Functional complementation of Glra1spd-ot, a glycine receptor subunit mutant, by independently expressed C-Terminal domains

Journal of Neuroscience

Volumn 29, Issue 8, 2009, Pages 2440-2452

  Villmann, Carmen ^a   Oertel, Jana ^a,d   Ma Högemeier, Zhan Lu ^b   Hollmann, Michael ^b   Sprengel, Rolf ^c   Becker, Kristina ^a   Breitinger, Hans Georg ^a,e   Becker, Cord Michael ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^d INSERM   (France)

^e German University in Cairo   (Egypt)

Author keywords

Chloride channel; Domain; Glycine receptor; Inhibition; Rescue; TM3 TM4 loop

Indexed keywords

CHLORIDE CHANNEL; GLYCINE RECEPTOR; ION CHANNEL; PROTEIN GLRA1; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; HOMOZYGOSITY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD NERVE CELL;

ANIMALS; BIOTINYLATION; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; EMBRYO, MAMMALIAN; HUMANS; ION CHANNEL GATING; LUMINESCENT PROTEINS; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; NEURONS; PATCH-CLAMP TECHNIQUES; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, GLYCINE; SPINAL CORD; TRANSFECTION;

EID: 61449130475     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4400-08.2009     Document Type: Article

References (46)

1. Andersson H, Bakker E, von Heijne G (1992) Different positively charged amino acids have similar effects on the topology of a polyopic transmembrane protein in Escherichia coli. J Biol Chem 267:1491-1495.
2. Becker CM, Hoch W, Betz H (1988) Glycine receptor heterogeneity in rat spinal cord during postnatal development. EMBO J 7:3717-3726.
3. Becker CM, Schmieden V, Tarroni P, Strasser U, Betz H (1992) Isoform-selective deficit of glycine receptors in the mouse mutant spastic. Neuron 8:283-289.
4. Becker K, Hohoff C, Schmitt B, Christen HJ, Neubauer BA, Sandrieser T, Becker CM (2006) Identification of the microdeletion breakpoint in a GLRA1null allele of Turkish hyperekplexia patients. Hum Mutat 27:1061-1062.
5. Becker K, Breitinger HG, Humeny A, Meinck HM, Dietz B, Aksu F, Becker CM (2008) The novel hyperekplexia allele GLRA1(S267N) affects the ethanol site of the glycine receptor. Eur J Hum Genet 16:223-228.
6. Betz H, Laube B (2006) Glycine receptors: recent insights into their structural organization and functional diversity. J Neurochem 97:1600-1610.
7. Breitinger HG, Becker CM (2002) The inhibitory glycine receptor - simple views of a complicated channel. Chembiochem 3:1042-1052.
8. Breitinger U, Breitinger HG, Bauer F, Fahmy K, Glockenhammer D, Becker CM (2004) Conserved high affinity ligand binding and membrane association in the native and refolded extracellular domain of the human glycine receptor alpha1-subunit. J Biol Chem 279:1627-1636.
9. Brodbeck J, Davies A, Courtney JM, Meir A, Balaguero N, Canti C, Moss FJ, Page KM, Pratt WS, Hunt SP, Barclay J, Rees M, Dolphin AC (2002) The ducky mutation in Cacna2d2 results in altered Purkinje cell morphology and is associated with the expression of a truncated alpha 2 delta-2 protein with abnormal function. J Biol Chem 277:7684-7693.
10. Buckwalter MS, Cook SA, Davisson MT, White WF, Camper SA (1994) A frameshift mutation in the mouse alpha 1 glycine receptor gene (Glra1) results in progressive neurological symptoms and juvenile death. Hum Mol Genet 3:2025-2030.
11. Büsselberg D, Bischoff AM, Becker K, Becker CM, Richter DW (2001) The respiratory rhythm in mutant oscillator mice. Neurosci Lett 316:99-102.
12. Eulenburg V, Becker K, Gomeza J, Schmitt B, Becker CM, Betz H (2006) Mutations within the human GLYT2 (SLC6A5) gene associated with hyperekplexia. Biochem Biophys Res Commun 348:400-405.
13. Grudzinska J, Schemm R, Haeger S, Nicke A, Schmalzing G, Betz H, Laube B (2005) The beta subunit determines the ligand binding properties of synaptic glycine receptors. Neuron 45:727-739.
14. Harvey RJ, Depner UB, Wässle H, Ahmadi S, Heindl C, Reinold H, Smart TG, Harvey K, Schutz B, Abo-Salem OM, Zimmer A, Poisbeau P, Welzl H, Wolfer DP, Betz H, Zeilhofer HU, Müller U (2004) GlyR alpha3: an essential target for spinal PGE2-mediated inflammatory pain sensitization. Science 304:884-887.
15. Hawkins LM, Prybylowski K, Chang K, Moussan C, Stephenson FA, Wenthold RJ (2004) Export from the endoplasmic reticulum of assembled N-methyl-D- aspartic acid receptors is controlled by a motif in the c terminus of the NR2 subunit. J Biol Chem 279:28903-28910.
16. Heinze L, Harvey RJ, Haverkamp S, Wassle H (2007) Diversity of glycine receptors in the mouse retina: localization ofthe alpha4 subunit. J Comp Neurol 500:693-707.
17. Hessa T, Kim H, Bihlmaier K, Lundin C, Boekel J, Andersson H, Nilsson I, White SH, von Heijne G (2005) Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433:377-381.
18. Hoch W, Betz H, Becker CM (1989) Primary cultures of mouse spinal cord express the neonatal isoform of the inhibitory glycine receptor. Neuron 3:339-348.
19. Holmes KD, Mattar PA, Marsh DR, Weaver LC, Dekaban GA (2002) The N-methyl-D-aspartate receptor splice variant NR1-4 C-terminal domain. Deletion analysis and role in subcellular distribution. J Biol Chem 277:1457-1468.
20. Jansen M, Bali M, Akabas MH (2008) Modular design of Cys-loop ligand- gated ion channels: functional 5-HT3 and GABA rho1 receptors lacking the large cytoplasmic M3M4 loop. J Gen Physiol 131:137-146.
21. Kingsmore SF, Giros B, Suh D, Bieniarz M, Caron MG, Seldin MF (1994) Glycine receptor beta-subunit gene mutation in spastic mouse associated with LINE-1 element insertion. Nat Genet 7:136-141.
22. Kling C, Koch M, Saul B, Becker CM (1997) The frameshift mutation oscillator(Glra1(spd-ot)) produces acomplete loss ofglycine receptor alpha1-polypeptide in mouse central nervous system. Neuroscience 78:411-417.
23. Kukhtina V, Kottwitz D, Strauss H, Heise B, Chebotareva N, Tsetlin V, Hucho F (2006) Intracellular domain of nicotinic acetylcholine receptor: the importance of being unfolded. J Neurochem 97 [Suppl 1]:63-67.
24. Langosch D, Herbold A, Schmieden V, Borman J, Kirsch J (1993) Importance of Arg-219 for correct biogenesis of alpha 1 homooligomeric glycine receptors. FEBS Lett 336:540-544.
25. Lynch JW (2004) Molecular structure and function of the glycine receptor chloride channel. Physiol Rev 84:1051-1095.
26. Malosio ML, Grenningloh G, Kuhse J, Schmieden V, Schmitt B, Prior P, Betz H (1991) Alternative splicing generates two variants ofthe alpha 1 subunit of the inhibitory glycine receptor. J Biol Chem 266:2048-2053.
27. Mulhardt C, Fischer M, Gass P, Simon-Chazottes D, Guenet JL, Kuhse J, Betz H, Becker CM (1994) The spastic mouse: aberrant splicing of glycine receptor beta subunit mRNA caused by intronic insertion ofL1 element. Neuron 13:1003-1015.
28. Nikolic Z, Laube B, Weber RG, Lichter P, Kioschis P, Poustka A, Mulhardt C, Becker CM (1998) The human glycine receptor subunit alpha3. Glra3 gene structure, chromosomal localization, and functional characterization of alternative transcripts. J Biol Chem 273:19708-19714.
29. Oertel J, Villmann C, Kettenmann H, Kirchhoff F, Becker CM (2007) A novel glycine receptor beta subunit splice variant predicts an unorthodox transmembrane topology. Assembly into heteromeric receptor complexes. J Biol Chem 282:2798-2807.
30. Rea R, Tijssen MA, Herd C, Frants RR, Kullmann DM (2002) Functional characterization of compound heterozygosity for GlyRalpha1 mutations in the startle disease hyperekplexia. Eur J Neurosci 16:186-196.
31. Rees MI, Andrew M, Jawad S, Owen MJ (1994) Evidence for recessive as well as dominant forms ofstartle disease (hyperekplexia) caused bymutations in the alpha 1 subunit ofthe inhibitoryglycine receptor. Hum Mol Genet 3:2175-2179.
32. Rees MI, Lewis TM, KwokJB, Mortier GR, Govaert P, Snell RG, Schofield PR, Owen MJ (2002) Hyperekplexia associated with compound heterozy- gote mutations in the beta-subunit of the human inhibitory glycine receptor (GLRB). Hum Mol Genet 11:853-860.
33. Rees MI, Harvey K, Pearce BR, Chung SK, Duguid IC, Thomas P, Beatty S, Graham GE, Armstrong L, Shiang R, Abbott KJ, Zuberi SM, Stephenson JB, Owen MJ, Tijssen MA, van den Maagdenberg AM, Smart TG, Sup- plisson S, Harvey RJ (2006) Mutations in the gene encoding GlyT2 (SLC6A5) define a presynaptic component of human startle disease. Nat Genet 38:801-806.
34. Ryan SG, Buckwalter MS, Lynch JW, Handford CA, Segura L, Shiang R, Wasmuth JJ, Camper SA, Schofield P, O'Connell P (1994) A missense mutation in the gene encoding the alpha 1 subunit of the inhibitory glycine receptor in the spasmodic mouse. Nat Genet 7:131-135.
35. Sadtler S, Laube B, Lashub A, Nicke A, Betz H, Schmalzing G (2003) A basic cluster determines topology of the cytoplasmic M3-M4 loop of the gly- cine receptor alpha1 subunit. J Biol Chem 278:16782-16790.
36. Saul B, Schmieden V, Kling C, Mulhardt C, Gass P, Kuhse J, Becker CM (1994) Point mutation of glycine receptor alpha 1 subunit in the spasmodic mouse affects agonist responses. FEBS Lett 350:71-76.
37. Schorge S, Colquhoun D (2003) Studies of NMDA receptor function and stoichiometry with truncated and tandem subunits. J Neurosci 23:1151-1158.
38. Schiller T, Mesic I, Madry C, Bartholomaus I, Laube B (2008) Formation of NR1/NR2 and NR1/NR3 heterodimers constitutes the initial step in N-methyl-D-aspartate receptor assembly. J Biol Chem 283:37-46.
39. Sontheimer H, Becker CM, Pritchett DB, Schofield PR, Grenningloh G, Ket- tenmann H, Betz H, Seeburg PH (1989) Functional chloride channels by mammalian cell expression of rat glycine receptor subunit. Neuron 2:1491-1497.
40. van Geest M, Lolkema JS (2000) Membrane topology and insertion of membrane proteins: search for topogenic signals. Microbiol Mol Biol Rev 64:13-33.
41. Villmann C, Bull L, Hollmann M (1997) Kainate binding proteins possess functional ion channel domains. J Neurosci 17:7634-7643.
42. Villmann C, Hoffmann J, Werner M, Kott S, Strutz-Seebohm N, Nilsson T, Hollmann M (2008) Different structural requirements for functional ion pore transplantation suggest different gating mechanisms of NMDA and kainate receptors. J Neurochem 107:453-465.
43. 2+ sensor. Nat Methods 5:797-804.
44. Yevenes GE, Moraga-Cid G, Guzmán L, Haeger S, Oliveira L, Olate J, Schmalzing G, Aguayo LG (2006) Molecular determinants for G protein βγ modulation of ionotropic glycine receptors. J Biol Chem 281:39300-39307.
45. Young TL, Cepko CL (2004) A role for ligand-gated ion channels in rod photoreceptor development. Neuron 41:867-879.
46. Zolotukhin S, Potter M, Zolotukhin I, Sakai Y, Loiler S, Fraites TJ Jr, Chiodo VA, Phillipsberg T, Muzyczka N, Hauswirth WW, Flotte TR, Byrne BJ, Snyder RO (2002) Production and purification ofserotype 1, 2, and 5 recombinant adeno-associated viral vectors. Methods 28:158 -167.