Asynchronous GABA release is a key determinant of tonic inhibition and controls neuronal excitability: A study in the synapsin II-/- mouse

Cerebral Cortex

Volumn 25, Issue 10, 2015, Pages 3356-3368

  Medrihan, Lucian ^a   Ferrea, Enrico ^a   Greco, Barbara ^a   Baldelli, Pietro ^a,b   Benfenati, Fabio ^a,b  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

Author keywords

Asynchronous; Epilepsy; GABA; Synapsin; Tonic

Indexed keywords

4 AMINOBUTYRIC ACID; GABOXADOL; SYNAPSIN II; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; ISOXAZOLE DERIVATIVE; SYNAPSIN;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLONIC SEIZURE; CONTROLLED STUDY; DISEASE PREDISPOSITION; EPILEPSY; EPILEPTOGENESIS; GENE DELETION; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLECULAR DYNAMICS; MOUSE; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NONHUMAN; PHENOTYPE; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; TONIC SEIZURE; ACTION POTENTIAL; ANIMAL; C57BL MOUSE; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; KNOCKOUT MOUSE; NERVE CELL INHIBITION; PATHOPHYSIOLOGY; PHYSIOLOGY; SEIZURE;

ACTION POTENTIALS; ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA AGONISTS; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIALS; ISOXAZOLES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURAL INHIBITION; NEURONS; SEIZURES; SYNAPSINS;

EID: 84948657333     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu141     Document Type: Article

References (70)

1. Atluri PP, Regehr WG. 1998. Delayed release of neurotransmitter from cerebellar granule cells. J Neurosci. 18:8214-8227.
2. Avoli M, de Curtis M. 2011. GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity. Prog Neurobiol. 95:104-132.
3. Balakrishnan V, Kuo SP, Roberts PD, Trussell LO. 2009. Slow glyciner-gic transmission mediated by transmitter pooling. Nat Neurosci. 12:286-294.
4. Baldelli P, Fassio A, Valtorta F, Benfenati F. 2007. Lack of synapsin I reduces the readily releasable pool of synaptic vesicles at central inhibitory synapses. J Neurosci. 27:13520-13531.
5. Bialer M, Johannessen SI, Levy RH, Perucca E, Tomson T, White HS. 2010. Progress report on new antiepileptic drugs: a summary of the Tenth Eilat Conference (EILAT X). Epilepsy Res. 92:89-124.
6. Bogen IL, Jensen V, Hvalby O, Walaas SI. 2009. Synapsin-dependent development of glutamatergic synaptic vesicles and presynaptic plasticity in postnatal mouse brain. Neuroscience. 158(1):231-241.
7. Boido D, Farisello P, Cesca F, Ferrea E, Valtorta F, Benfenati F, Baldelli P. 2010. Cortico-hippocampal hyperexcitability in synapsin I/II/III knockout mice: age-dependency and response to levitiracetam. Neuroscience. 171:268-283.
8. A receptor-mediated inhibition. Front Neural Circuits. 7:193.
9. Burgoyne RD, Barclay JW, Ciufo LF, Graham ME, Handley MT, Morgan A. 2009. The functions of Munc18-1 in regulated exocytosis. Ann N Y Acad Sci. 1152:76-86.
10. Capogna M, Pearce RA. 2011. GABA A, slow: causes and consequences. Trends Neurosci. 34:101-112.
11. Cavalleri GL, Weale ME, Shianna KV, Singh R, Lynch JM, Grinton B, Szoeke C, Murphy K, Kinirons P, O'Rourke D et al. 2007. Multicen-tre search for genetic susceptibility loci in sporadic epilepsy syndrome and seizure types: a case-control study. Lancet Neurol. 6:970-980.
12. Cesca F, Baldelli P, Valtorta F, Benfenati F. 2010. The synapsins: key actors of synapse function and plasticity. Prog Neurobiol. 91: 313-348.
13. Ciufo LF, Barclay JW, Burgoyne RD, Morgan A. 2005. Munc18-1 regulates early and late stages of exocytosis via syntaxin-independent protein interactions. Mol Biol Cell. 16:470-482.
14. Corradi A, Fadda M, Piton A, Patry L, Marte A, Rossi P, Cadieux-Dion M, Gauthier J, Lapointe L, Mottron L et al. 2014. SYN2 is an autism predisposing gene: loss-of-function mutations alter synaptic vesicle cycling and axon outgrowth. Hum Mol Genet. 23:90-103.
15. Corradi A, Zanardi A, Giacomini C, Onofri F, Valtorta F, Zoli M, Benfenati F. 2008. Synapsin-I-and synapsin-II-null mice display an increased age-dependent cognitive impairment. J Cell Sci. 121: 3042-3051.
16. Cremers T, Ebert B. 2007. Plasma and CNS concentrations of gaboxa-dol in rats following subcutaneous administration. Eur J Pharmacol. 562:47-52.
17. Crowder KM, Gunther JM, Jones TA, Hale BD, Zhang HZ, Peterson MR, Scheller RH, Chavkin C, Bajjalieh SM. 1999. Abnormal neurotrans-mission in mice lacking synaptic vesicle protein 2A (SV2A). Proc Natl Acad Sci USA. 96:15268-15273.
18. A receptors is a susceptibility locus for generalized epilepsies. Hum Mol Genet. 13:1315-1319.
19. Etholm L, Bahonjic E, Walaas SI, Kao HT, Heggelund P. 2012. Neuroetho-logically delineated differences in the seizure behavior of Synapsin 1 and Synapsin 2 knock-out mice. Epilepsy Res. 99:252-259.
20. Fang Q, Chen Z. 2012. Increased asynchronous GABA release causes more inhibition in human epileptic brain? Acta Pharmacol Sin. 33: 859-860.
21. Farisello P, Boido D, Nieus T, Medrihan L, Cesca F, Valtorta F, Baldelli P, Benfenati F. 2013. Synaptic and extrasynaptic origin of the excitation/inhibition imbalance in the hippocampus of synapsin I/II/III knockout mice. Cereb Cortex. 23:581-593.
22. Farrant M, Nusser Z. 2005. Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci. 6: 215-229.
23. Fassio A, Patry L, Congia S, Onofri F, Piton A, Gauthier J, Pozzi D, Messa M, Defranchi E, Fadda M et al. 2011. SYN1 loss-of-function mutations in autism and partial epilepsy cause impaired synaptic function. Hum Mol Genet. 20:2297-2307.
24. Feng G, Xiao F, Lu Y, Huang Z, Yuan J, Xiao Z, Xi Z, Wang X. 2009. Down-regulation synaptic vesicle protein 2A in the anterior temporal neocortex of patients with intractable epilepsy. J Mol Neuros-ci. 39:354-359.
25. A receptor modulation by neurosteroids in models of temporal lobe epilepsies. Epilepsia. 53(Suppl 9): 89-101.
26. Ferrea E, Maccione A, Medrihan L, Nieus T, Ghezzi D, Baldelli P, Benfe-nati F, Berdondini L. 2012. Large-scale, high-resolution electro-physiological imaging of field potentials in brain slices with microelectronic multielectrode arrays. Front Neural Circuits. 6:80.
27. Garcia CC, Blair HJ, Seager M, Coulthard A, Tennant S, Buddles M, Curtis A, Goodship JA. 2004. Identification of a mutation in synap-sin I, a synaptic vesicle protein, in a family with epilepsy. J Med Genet. 41:183-186.
28. Gerber SH, Rah JC, Min SW, Liu X, de Wit H, Dulubova I, Meyer AC, Rizo J, Arancillo M, Hammer RE et al. 2008. Conformational switch of syntaxin-1 controls synaptic vesicle fusion. Science. 321: 1507-1510.
29. Gitler D, Takagishi Y, Feng J, Ren Y, Rodriguiz RM, Wetsel WC, Greengard P, Augustine GJ. 2004. Different presynaptic roles of synapsins at excitatory and inhibitory synapses. J Neurosci. 24: 11368-11380.
30. A receptor alpha5 subunit-deficient mice. J Neurophysiol. 95:2796-2807.
31. Goda Y, Stevens CF. 1994. Two components of transmitter release at a central synapse. Proc Natl Acad Sci USA. 91:12942-12946.
32. Greco B, Manago F, Tucci V, Kao HT, Valtorta F, Benfenati F. 2013. Autism-related behavioral abnormalities in synapsin knockout mice. Behav Brain Res. 251:65-74.
33. Hamdan FF, Piton A, Gauthier J, Lortie A, Dubeau F, Dobrzeniecka S, Spiegelman D, Noreau A, Pellerin S, Cote M et al. 2009. De novo STXBP1 mutations in mental retardation and nonsyndromic epilepsy. Ann Neurol. 65:748-753.
34. Harrison V, Connell L, Hayesmoore J, McParland J, Pike MG, Blair E. 2011. Compound heterozygous deletion of NRXN1 causing severe developmental delay with early onset epilepsy in two sisters. Am J Med Genet A. 155A:2826-2831.
35. Hata Y, Sudhof TC. 1995. A novel ubiquitous form of Munc-18 interacts with multiple syntaxins. Use of the yeast two-hybrid system to study interactions between proteins involved in membrane traffic. J Biol Chem. 270:13022-13028.
36. Hefft S, Jonas P. 2005. Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci. 8:1319-1328.
37. Holter NI, Zylla MM, Zuber N, Bruehl C, Draguhn A. 2010. Tonic GA-BAergic control of mouse dentate granule cells during postnatal development. Eur J Neurosci. 32:1300-1309.
38. Jiang M, Zhu J, Liu Y, Yang M, Tian C, Jiang S, Wang Y, Guo H, Wang K, Shu Y. 2012. Enhancement of asynchronous release from fast-spiking interneuron in human and rat epileptic neocortex. PLoS Biol. 10:e1001324.
39. Lakhan R, Kalita J, Misra UK, Kumari R, Mittal B. 2010. Association of intronic polymorphism rs3773364 A>G in synapsin-2 gene with idiopathic epilepsy. Synapse. 64:403-408.
40. A receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci. 12:4151-4172.
41. Li L, Chin LS, Shupliakov O, Brodin L, Sihra TS, Hvalby O, Jensen V, Zheng D, McNamara JO, Greengard P et al. 1995. Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice. Proc Natl Acad Sci USA. 92:9235-9239.
42. Lignani G, Raimondi A, Ferrea E, Rocchi A, Paonessa F, Cesca F, Orlando M, Tkatch T, Valtorta F, Cossette P et al. 2013. Epileptogen-ic Q555X SYN1 mutant triggers imbalances in release dynamics and short-term plasticity. Hum Mol Genet. 22:2186-2199.
43. Lynch BA, Lambeng N, Nocka K, Kensel-Hammes P, Bajjalieh SM, Matagne A, Fuks B. 2004. The synaptic vesicle protein SV2A is the binding site for the antiepileptic drug levetiracetam. Proc Natl Acad Sci USA. 101:9861-9866.
44. Maccione A, Gandolfo M, Massobrio P, Novellino A, Martinoia S, Chiappalone M. 2009. A novel algorithm for precise identification of spikes in extracellularly recorded neuronal signals. J Neurosci Methods. 177:241-249.
45. Manseau F, Marinelli S, Mendez P, Schwaller B, Prince DA, Huguenard JR, Bacci A. 2010. Desynchronization of neocortical networks by asynchronous release of GABA at autaptic and synaptic contacts from fast-spiking interneurons. PLoS Biol. 8:e1000492.
46. Medrihan L, Cesca F, Raimondi A, Lignani G, Baldelli P, Benfenati F. 2013. Synapsin II desynchronizes neurotransmitter release at inhibitory synapses by interacting with presynaptic calcium channels. Nat Commun. 4:1512.
47. Milh M, Villeneuve N, Chouchane M, Kaminska A, Laroche C, Barthez MA, Gitiaux C, Bartoli C, Borges-Correia A, Cacciagli P et al. 2011. Epileptic and nonepileptic features in patients with early onset epileptic encephalopathy and STXBP1 mutations. Epilepsia. 52: 1828-1834.
48. 2+ channels to synaptic vesicle exocytosis. Nature. 423:939-948.
49. Mitchell SJ, Silver RA. 2003. Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron. 38:433-445.
50. Mody I, Pearce RA. 2004. Diversity of inhibitory neurotransmission through GABA(A) receptors. Trends Neurosci. 27:569-575.
51. Morrison RS, Wenzel HJ, Kinoshita Y, Robbins CA, Donehower LA, Schwartzkroin PA. 1996. Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J Neurosci. 16:1337-1345.
52. Nusser Z, Mody I. 2002. Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol. 87:2624-2628.
53. A receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci. 18:1693-1703.
54. Otsuka M, Oguni H, Liang JS, Ikeda H, Imai K, Hirasawa K, Tachikawa E, Shimojima K, Osawa M, Yamamoto T. 2010. STXBP1 mutations cause not only Ohtahara syndrome but also West syndrome-result of Japanese cohort study. Epilepsia. 51:2449-2452.
55. 2+-triggered exocytosis. Curr Opin Cell Biol. 22:496-505.
56. Pavlov I, Walker MC. 2013. Tonic GABA(A) receptor-mediated signalling in temporal lobe epilepsy. Neuropharmacology. 69:55-61.
57. Poduri A, Lowenstein D. 2011. Epilepsy genetics-past, present, and future. Curr Opin Genet Dev. 21:325-332.
58. Rosahl TW, Spillane D, Missler M, Herz J, Selig DK, Wolff JR, Hammer RE, Malenka RC, Sudhof TC. 1995. Essential functions of synapsins I and II in synaptic vesicle regulation. Nature. 375:488-493.
59. Saitsu H, Kato M, Mizuguchi T, Hamada K, Osaka H, Tohyama J, Uruno K, Kumada S, Nishiyama K, Nishimura A et al. 2008. De novo mutations in the gene encoding STXBP1 (MUNC18-1) cause early infantile epileptic encephalopathy. Nat Genet. 40:782-788.
60. Schivell AE, Mochida S, Kensel-Hammes P, Custer KL, Bajjalieh SM. 2005. SV2A and SV2C contain a unique synaptotagmin-binding site. Mol Cell Neurosci. 29:56-64.
61. Semyanov A, Walker MC, Kullmann DM, Silver RA. 2004. Tonically active GABA A receptors: modulating gain and maintaining the tone. Trends Neurosci. 27:262-269.
62. A-receptor delta subunit. Epilepsia. 43(Suppl 5):3-8.
63. Toader O, Forte N, Orlando M, Ferrea E, Raimondi A, Baldelli P, Benfe-nati F, Medrihan L. 2013. Dentate gyrus network dysfunctions precede the symptomatic phase in a genetic mouse model of seizures. Front Cell Neurosci. 7:138.
64. Volman V, Levine H, Sejnowski TJ. 2010. Shunting inhibition controls the gain modulation mediated by asynchronous neurotransmitter release in early development. PLoS Comput Biol. 6:e1000973.
65. A receptor-mediated signaling in epilepsy. In: Jasper's basic mechanisms of the epilepsies (Internet). 4th ed. Bethesda (MD): National Center for Biotechnology information (US).
66. Wei W, Zhang N, Peng Z, Houser CR, Mody I. 2003. Perisynaptic localization of delta subunit-containing GABA(A) receptors and their activation by GABA spillover in the mouse dentate gyrus. J Neurosci. 23:10650-10661.
67. Wen H, Linhoff MW, McGinley MJ, Li GL, Corson GM, Mandel G, Brehm P. 2010. Distinct roles for two synaptotagmin isoforms in synchronous and asynchronous transmitter release at zebrafish neuromuscular junction. Proc Natl Acad Sci USA. 107:13906-13911.
68. Xu T, Bajjalieh SM. 2001. SV2 modulates the size of the readily releas-able pool of secretory vesicles. Nat Cell Biol. 3:691-698.
69. Xu-Friedman MA, Regehr WG. 1999. Presynaptic strontium dynamics and synaptic transmission. Biophys J. 76:2029-2042.
70. Xu-Friedman MA, Regehr WG. 2000. Probing fundamental aspects of synaptic transmission with strontium. J Neurosci. 20:4414-4422.