Glycine receptors caught between genome and proteome - Functional implications of RNA editing and splicing

Frontiers in Molecular Neuroscience

Volumn 2, Issue NOV, 2011, Pages

  Legendre, Pascal ^a,b,c   Förstera, Benjamin ^d,e   Jüttner, Rene ^e   Meier, Jochen C ^e  

^a INSERM   (France)

^b Université Pierre et Marie Curie   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

^e MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Epilepsy; GABA; Hippocampus; RNA editing; RNA splicing

Indexed keywords

4 AMINOBUTYRIC ACID; ACTIVATION INDUCED CYTIDINE DEAMINASE; GLYCINE RECEPTOR; GLYCINE TRANSPORTER; LEUCINE; NEUROTRANSMITTER RECEPTOR; NICOTINIC RECEPTOR; POTASSIUM CHANNEL; PROLINE; PROTEOME; SEROTONIN RECEPTOR;

AMINO ACID SUBSTITUTION; ARTICLE; CELL MEMBRANE; DESENSITIZATION; ELECTROPHYSIOLOGY; FUNCTIONAL PROTEOMICS; GENETIC TRANSFECTION; GENOME ANALYSIS; HIPPOCAMPUS; HUMAN; HYDROPHOBICITY; MEMBRANE POTENTIAL; NERVE CELL NETWORK; NERVE CONDUCTION; POSTSYNAPTIC MEMBRANE; RNA EDITING; RNA SPLICING; TEMPORAL LOBE EPILEPSY; WHOLE CELL PATCH CLAMP;

EID: 77952671320     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.02.023.2009     Document Type: Article

References (72)

1. Anant, S., and Davidson, N. O. (2001). Molecular mechanisms of apolipoprotein B mRNA editing. Curr. Opin. Lipidol. 12, 159-165.
2. Betz, H., and Laube, B. (2006). Glycine receptors: recent insights into their structural organization and functional diversity. J. Neurochem. 97, 1600-1610.
3. Bhalla, T., Rosenthal, J. J., Holmgren, M., and Reenan, R. (2004). Control of human potassium channel inactivation by editing of a small mRNA hairpin. Nat. Struct. Mol. Biol. 11, 950-956.
4. Bragin, A., Claeys, P., Vonck, K., Van, R. D., Wilson, C., Boon, P., and Engel, J. Jr. (2007). Analysis of initial slow waves (ISWs) at the seizure onset in patients with drug resistant temporal lobe epilepsy. Epilepsia 48, 1883-1894.
5. Breitinger, H. G., and Becker, C. M. (2002). The inhibitory glycine receptor-simple views of a complicated channel. Chembiochem 3, 1042-1052.
6. Breitinger, H. G., Villmann, C., Becker, K., and Becker, C. M. (2001). Opposing effects of molecular volume and charge at the hyperekplexia site alpha 1(P250) govern glycine receptor activation and desensitization. J. Biol. Chem. 276, 29657-29663.
7. Breitinger, H. G., Villmann, C., Rennert, J., Ballhausen, D., and Becker, C. M. (2002). Hydroxylated residues influence desensitization behaviour of recombinant alpha3 glycine receptor channels. J. Neurochem. 83, 30-36.
8. Brusa, R., Zimmermann, F., Koh, D. S., Feldmeyer, D., Gass, P., Seeburg, P. H., and Sprengel, R. (1995). Earlyonset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice. Science 270, 1677-1680.
9. Buckingham, S. D., Biggin, P. C., Sattelle, B. M., Brown, L. A., and Sattelle, D. B. (2005). Insect GABA receptors: splicing, editing, and targeting by antiparasitics and insecticides. Mol. Pharmacol. 68, 942-951.
10. Burzomato, V., Beato, M., Groot-Kormelink, P. J., Colquhoun, D., and Sivilotti, L. G. (2004). Single-channel behavior of heteromeric alpha1beta glycine receptors: an attempt to detect a conformational change before the channel opens. J. Neurosci. 24, 10924-10940.
11. Caraiscos, V. B., Elliott, E. M., You, T., Cheng, V. Y., Belelli, D., Newell, J. G., Jackson, M. F., Lambert, J. J., Rosahl, T. W., Wafford, K. A., MacDonald, J. F., and Orser, B. A. (2004). Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by alpha5 subunitcontaining gamma-aminobutyric acid type A receptors. Proc. Natl. Acad. Sci. U.S. A 101, 3662-3667.
12. Celie, P. H., Klaassen, R. V., Rossum-Fikkert, S. E., van Elk, R., van Nierop, P., Smit, A. B., and Sixma, T. K. (2005). Crystal structure of AChBP from Bulinus truncatus reveals the conserved structural scaffold and sites of variation in nicotinic acetylcholine receptors. J. Biol. Chem. 280, 26457-26466.
13. Colquhoun, D. (1998). Binding, gating, affinity and efficacy: the interpretation of structure-activity relationships for agonists and of the effects of mutating receptors. Br. J. Pharmacol. 125, 924-947.
14. Cubelos, B., Gimenez, C., and Zafra, F. (2005). Localization of the GLYT1 glycine transporter at glutamatergic synapses in the rat brain. Cereb. Cortex 15, 448-459.
15. Dahan, M., Levi, S., Luccardini, C., Rostaing, P., Riveau, B., and Triller, A. (2003). Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science 302, 442-445.
16. De Saint, J., David-Watine, B., Korn, H., and Bregestovski, P. (2001). Activation of human alpha1 and alpha2 homomeric glycine receptors by taurine and GABA. J. Physiol. 535, 741-755.
17. Eichler, S. A., Forstera, B., Smolinsky, B., Juttner, R., Lehmann, T. N., Fahling, M., Schwarz, G., Legendre, P., and Meier, J. C. (2009). Splice-specific roles of glycine receptor r3 in the hippocampus. Eur. J. Neurosci. 30, 1077-1091.
18. Eichler, S. A., Kirischuk, S., Jüttner, R., Schäfermeier, P. K., Legendre, P., Lehmann, T. N., Gloveli, T., Grantyn, R., and Meier, J. C. (2008). Glycinergic tonic inhibition of hippocampal neurons with depolarising GABAergic transmission elicits histopathological signs of temporal lobe epilepsy. J. Cell. Mol. Med. 12, 2848-2866.
19. Eichler, S. A., and Meier, J. C. (2008). E-I balance and human diseases-from molecules to networking. Front. Mol. Neurosci. 1, 2. doi: 10.3389/neuro.02.002.2008.
20. Fisher, R. S., Webber, W. R., Lesser, R. P., Arroyo, S., and Uematsu, S. (1992). High-frequency EEG activity at the start of seizures. J. Clin. Neurophysiol. 9, 441-448.
21. Geiman, E. J., Zheng, W., Fritschy, J. M., and Alvarez, F. J. (2002). Glycine and GABA(A) receptor subunits on Renshaw cells: relationship with presynaptic neurotransmitters and postsynaptic gephyrin clusters. J. Comp. Neurol. 444, 275-289.
22. Gomeza, J., Ohno, K., and Betz, H. (2003). Glycine transporter isoforms in the mammalian central nervous system: structures, functions and therapeutic promises. Curr. Opin. Drug Discov. Devel. 6, 675-682.
23. Grenningloh, G., Rienitz, A., Schmitt, B., Methfessel, C., Zensen, M., Beyreuther, K., Gundelfinger, E. D., and Betz, H. (1987). The strychnine-binding subunit of the glycine receptor shows homology with nicotinic acetylcholine receptors. Nature 328, 215-220.
24. Grudzinska, J., Schemm, R., Haeger, S., Nicke, A., Schmalzing, G., Betz, H., and Laube, B. (2005). The Beta subunit determines the ligand binding properties of synaptic glycine receptors. Neuron 45, 727-739.
25. Gurevich, I., Englander, M. T., Adlersberg, M., Siegal, N. B., and Schmauss, C. (2002). Modulation of serotonin 2C receptor editing by sustained changes in serotonergic neurotransmission. J. Neurosci. 22, 10529-10532.
26. Haverkamp, S., Muller, U., Zeilhofer, H. U., Harvey, R. J., and Wassle, H. (2004). Diversity of glycine receptors in the mouse retina: localization of the alpha2 subunit. J. Comp. Neurol. 477, 399-411.
27. Honjo, T., Nagaoka, H., Shinkura, R., and Muramatsu, M. (2005). AID to overcome the limitations of genomic information. Nat. Immunol. 6, 655-661.
28. Jones, M. V., and Westbrook, G. L. (1995). Desensitized states prolong GABAA channel responses to brief agonist pulses. Neuron 15, 181-191.
29. Kirchner, A., Breustedt, J., Rosche, B., Heinemann, U. F., and Schmieden, V. (2003). Effects of taurine and glycine on epileptiform activity induced by removal of Mg2rrin combined rat entorhinal cortex-hippocampal slices. Epilepsia 44, 1145-1152.
30. Kirsch, J., Langosch, D., Prior, P., Littauer, U. Z., Schmitt, B., and Betz, H. (1991). The 93-kDa glycine receptorassociated protein binds to tubulin. J. Biol. Chem. 266, 22242-22245.
31. Lape, R., Colquhoun, D., and Sivilotti, L. G. (2008). On the nature of partial agonism in the nicotinic receptor superfamily. Nature 454, 722-727.
32. Laube, B., Kuryatov, A., Kuhse, J., and Betz, H. (1993). Glycine-glutamate interactions at the NMDA receptor: role of cysteine residues. FEBS Lett. 335, 331-334.
33. Lee, H., Chen, C. X., Liu, Y. J., Aizenman, E., and Kandler, K. (2005). KCC2 expression in immature rat cortical neurons is sufficient to switch the polarity of GABA responses. Eur. J. Neurosci. 21, 2593-2599.
34. Legendre, P. (1998). A reluctant gating mode of glycine receptor channels determines the time course of inhibitory miniature synaptic events in zebrafish hindbrain neurons. J. Neurosci. 18, 2856-2870.
35. Legendre, P. (2001). The glycinergic inhibitory synapse. Cell Mol. Life Sci. 58, 760-793.
36. Levi, S., Logan, S. M., Tovar, K. R., and Craig, A. M. (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.
37. Lewis, T. M., Sivilotti, L. G., Colquhoun, D., Gardiner, R. M., Schoepfer, R., and Rees, M. (1998). Properties of human glycine receptors containing the hyperekplexia mutation alpha1(K276E), expressed in Xenopus oocytes. J. Physiol. 507, 25-40.
38. Lohmann, C., Finski, A., and Bonhoeffer, T. (2005). Local calcium transients regulate the spontaneous motility of dendritic filopodia. Nat. Neurosci. 8, 305-312.
39. Loup, F., Wieser, H. G., Yonekawa, Y., Aguzzi, A., and Fritschy, J. M. (2000). Selective alterations in GABAA receptor subtypes in human temporal lobe epilepsy. J. Neurosci. 20, 5401-5419.
40. Lu, T., Rubio, M. E., and Trussell, L. O. (2008). Glycinergic transmission shaped by the corelease of GABA in a mammalian auditory synapse. Neuron 57, 524-535.
41. Lynch, J. W. (2009). Native glycine receptor subtypes and their physiological roles. Neuropharmacology 56, 303-309.
42. Malosio, M. L., Grenningloh, G., Kuhse, J., Schmieden, V., Schmitt, B., Prior, P., and Betz, H. (1991). Alternative splicing generates two variants of the alpha 1 subunit of the inhibitory glycine receptor. J. Biol. Chem. 266, 2048-2053.
43. Mangin, J. M., Baloul, M., Prado, D. C., Rogister, B., Rigo, J. M., and Legendre, P. (2003). Kinetics properties of the alpha2 homo-oligomeric glycine receptor impairs a proper synaptic functioning. J. Physiol. (Lond.) 553, 369-386.
44. Meier, J., and Grantyn, R. (2004). A gephyrin-related mechanism restraining glycine receptor anchoring at GABAergic synapses. J. Neurosci. 24, 1398-1405.
45. Meier, J., Meunier-Durmort, C., Forest, C., Triller, A., and Vannier, C. (2000). Formation of glycine receptor clusters and their accumulation at synapses. J. Cell Sci. 113, 2783-2795.
46. Meier, J., Vannier, C., Serge, A., Triller, A., and Choquet, D. (2001). Fast and reversible trapping of surface glycine receptors by gephyrin. Nat. Neurosci. 4, 253-260.
47. Meier, J. C., Henneberger, C., Melnick, I., Racca, C., Harvey, R. J., Heinemann, U., Schmieden, V., and Grantyn, R. (2005). RNA editing produces glycine receptor p3P185L resulting in high agonist potency. Nat. Neurosci. 8, 736-744.
48. Meyer, G., Kirsch, J., Betz, H., and Langosch, D. (1995). Identification of a gephyrin binding motif on the glycine receptor beta subunit. Neuron 15, 563-572.
49. Miller, P. S., Harvey, R. J., and Smart, T. G. (2004). Differential agonist sensitivity of glycine receptor alpha2 subunit splice variants. Br. J. Pharmacol. 143, 19-26.
50. Mody, I. (2001). Distinguishing between GABA(A) receptors responsible for tonic and phasic conductances. Neurochem. Res. 26, 907-913.
51. Mody, I., and Pearce, R. A. (2004). Diversity of inhibitory neurotransmission through GABA(A) receptors. Trends Neurosci. 27, 569-575.
52. Moorhouse, A. J., Jacques, P., Barry, P. H., and Schofield, P. R. (1999). The startle disease mutation Q266H, in the second transmembrane domain of the human glycine receptor, impairs channel gating. Mol. Pharmacol. 55, 386-395.
53. Mukhtasimova, N., Lee, W. Y., Wang, H. L., and Sine, S. M. (2009). Detection and trapping of intermediate states priming nicotinic receptor channel opening. Nature 459, 451-454.
54. Müller, E., Bakkar, W., Legendre, P., Bergeron, R., and Martina, M. (2007). Site and mechanism of glycine release at glutamatergic synapse in mouse hippocampus. (Program No. 358.12/J20). San Diego, CA: Society for Neuroscience.
55. Muller, E., Le, C. H., Triller, A., and Legendre, P. (2006). Developmental dissociation of presynaptic inhibitory neurotransmitter and postsynaptic receptor clustering in the hypoglossal nucleus. Mol. Cell. Neurosci. 32, 254-273.
56. Nakae, A., Tanaka, T., Miyake, K., Hase, M., and Mashimo, T. (2008). Comparing methods of detection and quantitation of RNA editing of rat glycine receptor alpha3. Int. J. Biol. Sci. 4, 397-405.
57. Nikolic, Z., Laube, B., Weber, R. G., Lichter, P., Kioschis, P., Poustka, A., Mulhardt, C., and Becker, C. M. (1998). The human glycine receptor subunit alpha3. Glra3 gene structure, chromosomal localization, and functional characterization of alternative transcripts. J. Biol. Chem. 273, 19708-19714.
58. Padgett, C. L., and Lummis, S. C. (2008). The F-loop of the GABA A receptor gamma2 subunit contributes to benzodiazepine modulation. J. Biol. Chem. 283, 2702-2708.
59. Palma, E., Amici, M., Sobrero, F., Spinelli, G., Di, A. S., Ragozzino, D., Mascia, A., Scoppetta, C., Esposito, V., Miledi, R., and Eusebi, F. (2006). Anomalous levels of Cl+ transporters in the hippocampal subiculum from temporal lobe epilepsy patients make GABA excitatory. Proc. Natl. Acad. Sci. U.S. A 103, 8465-8468.
60. Pless, S. A., and Lynch, J. W. (2009). Ligand-specific conformational changes in the alpha1 glycine receptor ligand-binding domain. J. Biol. Chem. 284, 15847-15856.
61. Plested, A. J., Groot-Kormelink, P. J., Colquhoun, D., and Sivilotti, L. G. (2007). Single-channel study of the spasmodic mutation alpha1A52S in recombinant rat glycine receptors. J. Physiol. 581, 51-73.
62. Rivera, C., Voipio, J., Thomas-Crusells, J., Li, H., Emri, Z., Sipila, S., Payne, J. A., Minichiello, L., Saarma, M., and Kaila, K. (2004). Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J. Neurosci. 24, 4683-4691.
63. Roux, M. J., and Supplisson, S. (2000). Neuronal and glial glycine transporters have different stoichiometries. Neuron 25, 373-383.
64. Seeburg, P. H., and Hartner, J. (2003). Regulation of ion channel/neurotransmitter receptor function by RNA editing. Curr. Opin. Neurobiol. 13, 279-283.
65. Simon, J., Wakimoto, H., Fujita, N., Lalande, M., and Barnard, E. A. (2004). Analysis of the set of GABA(A) receptor genes in the human genome. J. Biol. Chem. 279, 41422-41435.
66. Song, W., Chattipakorn, S. C., and McMahon, L. L. (2006). Glycine-gated chloride channels depress synaptic transmission in rat hippocampus. J. Neurophysiol. 95, 2366-2379.
67. Stief, F., Zuschratter, W., Hartmann, K., Schmitz, D., and Draguhn, A. (2007). Enhanced synaptic excitationinhibition ratio in hippocampal interneurons of rats with temporal lobe epilepsy. Eur. J. Neurosci. 25, 519-528.
68. Supplisson, S., and Roux, M. J. (2002). Why glycine transporters have different stoichiometries. FEBS Lett. 529, 93-101.
69. Tao, H. W., and Poo, M. M. (2005). Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields. Neuron 45, 829-836.
70. Unwin, N., Miyazawa, A., Li, J., and Fujiyoshi, Y. (2002). Activation of the Nicotinic Acetylcholine Receptor Involves a Switch in Conformation of the alpha Subunits. J. Mol. Biol. 319, 1165-1176.
71. Wisden, W., Cope, D., Klausberger, T., Hauer, B., Sinkkonen, S. T., Tretter, V., Lujan, R., Jones, A., Korpi, E. R., Mody, I., Sieghart, W., and Somogyi, P. (2002). Ectopic expression of the GABA(A) receptor alpha6 subunit in hippocampal pyramidal neurons produces extrasynaptic receptors and an increased tonic inhibition. Neuropharmacology 43, 530-549.
72. Zhang, L. H., Gong, N., Fei, D., Xu, L., and Xu, T. L. (2008). Glycine uptake regulates hippocampal network activity via glycine receptor-mediated tonic inhibition. Neuropsychopharmacology 33, 701-711.