Neuroligins, synapse balance and neuropsychiatric disorders

Pharmacological Reports

Volumn 66, Issue 5, 2014, Pages 830-835

  Maćkowiak, Marzena ^a   Mordalska, Patrycja ^a   Wȩdzony, Krzysztof ^a  

^a INSTITUTE OF PHARMACOLOGY   (Poland)

Author keywords

Autism; Cell adhesion molecules; Neuroligin; Schizophrenia; Synapse

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; GLYCINE; NEUROLIGIN; NEUROLIGIN 1; NEUROLIGIN 2; NEUROLIGIN 3; NEUROLIGIN 4; UNCLASSIFIED DRUG; NERVE CELL ADHESION MOLECULE;

AUTISM; EXCITATORY SYNAPSE; GENE MUTATION; HUMAN; INHIBITORY SYNAPSE; MEMORY; MENTAL DISEASE; NEUROLIGIN 2 GENE; NEUROLIGIN 3 GENE; NEUROLIGIN 4 GENE; NONHUMAN; PROTEIN LOCALIZATION; REVIEW; SCHIZOPHRENIA; SOCIAL BEHAVIOR; SYNAPSE; ANIMAL; GENETICS; METABOLISM; MOUSE; MUTATION; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; HUMANS; MEMORY; MENTAL DISORDERS; MICE; MICE, TRANSGENIC; MUTATION; SOCIAL BEHAVIOR; SYNAPSES;

EID: 84903589902     PISSN: 22995684     EISSN: 22995684     Source Type: Journal    
DOI: 10.1016/j.pharep.2014.04.011     Document Type: Review

References (62)

1. T.C. Sudhof Neuroligins and neurexins link synaptic function to cognitive disease Nature 455 2008 903 911
2. K. Ichtchenko, T. Nguyen, and T.C. Sudhof Structures, alternative splicing, and neurexin binding of multiple neuroligins J Biol Chem 271 1996 2676 2682 (Pubitemid 26047882)
3. M.F. Lise, and A. El-Husseini The neuroligin and neurexin families: from structure to function at the synapse Cell Mol Life Sci 63 2006 1833 1849
4. N. Wittenmayer, C. Korber, H. Liu, T. Kremer, F. Varoqueaux, and E.R. Chapman et al. Postsynaptic Neuroligin1 regulates presynaptic maturation Proc Natl Acad Sci U S A 106 2009 13564 13569
5. J.N. Levinson, and A. El-Husseini Building excitatory and inhibitory synapses: balancing neuroligin partnerships Neuron 48 2005 171 174 (Pubitemid 41476351)
6. B. Chih, H. Engelman, and P. Scheiffele Control of excitatory and inhibitory synapse formation by neuroligins Science 307 2005 1324 1328 (Pubitemid 40299984)
7. F. Varoqueaux, G. Aramuni, R.L. Rawson, R. Mohrmann, M. Missler, and K. Gottmann et al. Neuroligins determine synapse maturation and function Neuron 51 2006 741 754 (Pubitemid 44374915)
8. J.Y. Song, K. Ichtchenko, T.C. Sudhof, and N. Brose Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses Proc Natl Acad Sci U S A 96 1999 1100 1105 (Pubitemid 29072190)
9. E.R. Graf, X. Zhang, S.X. Jin, M.W. Linhoff, and A.M. Craig Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins Cell 119 2004 1013 1026 (Pubitemid 40037614)
10. E.C. Budreck, and P. Scheiffele Neuroligin-3 is a neuronal adhesion protein at GABAergic and glutamatergic synapses Eur J Neurosci 26 2007 1738 1748 (Pubitemid 47493212)
11. F. Varoqueaux, S. Jamain, and N. Brose Neuroligin 2 is exclusively localized to inhibitory synapses Eur J Cell Biol 83 2004 449 456 (Pubitemid 39433525)
12. M. Hoon, G. Bauer, J.M. Fritschy, T. Moser, B.H. Falkenburger, and F. Varoqueaux Neuroligin 2 controls the maturation of GABAergic synapses and information processing in the retina J Neurosci 29 2009 8039 8050
13. A. Poulopoulos, G. Aramuni, G. Meyer, T. Soykan, M. Hoon, and T. Papadopoulos et al. Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin Neuron 63 2009 628 642
14. N. Dong, J. Qi, and G. Chen Molecular reconstitution of functional GABAergic synapses with expression of neuroligin-2 and GABAA receptors Mol Cell Neurosci 35 2007 14 23 (Pubitemid 46636296)
15. M. Hoon, T. Soykan, B. Falkenburger, M. Hammer, A. Patrizi, and K.F. Schmidt et al. Neuroligin-4 is localized to glycinergic postsynapses and regulates inhibition in the retina Proc Natl Acad Sci U S A 108 2011 3053 3058
16. J. Schummers, J. Marino, and M. Sur Synaptic integration by V1 neurons depends on location within the orientation map Neuron 36 2002 969 978 (Pubitemid 35447867)
17. O. Prange, T.P. Wong, K. Gerrow, Y.T. Wang, and A. El-Husseini A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin Proc Natl Acad Sci U S A 101 2004 13915 13920 (Pubitemid 39298507)
18. R. Dahlhaus, R.M. Hines, B.D. Eadie, T.S. Kannangara, D.J. Hines, and C.E. Brown 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 20 2010 305 322
19. J. Blundell, C.A. Blaiss, M.R. Etherton, F. Espinosa, K. Tabuchi, and C. Walz et al. Neuroligin-1 deletion results in impaired spatial memory and increased repetitive behavior J Neurosci 30 2010 2115 2129
20. R.M. Hines, L. Wu, D.J. Hines, H. Steenland, S. Mansour, and R. Dahlhaus et al. Synaptic imbalance, stereotypies, and impaired social interactions in mice with altered neuroligin 2 expression J Neurosci 28 2008 6055 6067
21. B. Chih, S.K. Afridi, L. Clark, and P. Scheiffele Disorder-associated mutations lead to functional inactivation of neuroligins Hum Mol Genet 13 2004 1471 1477 (Pubitemid 39023055)
22. J.N. Levinson, N. Chery, K. Huang, T.P. Wong, K. Gerrow, and R. Kang et al. Neuroligins mediate excitatory and inhibitory synapse formation: involvement of PSD-95 and neurexin-1beta in neuroligin-induced synaptic specificity J Biol Chem 280 2005 17312 17319 (Pubitemid 41389200)
23. M. Irie, Y. Hata, M. Takeuchi, K. Ichtchenko, A. Toyoda, and K. Hirao et al. Binding of neuroligins to PSD-95 Science 277 1997 1511 1515 (Pubitemid 27449240)
24. K. Futai, M.J. Kim, T. Hashikawa, P. Scheiffele, M. Sheng, and Y. Hayashi Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin Nat Neurosci 10 2007 186 195 (Pubitemid 46174843)
25. K. Gerrow, S. Romorini, S.M. Nabi, M.A. Colicos, C. Sala, and A. El-Husseini A preformed complex of postsynaptic proteins is involved in excitatory synapse development Neuron 49 2006 547 562 (Pubitemid 43221890)
26. J.N. Levinson, R. Li, R. Kang, H. Moukhles, A. El-Husseini, and S.X. Bamji Postsynaptic scaffolding molecules modulate the localization of neuroligins Neuroscience 165 2010 782 793
27. C. Sun, L. Zhang, and G. Chen An unexpected role of neuroligin-2 in regulating KCC2 and GABA functional switch Mol Brain 6 2013 23
28. P. Blaesse, M.S. Airaksinen, C. Rivera, and K. Kaila Cation-chloride cotransporters and neuronal function Neuron 61 2009 820 838
29. H. Li, S. Khirug, C. Cai, A. Ludwig, P. Blaesse, and J. Kolikova et al. KCC2 interacts with the dendritic cytoskeleton to promote spine development Neuron 56 2007 1019 1033 (Pubitemid 350251117)
30. K.B. Hoover, and P.J. Bryant The genetics of the protein 4.1 family: organizers of the membrane and cytoskeleton Curr Opin Cell Biol 12 2000 229 234 (Pubitemid 30142571)
31. A.A. Chubykin, D. Atasoy, M.R. Etherton, N. Brose, E.T. Kavalali, and J.R. Gibson et al. Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2 Neuron 54 2007 919 931 (Pubitemid 46907504)
32. K. Wedzony, A. Chocyk, and M. Mackowiak Potential roles of NCAM/PSA-NCAM proteins in depression and the mechanism of action of antidepressant drugs Pharmacol Rep 65 2013 1471 1478
33. R. Grzadzinski, M. Huerta, and C. Lord DSM-5 and autism spectrum disorders (ASDs): an opportunity for identifying ASD subtypes Mol Autism 4 2013 12
34. S. Jamain, H. Quach, C. Betancur, M. Rastam, C. Colineaux, and I.C. Gillberg et al. Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism Nat Genet 34 2003 27 29 (Pubitemid 36548785)
35. F. Laumonnier, F. Bonnet-Brilhault, M. Gomot, R. Blanc, A. David, and M.P. Moizard 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 74 2004 552 557 (Pubitemid 38325925)
36. A. Lawson-Yuen, J.S. Saldivar, S. Sommer, and J. Picker Familial deletion within NLGN4 associated with autism and Tourette syndrome Eur J Hum Genet 16 2008 614 618 (Pubitemid 351594128)
37. Z. Talebizadeh, D.Y. Lam, M.F. Theodoro, D.C. Bittel, G.H. Lushington, and M.G. Butler Novel splice isoforms for NLGN3 and NLGN4 with possible implications in autism J Med Genet 43 2006 e21
38. J. Yan, G. Oliveira, A. Coutinho, C. Yang, J. Feng, and C. Katz et al. Analysis of the neuroligin 3 and 4 genes in autism and other neuropsychiatric patients Mol Psychiatry 10 2005 329 332
39. J. Yan, J. Feng, R. Schroer, W. Li, C. Skinner, and C.E. Schwartz et al. Analysis of the neuroligin 4Y gene in patients with autism Psychiatr Genet 18 2008 204 207
40. L. Shi, X. Chang, P. Zhang, M.P. Coba, W. Lu, and K. Wang The functional genetic link of NLGN4X knockdown and neurodevelopment in neural stem cells Hum Mol Genet 22 2013 3749 3760
41. H. Won, W. Mah, and E. Kim Autism spectrum disorder causes, mechanisms, and treatments: focus on neuronal synapses Front Mol Neurosci 6 2013 19
42. J. Kim, S.Y. Jung, Y.K. Lee, S. Park, J.S. Choi, and C.J. Lee et al. 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 2008 9087 9092
43. J. Blundell, K. Tabuchi, M.F. Bolliger, C.A. Blaiss, N. Brose, and X. Liu et al. Increased anxiety-like behavior in mice lacking the inhibitory synapse cell adhesion molecule neuroligin 2 Genes Brain Behav 8 2009 114 126
44. M. Wohr, J.L. Silverman, M.L. Scattoni, S.M. Turner, M.J. Harris, and R. Saxena et al. Developmental delays and reduced pup ultrasonic vocalizations but normal sociability in mice lacking the postsynaptic cell adhesion protein neuroligin2 Behav Brain Res 251 2013 50 64
45. C. Kohl, O. Riccio, J. Grosse, O. Zanoletti, C. Fournier, and M.V. Schmidt et al. Hippocampal neuroligin-2 overexpression leads to reduced aggression and inhibited novelty reactivity in rats PLoS One 8 2013 e56871
46. M.A. van der Kooij, M. Fantin, I. Kraev, I. Korshunova, J. Grosse, and O. Zanoletti et al. Impaired hippocampal neuroligin-2 function by chronic stress or synthetic peptide treatment is linked to social deficits and increased aggression Neuropsychopharmacology 39 2014 1148 1158
47. K. Radyushkin, K. Hammerschmidt, S. Boretius, F. Varoqueaux, A. El-Kordi, and A. Ronnenberg et al. Neuroligin-3-deficient mice: model of a monogenic heritable form of autism with an olfactory deficit Genes Brain Behav 8 2009 416 425
48. D. Comoletti, J.A. De, L.L. Jennings, R.E. Flynn, G. Gaietta, and I. Tsigelny et al. The Arg451Cys-neuroligin-3 mutation associated with autism reveals a defect in protein processing J Neurosci 24 2004 4889 4893 (Pubitemid 38668214)
49. K. Tabuchi, J. Blundell, M.R. Etherton, R.E. Hammer, X. Liu, and C.M. Powell et al. A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice Science 318 2007 71 76 (Pubitemid 47538032)
50. M. Etherton, C. Foldy, M. Sharma, K. Tabuchi, X. Liu, and M. Shamloo et al. Autism-linked neuroligin-3 R451C mutation differentially alters hippocampal and cortical synaptic function Proc Natl Acad Sci U S A 108 2011 13764 13769
51. R. Pizzarelli, and E. Cherubini Developmental regulation of GABAergic signalling in the hippocampus of neuroligin 3 R451C knock-in mice: an animal model of Autism Front Cell Neurosci 7 2013 85
52. M.R. Etherton, K. Tabuchi, M. Sharma, J. Ko, and T.C. Sudhof 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
53. S.A. McMahon, and E. Diaz Mechanisms of excitatory synapse maturation by trans-synaptic organizing complexes Curr Opin Neurobiol 21 2011 221 227
54. S. Jamain, K. Radyushkin, K. Hammerschmidt, S. Granon, S. Boretius, and F. Varoqueaux et al. Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism Proc Natl Acad Sci U S A 105 2008 1710 1715 (Pubitemid 351346579)
55. S.H. Fatemi, and T.D. Folsom The neurodevelopmental hypothesis of schizophrenia, revisited Schizophr Bull 35 2009 528 548
56. D.A. Lewis, and G. Gonzalez-Burgos Neuroplasticity of neocortical circuits in schizophrenia Neuropsychopharmacology 33 2008 141 165 (Pubitemid 350191315)
57. P.F. Sullivan, K.S. Kendler, and M.C. Neale Schizophrenia as a complex trait: evidence from a meta-analysis of twin studies Arch Gen Psychiatry 60 2003 1187 1192 (Pubitemid 37494071)
58. C. Sun, M.C. Cheng, R. Qin, D.L. Liao, T.T. Chen, and F.J. Koong et al. Identification and functional characterization of rare mutations of the neuroligin-2 gene (NLGN2) associated with schizophrenia Hum Mol Genet 20 2011 3042 3051
59. P. Sand, B. Langguth, G. Hajak, M. Perna, R. Prikryl, and H. Kucerova et al. Screening for Neuroligin 4 (NLGN4) truncating and transmembrane domain mutations in schizophrenia Schizophr Res 82 2006 277 278 (Pubitemid 43290695)
60. A.C. Lionel, A.K. Vaags, D. Sato, M.J. Gazzellone, E.B. Mitchell, and H.Y. Chen et al. Rare exonic deletions implicate the synaptic organizer Gephyrin (GPHN) in risk for autism, schizophrenia and seizures Hum Mol Genet 22 2013 2055 2066
61. P. Mordalska, E. Bator, M. Maćkowiak, and K. Wedzony Impairment of synaptic adhesion molecule expression in the medial prefrontal cortex in the neurodevelopmental model of schizophrenia Eur Neuropsychopharmacol 21 2011 S191
62. B.B. Sheitman, J.E. Kraus, J.W. Bodfish, and H. Carmel Are the negative symptoms of schizophrenia consistent with an autistic spectrum illness? Schizophr Res 69 2004 119 120 (Pubitemid 38625765)