Deletion of the mouse glycine transporter 2 results in a hyperekplexia phenotype and postnatal lethality

Neuron

Volumn 40, Issue 4, 2003, Pages 797-806

  Gomeza, Jesús ^a,c   Ohno, Koji ^a,d   Hülsmann, Swen ^b   Armsen, Wencke ^a   Eulenburg, Volker ^a   Richter, Diethelm W ^b   Laube, Bodo ^a   Betz, Heinrich ^a  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSPORTER; GLYCINE TRANSPORTER 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRIC CURRENT; EMBRYO; GENE DELETION; HISTOPATHOLOGY; HYPOGLOSSAL NERVE; IMMUNOHISTOCHEMISTRY; MOTOR NEURON DISEASE; MOUSE; NONHUMAN; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SPASTICITY; STARTLE EPILEPSY; TREMOR;

EID: 0242544067     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(03)00673-1     Document Type: Article

References (55)

1. Amara S.G., Kuhar M.J. Neurotransmitter transporters. recent progress Annu. Rev. Neurosci. 16:1993;73-93.
2. Andrew M., Owen M.J. Hyperekplexia. abnormal startle response due to glycine receptor mutations Br. J. Psychiatry. 170:1997;106-108.
3. Becker C.M., Hoch W., Betz H. Glycine receptor heterogeneity in rat spinal cord during postnatal development. EMBO J. 7:1988;3717-3726.
4. Becker C.M., Schmieden V., Tarroni P., Strasser U., Betz H. Isoform-selective deficit of glycine receptors in the mouse mutant spastic. Neuron. 8:1992;283-289.
5. Becker L., Hartenstein B., Schenkel J., Kuhse J., Betz H., Weiher H. Transient neuromotor phenotype in transgenic spastic mice expressing low levels of glycine receptor beta-subunit. an animal model of startle disease Eur. J. Neurosci. 12:2000;27-32.
6. Bengel D., Murphy D.L., Andrews A.M., Wichems C.H., Feltner D., Heils A., Mossner R., Westphal H., Lesch K.P. Altered brain serotonin homeostasis and locomotor insensitivity to 3, 4-methylenedioxymethamphetamine ("Ecstasy") in serotonin transporter-deficient mice. Mol. Pharmacol. 53:1998;649-655.
7. Bennett M.K., Calakos N., Scheller R.H. Syntaxin. a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones Science. 257:1992;255-259.
8. Breitinger H.G., Becker C.M. The inhibitory glycine receptor. prospects for a therapeutic orphan? Curr. Pharm. Des. 4:1998;315-334.
9. Buckwalter M.S., Cook S.A., Davisson M.T., White W.F., Camper S.A. A frameshift mutation in the mouse alpha 1 glycine receptor gene (Glra1) results in progressive neurological symptoms and juvenile death. Hum. Mol. Genet. 3:1994;2025-2030.
10. Cho K.O., Hunt C.A., Kennedy M.B. The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron. 9:1992;929-942.
11. Dumoulin A., Rostaing P., Bedet C., Levi S., Isambert M.F., Henry J.P., Triller A., Gasnier B. Presence of the vesicular inhibitory amino acid transporter in GABAergic and glycinergic synaptic terminal boutons. J. Cell Sci. 112:1999;811-823.
12. Feng G., Tintrup H., Kirsch J., Nichol M.C., Kuhse J., Betz H., Sanes J.R. Dual requirement for gephyrin in glycine receptor clustering and molybdoenzyme activity. Science. 282:1998;1321-1324.
13. Friauf E., Aragon C., Lohrke S., Westenfelder B., Zafra F. Developmental expression of the glycine transporter GLYT2 in the auditory system of rats suggests involvement in synapse maturation. J. Comp. Neurol. 412:1999;17-37.
14. Gainetdinov R.R., Jones S.R., Fumagalli F., Wightman R.M., Caron M.G. Re-evaluation of the role of the dopamine transporter in dopamine system homeostasis. Brain Res. Brain Res. Rev. 26:1998;148-153.
15. Gomeza J., Hulsmann S., Ohno K., Eulenburg V., Szoke K., Richter D., Betz H. Inactivation of the glycine transporter 1 gene discloses vital role of glial glycine uptake in glycinergic inhibition. Neuron. 40:2003;785-796. this issue.
16. Grenningloh G., Pribilla I., Prior P., Multhaup G., Beyreuther K., Taleb O., Betz H. Cloning and expression of the 58 kd beta subunit of the inhibitory glycine receptor. Neuron. 4:1990;963-970.
17. Hartenstein B., Schenkel J., Kuhse J., Besenbeck B., Kling C., Becker C.M., Betz H., Weiher H. Low level expression of glycine receptor beta subunit transgene is sufficient for phenotype correction in spastic mice. EMBO J. 15:1996;1275-1282.
18. Hülsmann S., Oku Y., Zhang W., Richter D.W. Metabotropic glutamate receptors and blockade of glial Krebs cycle depress glycinergic synaptic currents of mouse hypoglossal motoneurons. Eur. J. Neurosci. 12:2000;239-246.
19. Jones S.R., Gainetdinov R.R., Jaber M., Giros B., Wightman R.M., Caron M.G. Profound neuronal plasticity in response to inactivation of the dopamine transporter. Proc. Natl. Acad. Sci. USA. 95:1998;4029-4034.
20. Jones S.R., Gainetdinov R.R., Hu X.T., Cooper D.C., Wightman R.M., White F.J., Caron M.G. Loss of autoreceptor functions in mice lacking the dopamine transporter. Nat. Neurosci. 2:1999;649-655.
21. Kingsmore S.F., Giros B., Suh D., Bieniarz M., Caron M.G., Seldin M.F. Glycine receptor beta-subunit gene mutation in spastic mouse associated with LINE-1 element insertion. Nat. Genet. 7:1994;136-141.
22. Kirsch J., Betz H. The postsynaptic localization of the glycine receptor-associated protein gephyrin is regulated by the cytoskeleton. J. Neurosci. 15:1995;4148-4156.
23. Kling C., Koch M., Saul B., Becker C.M. The frameshift mutation oscillator (Glra1(spd-ot)) produces a complete loss of glycine receptor alpha1-polypeptide in mouse central nervous system. Neuroscience. 78:1997;411-417.
24. Kuhse J., Betz H., Kirsch J. The inhibitory glycine receptor. architecture, synaptic localization and molecular pathology of a postsynaptic ion-channel complex Curr. Opin. Neurobiol. 5:1995;318-323.
25. Langosch D., Laube B., Rundstrom N., Schmieden V., Bormann J., Betz H. Decreased agonist affinity and chloride conductance of mutant glycine receptors associated with human hereditary hyperekplexia. EMBO J. 13:1994;4223-4228.
26. 2+. a synergistic interplay between presynaptic P2X2 and postsynaptic glycine receptors Eur. J. Neurosci. 16:2002;1025-1036.
27. Laube B., Maksay G., Schemm R., Betz H. Modulation of glycine receptor function. a novel approach for therapeutic intervention at inhibitory synapses? Trends Pharmacol. Sci. 23:2002;519-527.
28. Lewis T.M., Sivilotti L.G., Colquhoun D., Gardiner R.M., Schoepfer R., Rees M. Properties of human glycine receptors containing the hyperekplexia mutation alpha1(K276E), expressed in Xenopus oocytes. J. Physiol. 507:1998;25-40.
29. Lim R., Alvarez F.J., Walmsley B. Quantal size is correlated with receptor cluster area at glycinergic synapses in the rat brainstem. J. Physiol. 516:1999;505-512.
30. Mahendrasingam S., Wallam C.A., Hackney C.M. An immunogold investigation of the relationship between the amino acids GABA and glycine and their transporters in terminals in the guinea-pig anteroventral cochlear nucleus. Brain Res. 887:2000;477-481.
31. Malosio M.L., Marqueze-Pouey B., Kuhse J., Betz H. Widespread expression of glycine receptor subunit mRNAs in the adult and developing rat brain. EMBO J. 10:1991;2401-2409.
32. Milani N., Dalpra L., del Prete A., Zanini R., Larizza L. A novel mutation (Gln266→His) in the alpha 1 subunit of the inhibitory glycine-receptor gene (GLRA1) in hereditary hyperekplexia. Am. J. Hum. Genet. 58:1996;420-422.
33. Moriyoshi K., Masu M., Ishii T., Shigemoto R., Mizuno N., Nakanishi S. Molecular cloning and characterization of the rat NMDA receptor. Nature. 354:1991;31-37.
34. Mulhardt C., Fischer M., Gass P., Simon-Chazottes D., Guenet J.L., Kuhse J., Betz H., Becker C.M. The spastic mouse. aberrant splicing of glycine receptor beta subunit mRNA caused by intronic insertion of L1 element Neuron. 13:1994;1003-1015.
35. - neurotransmitter transporters. J. Neurochem. 71:1998;1785-1803.
36. Overstreet L.S., Jones M.V., Westbrook G.L. Slow desensitization regulates the availability of synaptic GABA(A) receptors. J. Neurosci. 20:2000;7914-7921.
37. Pfeiffer F., Simler R., Grenningloh G., Betz H. Monoclonal antibodies and peptide mapping reveal structural similarities between the subunits of the glycine receptor of rat spinal cord. Proc. Natl. Acad. Sci. USA. 81:1984;7224-7227.
38. Poyatos I., Ponce J., Aragon C., Gimenez C., Zafra F. The glycine transporter GLYT2 is a reliable marker for glycine-immunoreactive neurons. Brain Res. Mol. Brain Res. 49:1997;63-70.
39. Prior P., Schmitt B., Grenningloh G., Pribilla I., Multhaup G., Beyreuther K., Maulet Y., Werner P., Langosch D., Kirsch J., et al. Primary structure and alternative splice variants of gephyrin, a putative glycine receptor-tubulin linker protein. Neuron. 8:1992;1161-1170.
40. Rajendra S., Schofield P.R. Molecular mechanisms of inherited startle syndromes. Trends Neurosci. 18:1995;80-82.
41. Rees M.I., Andrew M., Jawad S., Owen M.J. Evidence for recessive as well as dominant forms of startle disease (hyperekplexia) caused by mutations in the alpha 1 subunit of the inhibitory glycine receptor. Hum. Mol. Genet. 3:1994;2175-2179.
42. Ryan S.G., Buckwalter M.S., Lynch J.W., Handford C.A., Segura L., Shiang R., Wasmuth J.J., Camper S.A., Schofield P., O'Connell P. A missense mutation in the gene encoding the alpha 1 subunit of the inhibitory glycine receptor in the spasmodic mouse. Nat. Genet. 7:1994;131-135.
43. Sakata Y., Owada Y., Sato K., Kojima K., Hisanaga K., Shinka T., Suzuki Y., Aoki Y., Satoh J., Kondo H., et al. Structure and expression of the glycine cleavage system in rat central nervous system. Brain Res. Mol. Brain Res. 94:2001;119-130.
44. Saul B., Schmieden V., Kling C., Mulhardt C., Gass P., Kuhse J., Becker C.M. Point mutation of glycine receptor alpha 1 subunit in the spasmodic mouse affects agonist responses. FEBS Lett. 350:1994;71-76.
45. Schloss P., Puschel A.W., Betz H. Neurotransmitter transporters. new members of known families Curr. Opin. Cell Biol. 6:1994;595-599.
46. Schroder S., Hoch W., Becker C.M., Grenningloh G., Betz H. Mapping of antigenic epitopes on the alpha 1 subunit of the inhibitory glycine receptor. Biochemistry. 30:1991;42-47.
47. Shiang R., Ryan S.G., Zhu Y.Z., Fielder T.J., Allen R.J., Fryer A., Yamashita S., O'Connell P., Wasmuth J.J. Mutational analysis of familial and sporadic hyperekplexia. Ann. Neurol. 38:1995;85-91.
48. Singer J.H., Talley E.M., Bayliss D.A., Berger A.J. Development of glycinergic synaptic transmission to rat brain stem motoneurons. J. Neurophysiol. 80:1998;2608-2620.
49. Spike R.C., Watt C., Zafra F., Todd A.J. An ultrastructural study of the glycine transporter GLYT2 and its association with glycine in the superficial laminae of the rat spinal dorsal horn. Neuroscience. 77:1997;543-551.
50. Takahashi T., Momiyama A., Hirai K., Hishinuma F., Akagi H. Functional correlation of fetal and adult forms of glycine receptors with developmental changes in inhibitory synaptic receptor channels. Neuron. 9:1992;1155-1161.
51. Tijssen M.A., Voorkamp L.M., Padberg G.W., van Dijk J.G. Startle responses in hereditary hyperekplexia. Arch. Neurol. 54:1997;388-393.
52. Triller A., Cluzeaud F., Pfeiffer F., Betz H., Korn H. Distribution of glycine receptors at central synapses. an immunoelectron microscopy study J. Cell Biol. 101:1985;683-688.
53. Vergouwe M.N., Tijssen M.A., Shiang R., van Dijk J.G., al Shahwan S., Ophoff R.A., Frants R.R. Hyperekplexia-like syndromes without mutations in the GLRA1 gene. Clin. Neurol. Neurosurg. 99:1997;172-178.
54. Zafra F., Aragon C., Olivares L., Danbolt N.C., Gimenez C., Storm-Mathisen J. Glycine transporters are differentially expressed among CNS cells. J. Neurosci. 15:1995;3952-3969. a.
55. Zafra F., Gomeza J., Olivares L., Aragon C., Gimenez C. Regional distribution and developmental variation of the glycine transporters GLYT1 and GLYT2 in the rat CNS. Eur. J. Neurosci. 7:1995;1342-1352. b.