A human mutation in Gabrg2 associated with generalized epilepsy alters the membrane dynamics of GABA: A receptors

Cerebral Cortex

Volumn 22, Issue 7, 2012, Pages 1542-1553

  Bouthour, Walid ^a,b,c   Leroy, Félix ^a,b,c   Emmanuelli, Charline ^a,b,c   Carnaud, Michle ^a,b,c   Dahan, Maxime ^d   Poncer, Jean Christophe ^a,b,c   Lévi, Sabine ^a,b,c  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSTITUT DU FER À MOULIN   (France)

^d CNRS   (France)

Author keywords

epilepsy; GABA; GABA A receptor; hippocampus; quantum dots; single particle tracking

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOPYRIDINE; GLUTAMATE RECEPTOR ANTAGONIST;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; DIFFUSION; EMBRYO; FEBRILE CONVULSION; GABAERGIC TRANSMISSION; GABRG2 GENE; GENE; GENE MUTATION; GENERALIZED EPILEPSY; GENETIC ASSOCIATION; GENETIC RECOMBINATION; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; MINIATURE ENDPLATE POTENTIAL; MUTANT; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE; SYNAPTIC TRANSMISSION; TEMPERATURE DEPENDENCE; WILD TYPE;

ANIMALS; CELL MEMBRANE; CELLS, CULTURED; EPILEPSY, GENERALIZED; HIPPOCAMPUS; HUMANS; MUTATION; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SYNAPTIC TRANSMISSION;

EID: 84862879085     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr225     Document Type: Article

References (66)

1. Alivisatos AP, Gu W, Larabell C. 2005. Quantum dots as cellular probes. Annu Rev Biomed Eng. 7:55-76.
2. Andersen P, Moser EI. 1995. Brain temperature and hippocampal function. Hippocampus. 5:491-498.
3. Ankri N, Legendre P, Faber DS, Korn H. 1994. Automatic detection of spontaneous synaptic responses in central neurons. J Neurosci Methods. 52:87-100.
4. Audenaert D, Schwartz E, Claeys KG, Claes L, Deprez L, Suls A, Van Dyck T, Lagae L, Van Broeckhoven C, Macdonald RL, et al. 2006. A novel GABRG2 mutation associated with febrile seizures. Neurology. 67:687-690.
5. Baer K, Essrich C, Balsiger S, Wick MJ, Harris RA, Fritschy JM, Lüscher B. 2000. Rescue of gamma2 subunit-deficient mice by transgenic overexpression of the GABAA receptor gamma2S or gamma2L subunit isoforms. Eur J Neurosci. 12:2639-2643.
6. Banna H, Leívi S, Schweizer C, Dahan M, Triller A. 2006. Imaging the lateral diffusion of membrane molecules with quantum dots. Nat Protoc. 1:2628-2634.
7. Banna H, Leívi S, Schweizer C, Inoue T, Launey T, Racine V, Sibarita JB, Mikoshiba K, Triller A. 2009. Activity-dependent tuning of inhibitory neurotransmission based on GABAAR diffusion dynamics. Neuron. 62:670-682.
8. Baulac S, Huberfeld G, Gourfinkel-An I, Mitropoulou G, Beranger A, Prud'homme JF, Baulac M, Brice A, Bruzzone R, LeGuern E. 2001. First genetic evidence of GABA(A) receptor dysfunction in epilepsy: a mutation in the gamma2-subunit gene. Nat Genet. 28:46-48.
9. Bedet C, Bruusgaard JC, Vergo S, Groth-Pedersen L, Eimer S, Triller A, Vannier C. 2006. Regulation of gephyrin assembly and glycine receptor synaptic stability. J Biol Chem. 281:30046-30056.
10. Bianchi MT, Song L, Zhang H, Macdonald RL. 2002. Two different mechanisms of disinhibition produced by GABAA receptor mutations linked to epilepsy in humans. J Neurosci. 22:5321-5327.
11. Bogdanov Y, Michels G, Armstrong-Gold C, Haydon PG, Lindstrom J, Pangalos M, Moss SJ. 2006. Synaptic GABAA receptors are directly recruited from their extrasynaptic counterparts. EMBO J. 25:4381-4389.
12. Bonneau S, Dahan M, Cohen LD. 2005. Single quantum dot tracking based on perceptual grouping using minimal paths in a spatiotemporal volume. IEEE Trans Image Process. 14:1384-1395.
13. Calamai M, Specht CG, Heller J, Alcor D, Machado P, Vannier C, Triller A. 2009. Gephyrin oligomerization controls GlyR mobility and synaptic clustering. J Neurosci. 29:7639-7648.
14. Charrier C, Ehrensperger MV, Dahan M, Leívi S, Triller A. 2006. Cytoskeleton regulation of glycine receptor number at synapses and diffusion in the plasma membrane. J Neurosci. 26:8502-8511.
15. Charrier C, Machado P, Tweedie-Cullen RY, Rutishauser D, Mansuy IM, Triller A. 2010. A crosstalk between b1 and b3 integrins controls glycine receptor and gephyrin trafficking at synapses. Nat Neurosci. 13:1388-1395.
16. Choquet D, Triller A. 2003. The role of receptor diffusion in the organization of the postsynaptic membrane. Nat Rev Neurosci. 4:251-265.
17. Collingridge GL, Isaac JT, Wang YT. 2004. Receptor trafficking and synaptic plasticity. Nat Rev Neurosci. 5:952-962.
18. Dahan M, Leívi S, Luccardini C, Rostaing P, Riveau B, Triller A. 2003. Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science. 302:442-445.
19. Ehrensperger MV, Hanus C, Vannier C, Triller A, Dahan M. 2007. Multiple association states between glycine receptors and gephyrin identified by SPT analysis. Biophys J. 92:3706-3718.
20. Essrich C, Lorez M, Benson JA, Fritschy JM, Luscher B. 1998. Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat Neurosci. 1:563-571.
21. Eugène E, Depienne C, Baulac S, Baulac M, Fritschy JM, Le Guern E, Miles R, Poncer JC. 2007. GABA(A) receptor gamma 2 subunit mutations linked to human epileptic syndromes differentially affect phasic and tonic inhibition. J Neurosci. 27:14108-14116.
22. Frugier G, Coussen F, Giraud MF, Odessa MF, Emerit MB, Boue-Grabot E, Garret M. 2007. A gamma 2(R43Q) mutation, linked to epilepsy in humans, alters GABAA receptor assembly and modifies subunit composition on the cell surface. J Biol Chem. 282:3819-3828.
23. Gunther U, Benson J, Benke D, Fritschy JM, Reyes G, Knoflach F, Crestani F, Aguzzi A, Arigoni M, Lang Y, et al. 1995. Benzodiazepineinsensitive mice generated by targeted disruption of the gamma 2 subunit gene of gamma-aminobutyric acid type A receptors. Proc Natl Acad Sci USA. 92:7749-7753.
24. Gutiérrez A, Khan ZU, De Blas AL. 1994. Immunocytochemical localization of gamma 2 short and gamma 2 long subunits of the GABAA receptor in the rat brain. J Neurosci. 11:7168-7179.
25. Hales TG, Deeb TZ, Tang H, Bollan KA, King DP, Johnson SJ, Connolly CN. 2006. An asymmetric contribution to gammaaminobutyric type A receptor function of a conserved lysine within TM2-3 of alpha1, beta2, and gamma2 subunits. J Biol Chem. 281: 17034-17043.
26. Hanus C, Ehrensperger MV, Triller A. 2006. Activity-dependent movements of postsynaptic scaffolds at inhibitory synapses. J Neurosci. 26:4586-4595.
27. Jacob TC, Bogdanov YD, Magnus C, Saliba RS, Kittler JT, Haydon PG, Moss SJ. 2005. Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J Neurosci. 25:10469-10478.
28. Kang JQ, Shen W, Macdonald RL. 2006. Why does fever trigger febrile seizures? GABAA receptor c2 subunit mutations associated with idiopathic generalized epilepsies have temperature-dependent trafficking deficiencies. J Neurosci. 26:2590-2597.
29. Katz B, Miledi R. 1965. The effect of temperature on the synaptic delay at the neuromuscular junction. J Physiol. 181:656-670.
30. Khan ZU, Gutiérrez A, De Blas AL. 1994. Short and long form gamma 2 subunits of the GABAA/benzodiazepine receptors. J Neurochem. 63:1466-1476.
31. Kneussel M, Brandstatter JH, Gasnier B, Feng G, Sanes JR, Betz H. 2001. Gephyrin-independent clustering of postsynaptic GABA(A) receptor subtypes. Mol Cell Neurosci. 17:973-982.
32. Kneussel M, Brandstatter JH, Laube B, Stahl S, Müller U, Betz H. 1999. Loss of postsynaptic GABA(A) receptor clustering in gephyrindeficient mice. J Neurosci. 19:9289-9297.
33. Kushmerick C, Renden R, von Gersdorff H. 2006. Physiological temperatures reduce the rate of vesicle pool depletion and shortterm depression via an acceleration of vesicle recruitment. J Neurosci. 26:1366-1377.
34. Kusumi A, Sako Y, Yamamoto M. 1993. Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys J. 65:2021-2040.
35. Leívi S, Logan SM, Tovar KR, Craig AM. 2004. Gephyrin is critical for glycine receptor clustering but not for the formation of functional GABAergic synapses in hippocampal neurons. J Neurosci. 24: 207-217.
36. Leívi S, Schweizer C, Banna H, Pascual O, Charrier C, Triller A. 2008. Homeostatic regulation of synaptic GlyR numbers driven by lateral diffusion. Neuron. 59:261-273.
37. Lüscher B, Keller CA. 2004. Regulation of GABAA receptor trafficking, channel activity, and functional plasticity of inhibitory synapses. Pharmacol Ther. 102:195-221.
38. Macdonald RL, Kang JQ, Gallagher MJ. 2010. Mutations in GABAA receptor subunits associated with genetic epilepsies. J Physiol. 588:1861-1869.
39. Marks B, McMahon HT. 1998. Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr Biol. 8:740-749.
40. Marsh M, McMahon HT. 1999. The structural era of endocytosis. Science. 285:215-220.
41. Meier J, Grantyn R. 2004. Preferential accumulation of GABAA receptor gamma 2L, not gamma 2S, cytoplasmic loops at rat spinal cord inhibitory synapses. J Physiol. 559:355-365.
42. Miralles CP, Gutiérrez A, Khan ZU, Vitorica J, De Blas AL. 1994. Differential expression of the short and long forms of the gamma 2 subunit of the GABAA/benzodiazepine receptors. Brain Res Mol Brain Res. 24:129-139.
43. Mohler H, Fritschy JM, Rudolph U. 2002. A new benzodiazepine pharmacology. J Pharmacol Exp Ther. 300:2-8.
44. Moser E, Mathiesen I, Andersen P. 1993. Association between brain temperature and dentate field potentials in exploring and swimming rats. Science. 259:1324-1326.
45. Moss SJ, Doherty CA, Huganir RL. 1992. Identification of the cAMPdependent protein kinase and protein kinase C phosphorylation sites within the major intracellular domains of the beta 1, gamma 2S, and gamma 2L subunits of the gamma-aminobutyric acid type A receptor. J Biol Chem. 267:14470-14476.
46. Muir J, Arancibia-Carcamo IL, MacAskill AF, Smith KR, Griffin LD, Kittler JT. 2010. NMDA receptors regulate GABAA receptor lateral mobility and clustering at inhibitory synapses through serine 327 on the c2 subunit. Proc Natl Acad Sci USA. 107:16679-16684.
47. O'Mara M, Cromer B, Parker M, Chung SH. 2005. Homology model of the GABAA receptor examined using Brownian dynamics. Biophys J. 88:3286-3299.
48. Petrini EM, Lu J,Cognet L, Lounis B, EhlersMD,ChoquetD. 2009. Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron. 63:92-105.
49. Poncer JC, Dürr R, Gahwiler BH, Thompson SM. 1996. Modulation of synaptic GABAA receptor function by benzodiazepines in area CA3 of rat hippocampal slice cultures. Neuropharmacology. 35:1169-1179.
50. Postlethwaite M, Hennig MH, Steinert JR, Graham BP, Forsythe ID. 2007. Acceleration of AMPA receptor kinetics underlies temperaturedependent changes in synaptic strength at the rat calyx of Held. J Physiol. 579:69-84.
51. Pyott SJ, Rosenmund C. 2002. The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons. J Physiol. 539:523-535.
52. Ramakrishnan L, Hess GP. 2004. On the mechanism of a mutated and abnormally functioning gamma-aminobutyric acid (A) receptor linked to epilepsy. Biochemistry. 43:7534-7540.
53. Saxton MJ. 1997. Single-particle tracking: the distribution of diffusion coefficients. Biophys J. 72:1744-1753.
54. Schiff SJ, Somjen GG. 1985. The effects of temperature on synaptic transmission in hippocampal tissue slices. Brain Res. 345:279-284.
55. Schuchmann S, Schmitz D, Rivera C, Vanhatalo S, Salmen B, Mackie K, Sipild ST, Voipio J, Kaila K. 2006. Experimental febrile seizures are precipitated by a hyperthermia-induced respiratory alkalosis. Nat Med. 12:817-823.
56. Schweizer C, Balsiger S, Bluethmann H, Mansuy IM, Fritschy JM, Mohler H, Luscher B. 2003. The gamma 2 subunit of GABA(A) receptors is required for maintenance of receptors at mature synapses. Mol Cell Neurosci. 24:442-450.
57. Sun H, Zhang Y, Liang J, Liu X, Ma X, Wu H, Xu K, Qin J, Qi Y, Wu X. 2008. SCN1A, SCN1B, and GABRG2 gene mutation analysis in Chinese families with generalized epilepsy with febrile seizures plus. J Hum Genet. 53:769-774.
58. Tan HO, Reid CA, Single FN, Davies PJ, Chiu C, Murphy S, Clarke AL, Dibbens L, Krestel H, Mulley JC, et al. 2007. Reduced cortical inhibition in a mouse model of familial childhood absence epilepsy. Proc Natl Acad Sci USA. 104:17536-17541.
59. Tardin C, Cognet L, Bats C, Lounis B, Choquet D. 2003. Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO J. 22:4656-4665.
60. Thomas P, Mortensen M, Hosie AM, Smart TG. 2005. Dynamic mobility of functional GABAA receptors at inhibitory synapses. Nat Neurosci. 8:889-897.
61. Tretter V, Jacob TC, Mukherjee J, Fritschy JM, Pangalos MN, Moss SJ. 2008. The clustering of GABA(A) receptor subtypes at inhibitory synapses is facilitated via the direct binding of receptor alpha 2 subunits to gephyrin. J Neurosci. 28:1356-1365.
62. Triller A, Choquet D. 2005. Surface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move! Trends Neurosci. 28:133-139.
63. Triller A, Choquet D. 2008. New concepts in synaptic biology derived from single-molecule imaging. Neuron. 59:359-374.
64. Volgushev M, Vidyasagar TR, Chistiakova M, Eysel UT. 2000. Synaptic transmission in the neocortex during reversible cooling. Neuroscience. 98:9-22.
65. Wigge P, Vallis Y, McMahon HT. 1997. Inhibition of receptor-mediated endocytosis by the amphiphysin SH3 domain. Curr Biol. 7:554-560.
66. Zita MM, Marchionni I, Bottos E, Righi M, Del Sal G, Cherubini E, Zacchi P. 2007. Post-phosphorylation prolyl isomerisation of gephyrin represents a mechanism to modulate glycine receptors function. EMBO J. 26:1761-1771.