-latrotoxin receptors Neuron 22 1999 489 496
41. S. Sugita, F. Saito, J. Tang, J. Satz, K. Campbell, and T.C. Südhof A stoichiometric complex of neurexins and dystroglycan in brain J. Cell Biol. 154 2001 435 445
42. K. Tabuchi, and T.C. Südhof Structure and evolution of neurexin genes: insight into the mechanism of alternative splicing Genomics 79 2002 849 859
43. H. Taniguchi, L. Gollan, F.G. Scholl, V. Mahadomrongkul, E. Dobler, N. Limthong, M. Peck, C. Aoki, and P. Scheiffele Silencing of neuroligin function by postsynaptic neurexins J. Neurosci. 27 2007 2815 2824
44. J.S. Taube Electrophysiological properties of neurons in the rat subiculum in vitro Exp. Brain Res. 96 1993 304 318
45. T. Uemura, S.J. Lee, M. Yasumura, T. Takeuchi, T. Yoshida, M. Ra, R. Taguchi, K. Sakimura, and M. Mishina Trans-synaptic interaction of GluRdelta2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum Cell 141 2010 1068 1079
46. B. Ullrich, Y.A. Ushkaryov, and T.C. Südhof Cartography of neurexins: more than 1000 isoforms generated by alternative splicing and expressed in distinct subsets of neurons Neuron 14 1995 497 507
47. Y.A. Ushkaryov, and T.C. Südhof Neurexin III α: extensive alternative splicing generates membrane-bound and soluble forms Proc. Natl. Acad. Sci. USA 90 1993 6410 6414
48. Y.A. Ushkaryov, A.G. Petrenko, M. Geppert, and T.C. Südhof Neurexins: synaptic cell surface proteins related to the α-latrotoxin receptor and laminin Science 257 1992 50 56
49. Y.A. Ushkaryov, Y. Hata, K. Ichtchenko, C. Moomaw, S. Afendis, C.A. Slaughter, and T.C. Südhof Conserved domain structure of β-neurexins. Unusual cleaved signal sequences in receptor-like neuronal cell-surface proteins J. Biol. Chem. 269 1994 11987 11992
50. A.K. Vaags, A.C. Lionel, D. Sato, M. Goodenberger, Q.P. Stein, S. Curran, C. Ogilvie, J.W. Ahn, I. Drmic, and L. Senman Rare deletions at the neurexin 3 locus in autism spectrum disorder Am. J. Hum. Genet. 90 2012 133 141
51. C. Wozny, N. Maier, D. Schmitz, and J. Behr Two different forms of long-term potentiation at CA1-subiculum synapses J. Physiol. 586 2008 2725 2734
52. W. Xu, W. Morishita, P.S. Buckmaster, Z.P. Pang, R.C. Malenka, and T.C. Südhof Distinct neuronal coding schemes in memory revealed by selective erasure of fast synchronous synaptic transmission Neuron 73 2012 990 1001
53. J. Aoto, P. Ting, B. Maghsoodi, N. Xu, M. Henkemeyer, and L. Chen Postsynaptic ephrinB3 promotes shaft glutamatergic synapse formation J. Neurosci. 27 2007 7508 7519
54. A.A. Boucard, A.A. Chubykin, D. Comoletti, P. Taylor, and T.C. Südhof A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to α- and β-neurexins Neuron 48 2005 229 236
55. A.A. Boucard, J. Ko, and T.C. Südhof High affinity neurexin binding to cell adhesion G-protein-coupled receptor CIRL1/latrophilin-1 produces an intercellular adhesion complex J. Biol. Chem. 287 2012 9399 9413
56. R.C. Carroll, D.V. Lissin, M. von Zastrow, R.A. Nicoll, and R.C. Malenka Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures Nat. Neurosci. 2 1999 454 460
57. A. Matus, V. Biou, H. Brinkhaus, and M. Roelandse Transfecting cultured hippocampal neurons with an actin-GFP plasmid CSH Protoc. 2007 2007 pdb prot4664
58. A. Maximov, Z.P. Pang, D.G. Tervo, and T.C. Südhof Monitoring synaptic transmission in primary neuronal cultures using local extracellular stimulation J. Neurosci. Methods 161 2007 75 87
59. 2+)-independent mechanism Neuron 70 2011 244 251
60. K. Tabuchi, J. Blundell, M.R. Etherton, R.E. Hammer, X. Liu, C.M. Powell, and T.C. Südhof A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice Science 318 2007 71 76