Novel missense mutations in the glycine receptor β subunit gene (GLRB) in startle disease

Neurobiology of Disease

Volumn 52, Issue , 2013, Pages 137-149

  James, Victoria M ^a,b   Bode, Anna ^c   Chung, Seo Kyung ^d   Gill, Jennifer L ^a   Nielsen, Maartje ^e   Cowan, Frances M ^f   Vujic, Mihailo ^f,g   Thomas, Rhys H ^d   Rees, Mark I ^d   Harvey, Kirsten ^a   Keramidas, Angelo ^c   Topf, Maya ^b   Ginjaar, Ieke ^e   Lynch, Joseph W ^c   Harvey, Robert J ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d SWANSEA UNIVERSITY   (United Kingdom)

^e LEIDEN UNIVERSITY   (Netherlands)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

^g SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

GLRA1; GLRB; Glycine receptor; Hyperekplexia; Startle disease

Indexed keywords

ARGININE; CYSTEINE; GLYCINE; LEUCINE; METHIONINE; TRYPTOPHAN;

ARTICLE; BIOTINYLATION; BRAIN ELECTROPHYSIOLOGY; CLINICAL ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; DNA SEQUENCE; EMBRYO; FEMALE; GENE; GENE INSERTION; GLYCINE RECEPTOR BETA SUBUNIT GENE; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; HUMAN CELL; HYDROPHOBICITY; HYPEREKPLEXIA; MALE; MISSENSE MUTATION; MOLECULAR MODEL; MUTATIONAL ANALYSIS; NERVE CELL MEMBRANE CONDUCTANCE; PRIORITY JOURNAL; RESIDUE ANALYSIS; SENSITIVITY ANALYSIS; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; SUBSTITUTION REACTION;

FEMALE; HUMANS; MALE; MUSCLE HYPERTONIA; MUTATION, MISSENSE; RECEPTORS, GLYCINE; REFLEX, ABNORMAL; SEQUENCE ANALYSIS, DNA; STARTLE REACTION;

EID: 84873526942     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.12.001     Document Type: Article

References (58)

1. Adzhubei I.A., Schmidt S., Peshkin L., Ramensky V.E., Gerasimova A., Bork P., et al. A method and server for predicting damaging missense mutations. Nat. Methods 2010, 7:248-249.
2. Al-Owain M., Colak D., Al-Bakheet A., Al-Hashmi N., Shuaib T., Al-Hemidan A., et al. Novel mutation in GLRB in a large family with hereditary hyperekplexia. Clin. Genet. 2012, 81:479-484.
3. Benkert P., Biasini M., Schwede T. Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics 2011, 27:343-350.
4. Bocquet N., Nury H., Baaden M., Le Poupon C., Changeux J.P., Delarue M., et al. X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation. Nature 2009, 457:111-114.
5. Bormann J., Rundström N., Betz H., Langosch D. Residues within transmembrane segment M2 determine chloride conductance of glycine receptor homo- and hetero-oligomers. EMBO J. 1993, 12:3729-3737.
6. Buckwalter M.S., Cook S.A., Davisson M.T., White W.F., Camper S.A. A frameshift mutation in the mouse α1 glycine receptor gene (Glra1) results in progressive neurological symptoms and juvenile death. Hum. Mol. Genet. 1994, 3:2025-2030.
7. Careaga C.L., Falke J.J. Thermal motions of surface α-helices in the D-galactose chemosensory receptor. Detection by disulfide trapping. J. Mol. Biol. 1992, 226:1219-1235.
8. Carta E., Chung S.K., James V.M., Robinson A., Gill J.L., Remy N., et al. Mutations in the GlyT2 gene (SLC6A5) are a second major cause of hyperekplexia. J. Biol. Chem. 2012, 287:28975-28985.
9. Chang Y., Weiss D.S. Substitutions of the highly conserved M2 leucine create spontaneously opening ρ1 γ-aminobutyric acid receptors. Mol. Pharmacol. 1998, 53:511-523.
10. Chang Y., Weiss D.S. Allosteric activation mechanism of the α1β2γ2 γ-aminobutyric acid type A receptor revealed by mutation of the conserved M2 leucine. Biophys. J. 1999, 77:2542-2551.
11. Chung S.K., Vanbellinghen J.F., Mullins J.G., Robinson A., Hantke J., Hammond C.L., et al. Pathophysiological mechanisms of dominant and recessive GLRA1 mutations in hyperekplexia. J. Neurosci. 2010, 30:9612-9620.
12. Cymes G.D., Grosman C. Tunable pKa values and the basis of opposite charge selectivities in nicotinic-type receptors. Nature 2011, 474:526-530.
13. del Pino I., Paarmann I., Karas M., Kilimann M.W., Betz H. The trafficking proteins Vacuolar Protein Sorting 35 and Neurobeachin interact with the glycine receptor β subunit. Biochem. Biophys. Res. Commun. 2011, 412:435-440.
14. Dunbrack R.L. Rotamer libraries in the 21st century. Curr. Opin. Struct. Biol. 2002, 12:431-440.
15. Dutertre S., Drwal M., Laube B., Betz H. Probing the pharmacological properties of distinct subunit interfaces within heteromeric glycine receptors reveals a functional ββ agonist binding site. J. Neurochem. 2012, 122:38-47.
16. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
17. Eswar N., John B., Mirkovic N., Fiser A., Ilyin V.A., Pieper U., et al. Tools for comparative protein structure modeling and analysis. Nucleic Acids Res. 2003, 31:3375-3380.
18. Feng G., Tintrup H., Kirsch J., Nichol M.C., Kuhse J., Betz H., et al. Dual requirement for gephyrin in glycine receptor clustering and molybdoenzyme activity. Science 1998, 282:1321-1324.
19. Giménez C., Pérez-Siles G., Martínez-Villarreal J., Arribas-González E., Jiménez E., Núñez E., et al. A novel dominant hyperekplexia mutation Y705C alters trafficking and biochemical properties of the presynaptic glycine transporter GlyT2. J. Biol. Chem. 2012, 287:28986-29002.
20. Grudzinska J., Schemm R., Haeger S., Nicke A., Schmalzing G., Betz H., et al. The β subunit determines the ligand binding properties of synaptic glycine receptors. Neuron 2005, 45:727-739.
21. Haeger S., Kuzmin D., Detro-Dassen S., Lang N., Kilb M., Tsetlin V., et al. An intramembrane aromatic network determines pentameric assembly of Cys-loop receptors. Nat. Struct. Mol. Biol. 2010, 17:90-98.
22. Hibbs R.E., Gouaux E. Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 2011, 474:54-60.
23. Hilf R.J., Dutzler R. Structure of a potentially open state of a proton-activated pentameric ligand-gated ion channel. Nature 2009, 457:115-118.
24. Hirata H., Saint-Amant L., Downes G.B., Cui W.W., Zhou W., Granato M., et al. Zebrafish bandoneon mutants display behavioral defects due to a mutation in the glycine receptor β-subunit. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:8345-8350.
25. Holland K.D., Fleming M.T., Cheek S., Moran J.L., Beier D.R., Meisler M.H. De novo exon duplication in a new allele of mouse Glra1 (spasmodic). Genetics 2006, 174:2245-2247.
26. Islam R., Lynch J.W. Mechanism of action of the insecticides, lindane and fipronil, on glycine receptor chloride channels. Br. J. Pharmacol. 2012, 165:2707-2720.
27. Kim E.Y., Schrader N., Smolinsky B., Bedet C., Vannier C., Schwarz G., et al. Deciphering the structural framework of glycine receptor anchoring by gephyrin. EMBO J. 2006, 25:1385-1395.
28. Kingsmore S.F., Giros B., Suh D., Bieniarz M., Caron M.G., Seldin M.F. Glycine receptor β-subunit gene mutation in spastic mouse associated with LINE-1 element insertion. Nat. Genet. 1994, 7:136-141.
29. Kirsch J., Kuhse J., Betz H. Targeting of glycine receptor subunits to gephyrin-rich domains in transfected human embryonic kidney cells. Mol. Cell. Neurosci. 1995, 6:450-461.
30. A receptor chloride channels. Neurosci. Lett. 2005, 380:340-345.
31. Kumar P., Henikoff S., Ng P.C. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat. Protoc. 2009, 4:1073-1081.
32. Langosch D., Thomas L., Betz H. Conserved quaternary structure of ligand-gated ion channels: the postsynaptic glycine receptor is a pentamer. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:7394-7398.
33. Lee, C.G., Kwon, M.J., Yu, H.J., Nam, S.H., Lee, J., Ki, C.S. et al. 2012. Clinical features and genetic analysis of children with hyperekplexia in Korea. J. Child Neurol. http://dx.doi.org/10.1177/0883073812.
34. Lemke J.R., Riesch E., Scheurenbrand T., Schubach M., Wilhelm C., Steiner I., et al. Targeted next generation sequencing as a diagnostic tool in epileptic disorders. Epilepsia 2012, 53:1387-1398.
35. Lynch J.W. Native glycine receptor subtypes and their physiological roles. Neuropharmacology 2009, 56:303-309.
36. Manzke T., Niebert M., Koch U.R., Caley A., Vogelgesang S., Hülsmann S., Ponimaskin E., Müller U., Smart T.G., Harvey R.J., Richter D.W. Serotonin receptor 1A-modulated phosphorylation of glycine receptor α3 controls breathing in mice. J. Clin. Invest. 2010, 120:4118-4128.
37. Meyer G., Kirsch J., Betz H., Langosch D. Identification of a gephyrin binding motif on the glycine receptor β subunit. Neuron 1995, 15:563-572.
38. Milani N., Mülhardt C., Weber R.G., Lichter P., Kioschis P., Poustka A., et al. The human glycine receptor β subunit gene (GLRB): structure, refined chromosomal localization, and population polymorphism. Genomics 1998, 50:341-345.
39. Mülhardt C., Fischer M., Gass P., Simon-Chazottes D., Guénet J.L., Kuhse J., et al. The spastic mouse: aberrant splicing of glycine receptor β subunit mRNA caused by intronic insertion of L1 element. Neuron 1994, 13:1003-1015.
40. Notredame C., Higgins D.G., Heringa J. T-COFFEE: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 2000, 302:205-217.
41. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., et al. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
42. Pierce K.D., Handford C.A., Morris R., Vafa B., Dennis J.A., Healy P.J., et al. A nonsense mutation in the α1 subunit of the inhibitory glycine receptor associated with bovine myoclonus. Mol. Cell. Neurosci. 2001, 17:354-363.
43. Pless S.A., Millen K.S., Hanek A.P., Lynch J.W., Lester H.A., Lummis S.C., et al. A cation-π interaction in the binding site of the glycine receptor is mediated by a phenylalanine residue. J. Neurosci. 2008, 28:10937-10942.
44. Pribilla I., Takagi T., Langosch D., Bormann J., Betz H. The atypical M2 segment of the β subunit confers picrotoxinin resistance to inhibitory glycine receptor channels. EMBO J. 1994, 11:4305-4311.
45. Rees M.I., Harvey K., Pearce B.R., Chung S.K., Duguid I.C., Thomas P., et al. Mutations in the gene encoding GlyT2 (SLC6A5) define a presynaptic component of human startle disease. Nat. Genet. 2006, 38:801-806.
46. Rees M.I., Lewis T.M., Kwok J.B., Mortier G.R., Govaert P., Snell R.G., et al. Hyperekplexia associated with compound heterozygote mutations in the β-subunit of the human inhibitory glycine receptor (GLRB). Hum. Mol. Genet. 2002, 11:853-860.
47. Ryan S.G., Buckwalter M.S., Lynch J.W., Handford C.A., Segura L., Shiang R., et al. A missense mutation in the gene encoding the α1 subunit of the inhibitory glycine receptor in the spasmodic mouse. Nat. Genet. 1994, 7:131-135.
48. Shan Q., Han L., Lynch J.W. β subunit M2-M3 loop conformational changes are uncoupled from α1β glycine receptor channel gating: implications for human hereditary hyperekplexia. PLoS One 2011, 6:e28105.
49. Shen M.Y., Sali A. Statistical potential for assessment and prediction of protein structures. Protein Sci. 2006, 15:2507-2524.
50. Shiang R., Ryan S.G., Zhu Y.Z., Fielder T.J., Allen R.J., Fryer A., et al. Mutational analysis of familial and sporadic hyperekplexia. Ann. Neurol. 1995, 38:85-91.
51. Shiang R., Ryan S.G., Zhu Y.Z., Hahn A.F., O'Connell P., Wasmuth J.J. Mutations in the α1 subunit of the inhibitory glycine receptor cause the dominant neurologic disorder, hyperekplexia. Nat. Genet. 1993, 5:351-358.
52. Söding J., Biegert A., Lupas A.N. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 2005, 33:W244-W248.
53. Tijssen M.A., Padberg G.W., van Dijk J.G. The startle pattern in the minor form of hyperekplexia. Arch. Neurol. 1996, 53:608-613.
54. Tijssen M.A., Shiang R., van Deutekom J., Boerman R.H., Wasmuth J.J., Sandkuijl L.A., et al. Molecular genetic reevaluation of the Dutch hyperekplexia family. Arch. Neurol. 1995, 52:578-582.
55. Tijssen M.A., Vergouwe M.N., van Dijk J.G., Rees M., Frants R.R., Brown P. Major and minor form of hereditary hyperekplexia. Mov. Disord. 2002, 17:826-830.
56. Traka M., Seburn K.L., Popko B. Nmf11 is a novel ENU-induced mutation in the mouse glycine receptor α1 subunit. Mamm. Genome 2006, 17:950-955.
57. Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4Å resolution. J. Mol. Biol. 2005, 346:967-989.
58. Yang Z., Taran E., Webb T.I., Lynch J.W. Stoichiometry and subunit arrangement of α1β glycine receptors as determined by atomic force microscopy. Biochemistry 2012, 51:5229-5231.