The cellular and molecular landscape of neuroligins

Trends in Neurosciences

Volumn 38, Issue 8, 2015, Pages 496-505

  Bemben, Michael A ^a,b   Shipman, Seth L ^c,d   Nicoll, Roger A ^e   Roche, Katherine W ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d Harvard University   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROLIGIN; LIGAND; NERVE CELL ADHESION MOLECULE;

CELLULAR DISTRIBUTION; DIMERIZATION; HUMAN; LANDSCAPE; MOLECULAR DYNAMICS; NERVE CELL PLASTICITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION; SYNAPSE;

AMINO ACID SEQUENCE; ANIMALS; CELL ADHESION MOLECULES, NEURONAL; HUMANS; LIGANDS; MODELS, NEUROLOGICAL; MOLECULAR SEQUENCE DATA; NEURONAL PLASTICITY; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; SYNAPSES;

EID: 84938553337     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2015.06.004     Document Type: Review

References (88)

1. Nguyen T., Sudhof T.C. Binding properties of neuroligin 1 and neurexin 1beta reveal function as heterophilic cell adhesion molecules. J. Biol. Chem. 1997, 272:26032-26039.
2. Choi U.B., et al. Beyond the random coil: stochastic conformational switching in intrinsically disordered proteins. Structure 2011, 19:566-576.
3. Sudhof T.C. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 2008, 455:903-911.
4. Chih B., et al. Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 2006, 51:171-178.
5. Koehnke J., et al. Splice form dependence of beta-neurexin/neuroligin binding interactions. Neuron 2010, 67:61-74.
6. Lee H., et al. Alternative splicing of neuroligin regulates the rate of presynaptic differentiation. J. Neurosci. 2010, 30:11435-11446.
7. Shipman S.L., Nicoll R.A. A subtype-specific function for the extracellular domain of neuroligin 1 in hippocampal LTP. Neuron 2012, 76:309-316.
8. Arikkath J., Reichardt L.F. Cadherins and catenins at synapses: roles in synaptogenesis and synaptic plasticity. Trends Neurosci. 2008, 31:487-494.
9. Biederer T., et al. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 2002, 297:1525-1531.
10. de Wit J., et al. LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation. Neuron 2009, 64:799-806.
11. Ko J., et al. LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation. Neuron 2009, 64:791-798.
12. Linhoff M.W., et al. An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers. Neuron 2009, 61:734-749.
13. Uemura T., et al. Trans-synaptic interaction of GluRdelta2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum. Cell 2010, 141:1068-1079.
14. Boucard A.A., et al. High affinity neurexin binding to cell adhesion G-protein-coupled receptor CIRL1/latrophilin-1 produces an intercellular adhesion complex. J. Biol. Chem. 2012, 287:9399-9413.
15. Woo J., et al. Trans-synaptic adhesion between NGL-3 and LAR regulates the formation of excitatory synapses. Nat. Neurosci. 2009, 12:428-437.
16. Mosca T.J., et al. Trans-synaptic Teneurin signalling in neuromuscular synapse organization and target choice. Nature 2012, 484:237-241.
17. Treutlein B., et al. Cartography of neurexin alternative splicing mapped by single-molecule long-read mRNA sequencing. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:E1291-E1299.
18. Ullrich B., et al. Cartography of neurexins: more than 1000 isoforms generated by alternative splicing and expressed in distinct subsets of neurons. Neuron 1995, 14:497-507.
19. Budreck E.C., Scheiffele P. Neuroligin-3 is a neuronal adhesion protein at GABAergic and glutamatergic synapses. Eur. J. Neurosci. 2007, 26:1738-1748.
20. Graf E.R., et al. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 2004, 119:1013-1026.
21. Song J.Y., et al. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:1100-1105.
22. Varoqueaux F., et al. Neuroligin 2 is exclusively localized to inhibitory synapses. Eur. J. Cell Biol. 2004, 83:449-456.
23. Chubykin A.A., et al. Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 2007, 54:919-931.
24. Shipman S.L., et al. Functional dependence of neuroligin on a new non-PDZ intracellular domain. Nat. Neurosci. 2011, 14:718-726.
25. Bolliger M.F., et al. Unusually rapid evolution of Neuroligin-4 in mice. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:6421-6426.
26. Hoon M., et al. Neuroligin-4 is localized to glycinergic postsynapses and regulates inhibition in the retina. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:3053-3058.
27. Suckow A.T., et al. Transcellular neuroligin-2 interactions enhance insulin secretion and are integral to pancreatic β cell function. J. Biol. Chem. 2012, 287:19816-19826.
28. Comoletti D., et al. Characterization of the interaction of a recombinant soluble neuroligin-1 with neurexin-1beta. J. Biol. Chem. 2003, 278:50497-50505.
29. Dean C., et al. Neurexin mediates the assembly of presynaptic terminals. Nat. Neurosci. 2003, 6:708-716.
30. 2+ interactions. Neuron 2007, 56:992-1003.
31. Comoletti D., et al. Synaptic arrangement of the neuroligin/beta-neurexin complex revealed by X-ray and neutron scattering. Structure 2007, 15:693-705.
32. Fabrichny I.P., et al. Structural analysis of the synaptic protein neuroligin and its beta-neurexin complex: determinants for folding and cell adhesion. Neuron 2007, 56:979-991.
33. Koehnke J., et al. Crystal structure of the extracellular cholinesterase-like domain from neuroligin-2. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:1873-1878.
34. Ko J., et al. Neuroligin-1 performs neurexin-dependent and neurexin-independent functions in synapse validation. EMBO J. 2009, 28:3244-3255.
35. Poulopoulos A., et al. Homodimerization and isoform-specific heterodimerization of neuroligins. Biochem. J. 2012, 446:321-330.
36. Shipman S.L., Nicoll R.A. Dimerization of postsynaptic neuroligin drives synaptic assembly via transsynaptic clustering of neurexin. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:19432-19437.
37. Tanaka H., et al. Higher-order architecture of cell adhesion mediated by polymorphic synaptic adhesion molecules neurexin and neuroligin. Cell Rep. 2012, 2:101-110.
38. Irie M., et al. Binding of neuroligins to PSD-95. Science 1997, 277:1511-1515.
39. Meyer G., et al. The complexity of PDZ domain-mediated interactions at glutamatergic synapses: a case study on neuroligin. Neuropharmacology 2004, 47:724-733.
40. Dresbach T., et al. Synaptic targeting of neuroligin is independent of neurexin and SAP90/PSD95 binding. Mol. Cell. Neurosci. 2004, 27:227-235.
41. Hirao K., et al. A novel multiple PDZ domain-containing molecule interacting with N-methyl-D-aspartate receptors and neuronal cell adhesion proteins. J. Biol. Chem. 1998, 273:21105-21110.
42. Iida J., et al. Synaptic scaffolding molecule is involved in the synaptic clustering of neuroligin. Mol. Cell. Neurosci. 2004, 27:497-508.
43. Sumita K., et al. Synaptic scaffolding molecule (S-SCAM) membrane-associated guanylate kinase with inverted organization (MAGI)-2 is associated with cell adhesion molecules at inhibitory synapses in rat hippocampal neurons. J. Neurochem. 2007, 100:154-166.
44. Poulopoulos A., et al. Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 2009, 63:628-642.
45. Giannone G., et al. Neurexin-1beta binding to neuroligin-1 triggers the preferential recruitment of PSD-95 versus gephyrin through tyrosine phosphorylation of neuroligin-1. Cell Rep. 2013, 3:1996-2007.
46. Harvey K., et al. The GDP-GTP exchange factor collybistin: an essential determinant of neuronal gephyrin clustering. J. Neurosci. 2004, 24:5816-5826.
47. Kins S., et al. Collybistin, a newly identified brain-specific GEF, induces submembrane clustering of gephyrin. Nat. Neurosci. 2000, 3:22-29.
48. Soykan T., et al. A conformational switch in collybistin determines the differentiation of inhibitory postsynapses. EMBO J. 2014, 33:2113-2133.
49. Papadopoulos T., Soykan T. The role of collybistin in gephyrin clustering at inhibitory synapses: facts and open questions. Front. Cell. Neurosci. 2011, 5:11.
50. Budreck E.C., et al. Neuroligin-1 controls synaptic abundance of NMDA-type glutamate receptors through extracellular coupling. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:725-730.
51. Blundell J., et al. Neuroligin-1 deletion results in impaired spatial memory and increased repetitive behavior. J. Neurosci. 2010, 30:2115-2129.
52. Lee K., et al. MDGAs interact selectively with neuroligin-2 but not other neuroligins to regulate inhibitory synapse development. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:336-341.
53. Pettem K.L., et al. Interaction between autism-linked MDGAs and neuroligins suppresses inhibitory synapse development. J. Cell Biol. 2013, 200:321-336.
54. Shen C., et al. Novel interactive partners of neuroligin 3: new aspects for pathogenesis of autism. J. Mol. Neurosci. 2015, 56:89-101.
55. Rosales C.R., et al. A cytoplasmic motif targets neuroligin-1 exclusively to dendrites of cultured hippocampal neurons. Eur. J. Neurosci. 2005, 22:2381-2386.
56. Bemben M.A., et al. CaMKII phosphorylation of neuroligin-1 regulates excitatory synapses. Nat. Neurosci. 2014, 17:56-64.
57. Peixoto R.T., et al. Transsynaptic signaling by activity-dependent cleavage of neuroligin-1. Neuron 2012, 76:396-409.
58. Suzuki K., et al. Activity-dependent proteolytic cleavage of neuroligin-1. Neuron 2012, 76:410-422.
59. Antonelli R., et al. Pin1-dependent signalling negatively affects GABAergic transmission by modulating neuroligin2/gephyrin interaction. Nat. Commun. 2014, 5:5066.
60. Jamain S., et al. Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat. Genet. 2003, 34:27-29.
61. Laumonnier F., et al. X-linked mental retardation and autism are associated with a mutation in the NLGN4 gene, a member of the neuroligin family. Am. J. Hum. Genet. 2004, 74:552-557.
62. Lawson-Yuen A., et al. Familial deletion within NLGN4 associated with autism and Tourette syndrome. Eur. J. Hum. Genet. 2008, 16:614-618.
63. Yan J., et al. Analysis of the neuroligin 4Y gene in patients with autism. Psychiatr. Genet. 2008, 18:204-207.
64. Yan J., et al. Analysis of the neuroligin 3 and 4 genes in autism and other neuropsychiatric patients. Mol. Psychiatry 2005, 10:329-332.
65. Etherton M.R., et al. An autism-associated point mutation in the neuroligin cytoplasmic tail selectively impairs AMPA receptor-mediated synaptic transmission in hippocampus. EMBO J. 2011, 30:2908-2919.
66. Bemben M.A., et al. Autism-associated mutation inhibits protein kinase C-mediated neuroligin-4X enhancement of excitatory synapses. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:2551-2556.
67. Chanda S., et al. Pathogenic mechanism of an autism-associated neuroligin mutation involves altered AMPA-receptor trafficking. Mol. Psychiatry 2015, Published online March 17, 2015. 10.1038/mp.2015.20.
68. Boucard A.A., et al. A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron 2005, 48:229-236.
69. Chih B., et al. Control of excitatory and inhibitory synapse formation by neuroligins. Science 2005, 307:1324-1328.
70. Dahlhaus R., et al. 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 2010, 20:305-322.
71. Hines R.M., et al. Synaptic imbalance, stereotypies, and impaired social interactions in mice with altered neuroligin 2 expression. J. Neurosci. 2008, 28:6055-6067.
72. Varoqueaux F., et al. Neuroligins determine synapse maturation and function. Neuron 2006, 51:741-754.
73. Fu Z., et al. Functional excitatory synapses in HEK293 cells expressing neuroligin and glutamate receptors. J. Neurophysiol. 2003, 90:3950-3957.
74. Scheiffele P., et al. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 2000, 101:657-669.
75. Tallafuss A., et al. Organization of central synapses by adhesion molecules. Eur. J. Neurosci. 2010, 32:198-206.
76. Varoqueaux F., et al. Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:9037-9042.
77. Lu W., et al. The cell-autonomous role of excitatory synaptic transmission in the regulation of neuronal structure and function. Neuron 2013, 78:433-439.
78. Comoletti D., et al. The Arg451Cys-neuroligin-3 mutation associated with autism reveals a defect in protein processing. J. Neurosci. 2004, 24:4889-4893.
79. Jedlicka P., et al. Neuroligin-1 regulates excitatory synaptic transmission, LTP and EPSP-spike coupling in the dentate gyrus in vivo. Brain Struct. Funct. 2013, 220:47-58.
80. Kerchner G.A., Nicoll R.A. Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat. Rev. Neurosci. 2008, 9:813-825.
81. Ichtchenko K., et al. Neuroligin 1: a splice site-specific ligand for beta-neurexins. Cell 1995, 81:435-443.
82. Hoffman R.C., et al. Structural characterization of recombinant soluble rat neuroligin 1: mapping of secondary structure and glycosylation by mass spectrometry. Biochemistry 2004, 43:1496-1506.
83. Tabuchi K., et al. A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science 2007, 318:71-76.
84. Zhang C., et al. A neuroligin-4 missense mutation associated with autism impairs neuroligin-4 folding and endoplasmic reticulum export. J. Neurosci. 2009, 29:10843-10854.
85. Kwon H.B., et al. Neuroligin-1-dependent competition regulates cortical synaptogenesis and synapse number. Nat. Neurosci. 2012, 15:1667-1674.
86. Chadman K.K., et al. Minimal aberrant behavioral phenotypes of neuroligin-3 R451C knockin mice. Autism Res. 2008, 1:147-158.
87. Etherton M., et al. Autism-linked neuroligin-3 R451C mutation differentially alters hippocampal and cortical synaptic function. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:13764-13769.
88. Stam C.J. Modern network science of neurological disorders. Nat. Rev. Neurosci. 2014, 15:683-695.