Synaptic organizing complexes

Current Opinion in Neurobiology

Volumn 21, Issue 1, 2011, Pages 132-143

  Siddiqui, Tabrez J ^a   Craig, Ann Marie ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; FIBROBLAST GROWTH FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLUTAMATE RECEPTOR; LEUCINE RICH REPEAT TRANSMEMBRANE NEURONAL PROTEIN; MEMBRANE PROTEIN; NEUREXIN; NEUROLIGIN; PROTEIN TYROSINE PHOSPHATASE; THROMBOSPONDIN; UNCLASSIFIED DRUG;

DENDRITE; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTOGENESIS; TRANSCRIPTION REGULATION;

ANIMALS; AXONS; DENDRITES; HUMANS; NEURAL CELL ADHESION MOLECULES; SYNAPSES; TRANSCRIPTION FACTORS;

EID: 79952071854     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2010.08.016     Document Type: Review

References (106)

1. Yamagata M., Sanes J.R., Weiner J.A. Synaptic adhesion molecules. Curr Opin Cell Biol 2003, 15:621-632.
2. Greer P.L., Greenberg M.E. From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function. Neuron 2008, 59:846-860.
3. Ichtchenko K., Nguyen T., Sudhof T.C. Structures, alternative splicing, and neurexin binding of multiple neuroligins. J Biol Chem 1996, 271:2676-2682.
4. Craig A.M., Kang Y. Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol 2007, 17:43-52.
5. Sudhof T.C. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 2008, 455:903-911.
6. Linhoff M.W., Lauren J., Cassidy R.M., Dobie F.A., Takahashi H., Nygaard H.B., Airaksinen M.S., Strittmatter S.M., Craig A.M. An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers. Neuron 2009, 61:734-749.
7. Ko J., Fuccillo M.V., Malenka R.C., Sudhof T.C. LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation. Neuron 2009, 64:791-798.
8. de Wit J., Sylwestrak E., O'Sullivan M.L., Otto S., Tiglio K., Savas J.N., Yates J.R., Comoletti D., Taylor P., Ghosh A. LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation. Neuron 2009, 64:799-806.
9. Siddiqui T.J., Pancaroglu R., Kang Y., Rooyakkers A., Craig A.M. LRRTMs and neuroligins bind neurexins with a differential code to cooperate in glutamate synapse development. J Neurosci 2010, 30:7495-7506.
10. Varoqueaux F., Aramuni G., Rawson R.L., Mohrmann R., Missler M., Gottmann K., Zhang W., Sudhof T.C., Brose N. Neuroligins determine synapse maturation and function. Neuron 2006, 51:741-754.
11. Lauren J., Airaksinen M.S., Saarma M., Timmusk T. A novel gene family encoding leucine-rich repeat transmembrane proteins differentially expressed in the nervous system. Genomics 2003, 81:411-421.
12. Uemura T., Lee S.J., Yasumura M., Takeuchi T., Yoshida T., Ra M., Taguchi R., Sakimura K., Mishina M. Trans-synaptic interaction of GluRdelta2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum. Cell 2010, 141:1068-1079.
13. Matsuda K., Miura E., Miyazaki T., Kakegawa W., Emi K., Narumi S., Fukazawa Y., Ito-Ishida A., Kondo T., Shigemoto R., et al. Cbln1 is a ligand for an orphan glutamate receptor delta2, a bidirectional synapse organizer. Science 2010, 328:363-368.
14. Hirai H., Pang Z., Bao D., Miyazaki T., Li L., Miura E., Parris J., Rong Y., Watanabe M., Yuzaki M., et al. Cbln1 is essential for synaptic integrity and plasticity in the cerebellum. Nat Neurosci 2005, 8:1534-1541.
15. Kashiwabuchi N., Ikeda K., Araki K., Hirano T., Shibuki K., Takayama C., Inoue Y., Kutsuwada T., Yagi T., Kang Y., et al. Impairment of motor coordination. Purkinje cell synapse formation, and cerebellar long-term depression in GluR delta 2 mutant mice. Cell 1995, 81:245-252.
16. Woo J., Kwon S.K., Choi S., Kim S., Lee J.R., Dunah A.W., Sheng M., Kim E. Trans-synaptic adhesion between NGL-3 and LAR regulates the formation of excitatory synapses. Nat Neurosci 2009, 12:428-437.
17. Kwon S.K., Woo J., Kim S.Y., Kim H., Kim E. 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 2010, 285:13966-13978.
18. Kim S., Burette A., Chung H.S., Kwon S.K., Woo J., Lee H.W., Kim K., Kim H., Weinberg R.J., Kim E. NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nat Neurosci 2006, 9:1294-1301.
19. Umemori H., Linhoff M.W., Ornitz D.M., Sanes J.R. FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 2004, 118:257-270.
20. Christopherson K.S., Ullian E.M., Stokes C.C., Mullowney C.E., Hell J.W., Agah A., Lawler J., Mosher D.F., Bornstein P., Barres B.A. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 2005, 120:421-433.
21. Li A.J., Suzuki S., Suzuki M., Mizukoshi E., Imamura T. Fibroblast growth factor-2 increases functional excitatory synapses on hippocampal neurons. Eur J Neurosci 2002, 16:1313-1324.
22. Umemori H., Sanes J.R. Signal regulatory proteins (SIRPS) are secreted presynaptic organizing molecules. J Biol Chem 2008, 283:34053-34061.
23. Terauchi A., Johnson-Venkatesh E.M., Toth A.B., Javed D., Sutton M.A., Umemori H. Distinct FGFs promote differentiation of excitatory and inhibitory synapses. Nature 2010, 465:783-787.
24. Eroglu C., Allen N.J., Susman M.W., O'Rourke N.A., Park C.Y., Ozkan E., Chakraborty C., Mulinyawe S.B., Annis D.S., Huberman A.D., et al. Gabapentin receptor alpha2delta-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis. Cell 2009, 139:380-392.
25. Xu J., Xiao N., Xia J. Thrombospondin 1 accelerates synaptogenesis in hippocampal neurons through neuroligin 1. Nat Neurosci 2010, 13:22-24.
26. Scheiffele P., Fan J., Choih J., Fetter R., Serafini T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 2000, 101:657-669.
27. Dean C., Scholl F.G., Choih J., DeMaria S., Berger J., Isacoff E., Scheiffele P. Neurexin mediates the assembly of presynaptic terminals. Nat Neurosci 2003, 6:708-716.
28. Ko J., Zhang C., Arac D., Boucard A.A., Brunger A.T., Sudhof T.C. Neuroligin-1 performs neurexin-dependent and neurexin-independent functions in synapse validation. EMBO J 2009, 28:3244-3255.
29. Boucard A.A., Chubykin A.A., Comoletti D., Taylor P., Sudhof T.C. A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron 2005, 48:229-236.
30. Missler M., Zhang W., Rohlmann A., Kattenstroth G., Hammer R.E., Gottmann K., Sudhof T.C. Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 2003, 424:939-948.
31. Chih B., Gollan L., Scheiffele P. Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 2006, 51:171-178.
32. Kang Y., Zhang X., Dobie F., Wu H., Craig A.M. Induction of GABAergic postsynaptic differentiation by alpha-neurexins. J Biol Chem 2008, 283:2323-2334.
33. Sugita S., Saito F., Tang J., Satz J., Campbell K., Sudhof T.C. A stoichiometric complex of neurexins and dystroglycan in brain. J Cell Biol 2001, 154:435-445.
34. Knuesel I., Mastrocola M., Zuellig R.A., Bornhauser B., Schaub M.C., Fritschy J.M. Short communication: altered synaptic clustering of GABAA receptors in mice lacking dystrophin (mdx mice). Eur J Neurosci 1999, 11:4457-4462.
35. Levi S., Grady R.M., Henry M.D., Campbell K.P., Sanes J.R., Craig A.M. Dystroglycan is selectively associated with inhibitory GABAergic synapses but is dispensable for their differentiation. J Neurosci 2002, 22:4274-4285.
36. Hata Y., Butz S., Sudhof T.C. CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J Neurosci 1996, 16:2488-2494.
37. Biederer T., Sudhof T.C. Mints as adaptors. Direct binding to neurexins and recruitment of munc18. J Biol Chem 2000, 275:39803-39806.
38. Grootjans J.J., Reekmans G., Ceulemans H., David G. Syntenin-syndecan binding requires syndecan-synteny and the co-operation of both PDZ domains of syntenin. J Biol Chem 2000, 275:19933-19941.
39. Biederer T., Sudhof T.C. CASK and protein 4.1 support F-actin nucleation on neurexins. J Biol Chem 2001, 276:47869-47876.
40. Hata Y., Davletov B., Petrenko A.G., Jahn R., Sudhof T.C. Interaction of synaptotagmin with the cytoplasmic domains of neurexins. Neuron 1993, 10:307-315.
41. Fu Z., Washbourne P., Ortinski P., Vicini S. Functional excitatory synapses in HEK293 cells expressing neuroligin and glutamate receptors. J Neurophysiol 2003, 90:3950-3957.
42. Sara Y., Biederer T., Atasoy D., Chubykin A., Mozhayeva M.G., Sudhof T.C., Kavalali E.T. Selective capability of SynCAM and neuroligin for functional synapse assembly. J Neurosci 2005, 25:260-270.
43. Mukherjee K., Sharma M., Urlaub H., Bourenkov G.P., Jahn R., Sudhof T.C., Wahl M.C. CASK functions as a Mg2+-independent neurexin kinase. Cell 2008, 133:328-339.
44. Lucido A.L., Suarez Sanchez F., Thostrup P., Kwiatkowski A.V., Leal-Ortiz S., Gopalakrishnan G., Liazoghli D., Belkaid W., Lennox R.B., Grutter P., et al. Rapid assembly of functional presynaptic boutons triggered by adhesive contacts. J Neurosci 2009, 29:12449-12466.
45. Pulido R., Serra-Pages C., Tang M., Streuli M. The LAR/PTP delta/PTP sigma subfamily of transmembrane protein-tyrosine-phosphatases: multiple human LAR, PTP delta, and PTP sigma isoforms are expressed in a tissue-specific manner and associate with the LAR-interacting protein LIP. 1. Proc Natl Acad Sci U S A 1995, 92:11686-11690.
46. Stryker E., Johnson K.G. LAR, liprin alpha and the regulation of active zone morphogenesis. J Cell Sci 2007, 120:3723-3728.
47. Sigrist SJ, Schmitz D: Structural and functional plasticity of the cytoplasmic active zone. Curr Opin Neurobiol 2011, in press, this issue, doi:10.1016/j.conb.2010.08.012.
48. Fogel A.I., Akins M.R., Krupp A.J., Stagi M., Stein V., Biederer T. SynCAMs organize synapses through heterophilic adhesion. J Neurosci 2007, 27:12516-12530.
49. Kayser M.S., McClelland A.C., Hughes E.G., Dalva M.B. Intracellular and trans-synaptic regulation of glutamatergic synaptogenesis by EphB receptors. J Neurosci 2006, 26:12152-12164.
50. McClelland A.C., Hruska M., Coenen A.J., Henkemeyer M., Dalva M.B. Trans-synaptic EphB2-ephrin-B3 interaction regulates excitatory synapse density by inhibition of postsynaptic MAPK signaling. Proc Natl Acad Sci U S A 2010, 107:8830-8835.
51. Aoto J., Ting P., Maghsoodi B., Xu N., Henkemeyer M., Chen L. Postsynaptic ephrinB3 promotes shaft glutamatergic synapse formation. J Neurosci 2007, 27:7508-7519.
52. Park J., Liu B., Chen T., Li H., Hu X., Gao J., Zhu Y., Zhu Q., Qiang B., Yuan J., et al. Disruption of Nectin-like 1 cell adhesion molecule leads to delayed axonal myelination in the CNS. J Neurosci 2008, 28:12815-12819.
53. Niederkofler V., Baeriswyl T., Ott R., Stoeckli E.T. Nectin-like molecules/SynCAMs are required for post-crossing commissural axon guidance. Development 2010, 137:427-435.
54. Wang Z., Wang B., Yang L., Guo Q., Aithmitti N., Songyang Z., Zheng H. Presynaptic and postsynaptic interaction of the amyloid precursor protein promotes peripheral and central synaptogenesis. J Neurosci 2009, 29:10788-10801.
55. Mah W., Ko J., Nam J., Han K., Chung W.S., Kim E. Selected SALM (synaptic adhesion-like molecule) family proteins regulate synapse formation. J Neurosci 2010, 30:5559-5568.
56. Seabold G.K., Wang P.Y., Chang K., Wang C.Y., Wang Y.X., Petralia R.S., Wenthold R.J. The SALM family of adhesion-like molecules forms heteromeric and homomeric complexes. J Biol Chem 2008, 283:8395-8405.
57. Stan A., Pielarski K.N., Brigadski T., Wittenmayer N., Fedorchenko O., Gohla A., Lessmann V., Dresbach T., Gottmann K. Essential cooperation of N-cadherin and neuroligin-1 in the transsynaptic control of vesicle accumulation. Proc Natl Acad Sci U S A 2010, 107:11116-11121.
58. Chubykin A.A., Atasoy D., Etherton M.R., Brose N., Kavalali E.T., Gibson J.R., Sudhof T.C. Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 2007, 54:919-931.
59. Poulopoulos A., Aramuni G., Meyer G., Soykan T., Hoon M., Papadopoulos T., Zhang M., Paarmann I., Fuchs C., Harvey K., et al. Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 2009, 63:628-642.
60. Gibson J.R., Huber K.M., Sudhof T.C. Neuroligin-2 deletion selectively decreases inhibitory synaptic transmission originating from fast-spiking but not from somatostatin-positive interneurons. J Neurosci 2009, 29:13883-13897.
61. Blundell J., Blaiss C.A., Etherton M.R., Espinosa F., Tabuchi K., Walz C., Bolliger M.F., Sudhof T.C., Powell C.M. Neuroligin-1 deletion results in impaired spatial memory and increased repetitive behavior. J Neurosci 2010, 30:2115-2129.
62. Poo M.M. Neurotrophins as synaptic modulators. Nat Rev Neurosci 2001, 2:24-32.
63. Ledda F., Paratcha G., Sandoval-Guzman T., Ibanez C.F. GDNF and GFRalpha1 promote formation of neuronal synapses by ligand-induced cell adhesion. Nat Neurosci 2007, 10:293-300.
64. Hall A.C., Lucas F.R., Salinas P.C. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 2000, 100:525-535.
65. Ahmad-Annuar A., Ciani L., Simeonidis I., Herreros J., Fredj N.B., Rosso S.B., Hall A., Brickley S., Salinas P.C. Signaling across the synapse: a role for Wnt and Dishevelled in presynaptic assembly and neurotransmitter release. J Cell Biol 2006, 174:127-139.
66. Cerpa W., Godoy J.A., Alfaro I., Farias G.G., Metcalfe M.J., Fuentealba R., Bonansco C., Inestrosa N.C. Wnt-7a modulates the synaptic vesicle cycle and synaptic transmission in hippocampal neurons. J Biol Chem 2008, 283:5918-5927.
67. Sahores M., Gibb A., Salinas P.C. Frizzled-5, a receptor for the synaptic organizer Wnt7a, regulates activity-mediated synaptogenesis. Development 2010, 137:2215-2225.
68. Salinas P.C., Zou Y. Wnt signaling in neural circuit assembly. Annu Rev Neurosci 2008, 31:339-358.
69. Inestrosa N.C., Arenas E. Emerging roles of Wnts in the adult nervous system. Nat Rev Neurosci 2010, 11:77-86.
70. Klassen M.P., Shen K. Wnt signaling positions neuromuscular connectivity by inhibiting synapse formation in C. elegans. Cell 2007, 130:704-716.
71. Graf E.R., Zhang X., Jin S.X., Linhoff M.W., Craig A.M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 2004, 119:1013-1026.
72. Irie M., Hata Y., Takeuchi M., Ichtchenko K., Toyoda A., Hirao K., Takai Y., Rosahl T.W., Sudhof T.C. Binding of neuroligins to PSD-95. Science 1997, 277:1511-1515.
73. Roche K.W., Ly C.D., Petralia R.S., Wang Y.X., McGee A.W., Bredt D.S., Wenthold R.J. Postsynaptic density-93 interacts with the delta2 glutamate receptor subunit at parallel fiber synapses. J Neurosci 1999, 19:3926-3934.
74. Meyer G., Varoqueaux F., Neeb A., Oschlies M., Brose N. The complexity of PDZ domain-mediated interactions at glutamatergic synapses: a case study on neuroligin. Neuropharmacology 2004, 47:724-733.
75. Uemura T., Mori H., Mishina M. Direct interaction of GluRdelta2 with Shank scaffold proteins in cerebellar Purkinje cells. Mol Cell Neurosci 2004, 26:330-341.
76. Dresbach T., Neeb A., Meyer G., Gundelfinger E.D., Brose N. Synaptic targeting of neuroligin is independent of neurexin and SAP90/PSD95 binding. Mol Cell Neurosci 2004, 27:227-235.
77. Nam C.I., Chen L. Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proc Natl Acad Sci U S A 2005, 102:6137-6142.
78. Ko J., Kim S., Chung H.S., Kim K., Han K., Kim H., Jun H., Kaang B.K., Kim E. SALM synaptic cell adhesion-like molecules regulate the differentiation of excitatory synapses. Neuron 2006, 50:233-245.
79. Wang C.Y., Chang K., Petralia R.S., Wang Y.X., Seabold G.K., Wenthold R.J. A novel family of adhesion-like molecules that interacts with the NMDA receptor. J Neurosci 2006, 26:2174-2183.
80. Dalva M.B., Takasu M.A., Lin M.Z., Shamah S.M., Hu L., Gale N.W., Greenberg M.E. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 2000, 103:945-956.
81. Chih B., Engelman H., Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 2005, 307:1324-1328.
82. Kayser M.S., Nolt M.J., Dalva M.B. EphB receptors couple dendritic filopodia motility to synapse formation. Neuron 2008, 59:56-69.
83. Lai K.O., Ip N.Y. Synapse development and plasticity: roles of ephrin/Eph receptor signaling. Curr Opin Neurobiol 2009, 19:275-283.
84. Conroy W.G., Nai Q., Ross B., Naughton G., Berg D.K. Postsynaptic neuroligin enhances presynaptic inputs at neuronal nicotinic synapses. Dev Biol 2007, 307:79-91.
85. Varoqueaux F., Jamain S., Brose N. Neuroligin 2 is exclusively localized to inhibitory synapses. Eur J Cell Biol 2004, 83:449-456.
86. Song J.Y., Ichtchenko K., Sudhof T.C., Brose N. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc Natl Acad Sci U S A 1999, 96:1100-1105.
87. Papadopoulos T., Korte M., Eulenburg V., Kubota H., Retiounskaia M., Harvey R.J., Harvey K., O'Sullivan G.A., Laube B., Hulsmann S., et al. Impaired GABAergic transmission and altered hippocampal synaptic plasticity in collybistin-deficient mice. EMBO J 2007, 26:3888-3899.
88. Zhang C., Atasoy D., Arac D., Yang X., Fucillo M.V., Robison A.J., Ko J., Brunger A.T., Sudhof T.C. Neurexins physically and functionally interact with GABA(A) receptors. Neuron 2010, 66:403-416.
89. Levinson J.N., El-Husseini A. Building excitatory and inhibitory synapses: balancing neuroligin partnerships. Neuron 2005, 48:171-174.
90. O'Brien R.J., Xu D., Petralia R.S., Steward O., Huganir R.L., Worley P. Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp. Neuron 1999, 23:309-323.
91. Xu D., Hopf C., Reddy R., Cho R.W., Guo L., Lanahan A., Petralia R.S., Wenthold R.J., O'Brien R.J., Worley P. Narp and NP1 form heterocomplexes that function in developmental and activity-dependent synaptic plasticity. Neuron 2003, 39:513-528.
92. Sia G.M., Beique J.C., Rumbaugh G., Cho R., Worley P.F., Huganir R.L. Interaction of the N-terminal domain of the AMPA receptor GluR4 subunit with the neuronal pentraxin NP1 mediates GluR4 synaptic recruitment. Neuron 2007, 55:87-102.
93. Koch S.M., Ullian E.M. Neuronal pentraxins mediate silent synapse conversion in the developing visual system. J Neurosci 2010, 30:5404-5414.
94. Bjartmar L., Huberman A.D., Ullian E.M., Renteria R.C., Liu X., Xu W., Prezioso J., Susman M.W., Stellwagen D., Stokes C.C., et al. Neuronal pentraxins mediate synaptic refinement in the developing visual system. J Neurosci 2006, 26:6269-6281.
95. Kurshan P.T., Oztan A., Schwarz T.L. Presynaptic alpha2delta-3 is required for synaptic morphogenesis independent of its Ca2+-channel functions. Nat Neurosci 2009, 12:1415-1423.
96. Nishimura-Akiyoshi S., Niimi K., Nakashiba T., Itohara S. Axonal netrin-Gs transneuronally determine lamina-specific subdendritic segments. Proc Natl Acad Sci U S A 2007, 104:14801-14806.
97. Takeuchi T., Miyazaki T., Watanabe M., Mori H., Sakimura K., Mishina M. Control of synaptic connection by glutamate receptor delta2 in the adult cerebellum. J Neurosci 2005, 25:2146-2156.
98. Gogolla N., Galimberti I., Deguchi Y., Caroni P. Wnt signaling mediates experience-related regulation of synapse numbers and mossy fiber connectivities in the adult hippocampus. Neuron 2009, 62:510-525.
99. Futai K., Kim M.J., Hashikawa T., Scheiffele P., Sheng M., Hayashi Y. Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin. Nat Neurosci 2007, 10:186-195.
100. Kakegawa W., Miyazaki T., Kohda K., Matsuda K., Emi K., Motohashi J., Watanabe M., Yuzaki M. The N-terminal domain of GluD2 (GluRdelta2) recruits presynaptic terminals and regulates synaptogenesis in the cerebellum in vivo. J Neurosci 2009, 29:5738-5748.
101. Jamain S., Quach H., Betancur C., Rastam M., Colineaux C., Gillberg I.C., Soderstrom H., Giros B., Leboyer M., Gillberg C., et al. Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat Genet 2003, 34:27-29.
102. Betancur C., Sakurai T., Buxbaum J.D. The emerging role of synaptic cell-adhesion pathways in the pathogenesis of autism spectrum disorders. Trends Neurosci 2009, 32:402-412.
103. Jamain S., Radyushkin K., Hammerschmidt K., Granon S., Boretius S., Varoqueaux F., Ramanantsoa N., Gallego J., Ronnenberg A., Winter D., et al. Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism. Proc Natl Acad Sci U S A 2008, 105:1710-1715.
104. Francks C., Maegawa S., Lauren J., Abrahams B.S., Velayos-Baeza A., Medland S.E., Colella S., Groszer M., McAuley E.Z., Caffrey T.M., et al. LRRTM1 on chromosome 2p12 is a maternally suppressed gene that is associated paternally with handedness and schizophrenia. Mol Psychiatry 2007, 12:1129-1139. 1057.
105. Fallin M.D., Lasseter V.K., Avramopoulos D., Nicodemus K.K., Wolyniec P.S., McGrath J.A., Steel G., Nestadt G., Liang K.Y., Huganir R.L., et al. Bipolar I disorder and schizophrenia: a 440-single-nucleotide polymorphism screen of 64 candidate genes among Ashkenazi Jewish case-parent trios. Am J Hum Genet 2005, 77:918-936.
106. Zhiling Y., Fujita E., Tanabe Y., Yamagata T., Momoi T., Momoi M.Y. Mutations in the gene encoding CADM1 are associated with autism spectrum disorder. Biochem Biophys Res Commun 2008, 377:926-929.