Synapse formation and clustering of neuroligin-2 in the absence of GABAa receptors

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 35, 2008, Pages 13151-13156

  Patrizi, Annarita ^a   Scelfo, Bibiana ^b   Viltono, Laura ^a   Briatore, Federica ^a   Fukaya, Masahiro ^c   Watanabe, Masahiko ^c   Strata, Piergiorgio ^c,d   Varoqueaux, Frédérique ^e   Brose, Nils ^e   Fritschy, Jean Marc ^f   Sassoè Pognetto, Marco ^a  

^a National Institute of Neuroscience Italy   (Italy)

^b National Institute of Neuroscience INN   (Italy)

^c HOKKAIDO UNIVERSITY   (Japan)

^d EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^e MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^f UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Gephyrin; Purkinje cell; Synaptogenesis

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; GEPHYRIN; NEUROLIGIN; NEUROLIGIN 2; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; KNOCKOUT MOUSE; MOUSE; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PURKINJE CELL; SYNAPSE; SYNAPTOGENESIS;

ANIMALS; DENDRITIC SPINES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; PROTEIN TRANSPORT; PURKINJE CELLS; RECEPTORS, GABA-A; SYNAPSES;

MUS;

EID: 51349129758     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0802390105     Document Type: Article

References (48)

1. Waites CL, Craig AM, Garner CC (2005) Mechanisms of vertebrate synaptogenesis. Annu Rev Neurosci 28:251-274.
2. Craig AM, Graf ER, Linhoff MW (2006) How to build a central synapse: Clues from cell culture. Trends Neurosci 29:8-20.
3. Dudanova I, Tabuchi K, Rohlmann A, Sudhof TC, Missler M (2007) Deletion of alpha-neurexins does not cause a major impairment of axonal pathfinding or synapse formation. J Comp Neurol 502:261-274.
4. Verhage M, et al. (2000) Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287:864-869.
5. Varoqueaux F, et al. (2002) Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc Natl Acad Sci USA 99:9037-9042.
6. Varoqueaux F, et al. (2006) Neuroligins determine synapse maturation and function. Neuron 51:741-754.
7. 2+ channels to synaptic vesicle exocytosis. Nature 423:939-948.
8. Wojcik SM, et al. (2006) A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron 50:575-587.
9. Farrant M, Nusser Z (2005) Variations on an inhibitory theme: Phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6:215-229.
10. Graf ER, Zhang X, Jin SX, Linhoff MW, Craig AM (2004) Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119:1013-1026.
11. Varoqueaux F, Jamain S, Brose N (2004) Neuroligin 2 is exclusively localized to inhibitory synapses. Eur J Cell Biol 83:449-456.
12. Ichtchenko K, et al. (1995) Neuroligin 1: A splice site-specific ligand for beta-neurexins. Cell 81:435-443.
13. Song JY, Ichtchenko K, Sudhof TC, Brose N (1999) Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc Natl Acad Sci USA 96:1100-1105.
14. Scheiffele P, Fan J, Choih J, Fetter R, Serafini T (2000) Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101:657-669.
15. Levinson JN, El-Husseini A (2005) Building excitatory and inhibitory synapses: Balancing neuroligin partnerships. Neuron 48:171-174.
16. Chubykin AA, et al. (2007) Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 54:919-931.
17. Chih B, Gollan L, Scheiffele P (2006) Alternative splicing controls selective transsynaptic interactions of the neuroligin-neurexin complex. Neuron 51:171-178.
18. Graf ER, Kang Y, Hauner AM, Craig AM (2006) Structure function and splice site analysis of the synaptogenic activity of the neurexin-1 beta LNS domain. J Neurosci 26:4256-4265.
19. Luscher B, Keller CA (2004) Regulation of GABAA receptor trafficking, channel activity, and functional plasticity of inhibitory synapses. Pharmacol Ther 102:195-221.
20. Kralic JE, et al. (2005) Genetic essential tremor in gamma-aminobutyric acidA receptor alpha1 subunit knockout mice. J Clin Invest 115:774-779.
21. Fritschy JM, Panzanelli P, Kralic JE, Vogt KE, Sassoe-Pognetto M (2006) Differential dependence of axo-dendritic and axo-somatic GABAergic synapses on GABAA receptors containing the alpha1 subunit in Purkinje cells. J Neurosci 26:3245-3255.
22. Kralic JE, et al. (2006) Compensatory alteration of inhibitory synaptic circuits in cerebellum and thalamus of gamma-aminobutyric acid type A receptor alpha1 subunit knockout mice. J Comp Neurol 495:408-421.
23. Tanaka J, et al. (2000) Gq protein alpha subunits Galphaq and Galpha11 are localized at postsynaptic extra-junctional membrane of cerebellar Purkinje cells and hippocampal pyramidal cells. Eur J Neurosci 12:781-792.
24. Altman J (1972) Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J Comp Neurol 145:399-463.
25. Laurie DJ, Seeburg PH, Wisden W (1992) The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. II. Olfactory bulb and cerebellum. J Neurosci 12:1063-1076.
26. Takayama C, Inoue Y (2004) Transient expression of GABAA receptor alpha2 and alpha3 subunits in differentiating cerebellar neurons. Brain Res Dev Brain Res 148:169-177.
27. Vicini S, et al. (2001) GABA(A) receptor alpha1 subunit deletion prevents developmental changes of inhibitory synaptic currents in cerebellar neurons. J Neurosci 21:3009-3016.
28. Vicini S, Ortinski P (2004) Genetic manipulations of GABAA receptor in mice make inhibition exciting. Pharmacol Ther 103:109-120.
29. Lagier S, et al. (2007) GABAergic inhibition at dendrodendritic synapses tunes gamma oscillations in the olfactory bulb. Proc Natl Acad Sci USA 104:7259-7264.
30. Goldstein PA, et al. (2002) Prolongation of hippocampal miniature inhibitory postsynaptic currents in mice lacking the GABA(A) receptor alpha1 subunit. J Neurophysiol 88:3208-3217.
31. Missias AC, et al. (1997) Deficient development and maintenance of postsynaptic specializations in mutant mice lacking an 'adult' acetylcholine receptor subunit. Development (Cambridge, UK) 124:5075-5086.
32. Rutherford LC, DeWan A, Lauer HM, Turrigiano GG (1997) Brain-derived neurotrophic factor mediates the activity-dependent regulation of inhibition in neocortical cultures. J Neurosci 17:4527-4535.
33. Seil FJ, Drake-Baumann R (2000) TrkB receptor ligands promote activity-dependent inhibitory synaptogenesis. J Neurosci 20:5367-5373.
34. Hartman KN, Pal SK, Burrone J, Murthy VN (2006) Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons. Nat Neurosci 9:642-649.
35. Li RW, et al. (2005) Disruption of postsynaptic GABA receptor clusters leads to decreased GABAergic innervation of pyramidal neurons. J Neurochem 95:756-770.
36. Fang C, et al. (2006) GODZ-mediated palmitoylation of GABA(A) receptors is required for normal assembly and function of GABAergic inhibitory synapses. J Neurosci 26:12758-12768.
37. Chattopadhyaya B, et al. (2007) GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 54:889-903.
38. Wu Y, Wang W, Diez-Sampedro A, Richerson GB (2007) Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 56:851-865.
39. Lichtman JW, Colman H (2000) Synapse elimination and indelible memory. Neuron 25:269-278.
40. Huang ZJ, et al. (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98:739-755.
41. Marty S, Wehrle R, Sotelo C (2000) Neuronal activity and brain-derived neurotrophic factor regulate the density of inhibitory synapses in organotypic slice cultures of postnatal hippocampus. J Neurosci 20:8087-8095.
42. Rico B, Xu B, Reichardt LF (2002) TrkB receptor signaling is required for establishment of GABAergic synapses in the cerebellum. Nat Neurosci 5:225-233.
43. Stevens B, et al. (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131:1164-1178.
44. Huang ZJ, Scheiffele P (2008) GABA and neuroligin signaling: Linking synaptic activity and adhesion in inhibitory synapse development. Curr Opin Neurobiol 18:1-7.
45. Sugita S, et al. (2002) A stoichiometric complex of neurexins and dystroglycan in brain. J Cell Biol 154:435-445.
46. Sumita K, et al. (2007) 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 100:154-166.
47. Lévi S, et al. (2002) Dystroglycan is selectively associated with inhibitory GABAergic synapses but is dispensable for their differentiation. J Neurosci 22:4274-4285.
48. Schneider Gasser EM, et al. (2006) Immunofluorescence in brain sections: Simultaneous detection of presynaptic and postsynaptic proteins in identified neurons. Nat Protoc 1:1887-1897.