Molecular basis of the differential interaction with lithium of glycine transporters GLYT1 and GLYT2

Journal of Neurochemistry

Volumn 118, Issue 2, 2011, Pages 195-204

  Pérez Siles, Gonzalo ^a,b   Morreale, Antonio ^a   Leo Macías, Alejandra ^a   Pita, Guillermo ^a   Ortíz, Ángel R ^a   Aragón, Carmen ^a,b   López Corcuera, Beatriz ^a,b  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

glycine; lithium site; neurotransmitter; sodium site; sodium symporters; transport

Indexed keywords

GLYCINE TRANSPORTER 1; GLYCINE TRANSPORTER 2; LITHIUM ION; SODIUM ION;

AQUIFEX AEOLICUS; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; MOLECULAR DYNAMICS; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; GLYCINE; GLYCINE PLASMA MEMBRANE TRANSPORT PROTEINS; LITHIUM; PROTEIN BINDING; PROTEIN TRANSPORT;

AQUIFEX AEOLICUS;

EID: 79959968564     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07309.x     Document Type: Article

References (43)

1. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., and, Lipman D. J., (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402. (Pubitemid 27359211)
2. Aragon C., and, Lopez-Corcuera B., (2003) Structure, function and regulation of glycine neurotransporters. Eur. J. Pharmacol. 479, 249-262. (Pubitemid 37377893)
3. Aragon C., and, Lopez-Corcuera B., (2005) Glycine transporters: crucial roles of pharmacological interest revealed by gene deletion. Trends Pharmacol. Sci. 26, 283-286. (Pubitemid 40733520)
4. Beuming T., Shi L., Javitch J. A., and, Weinstein H., (2006) A comprehensive structure-based alignment of prokaryotic and eukaryotic neurotransmitter/Na+ symporters (NSS) aids in the use of the LeuT structure to probe NSS structure and function. Mol. Pharmacol. 70, 1630-1642.
5. Broer A., Balkrishna S., Kottra G., Davis S., Oakley A., and, Broer S., (2009) Sodium translocation by the iminoglycinuria associated imino transporter (SLC6A20). Mol. Membr. Biol. 26, 333-346.
6. Chen N., Trowbridge C. G., and, Justice Jr J. B., (1999) Cationic modulation of human dopamine transporter: dopamine uptake and inhibition of uptake. J. Pharmacol. Exp. Ther. 290, 940-949. (Pubitemid 29400229)
7. 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. (Pubitemid 40388245)
8. Deutsch S. I., Stanley M., Peselow E. D., and, Banay-Schwartz M., (1983) Glycine: a possible role in lithium's action and affective illness. Neuropsychobiology 9, 215-218. (Pubitemid 13018095)
9. Dohi T., Morita K., Kitayama T., Motoyama N., and, Morioka N., (2009) Glycine transporter inhibitors as a novel drug discovery strategy for neuropathic pain. Pharmacol. Ther. 123, 54-79.
10. Eddy S. R., (1998) Profile hidden Markov models. Bioinformatics 14, 755-763. (Pubitemid 28552108)
11. Fornes A., Nunez E., Aragon C., and, Lopez-Corcuera B., (2004) The second intracellular loop of the glycine transporter 2 contains crucial residues for glycine transport and phorbol ester-induced regulation. J. Biol. Chem. 279, 22934-22943. (Pubitemid 38685595)
12. Fornes A., Nunez E., Alonso-Torres P., Aragon C., and, Lopez-Corcuera B., (2008) Trafficking properties and activity regulation of the neuronal glycine transporter GLYT2 by protein kinase C. Biochem. J. 412, 495-506. (Pubitemid 351846415)
13. Forrest L. R., Tavoulari S., Zhang Y. W., Rudnick G., and, Honig B., (2007) Identification of a chloride ion binding site in Na+/Cl -dependent transporters. Proc. Natl Acad. Sci. USA 104, 12761-12766. (Pubitemid 47255228)
14. Gomeza J., Hulsmann S., Ohno K., Eulenburg V., Szoke K., Richter D., and, Betz H., (2003a) Inactivation of the glycine transporter 1 gene discloses vital role of glial glycine uptake in glycinergic inhibition. Neuron 40, 785-796. (Pubitemid 37431038)
15. Gomeza J., Ohno K., and, Betz H., (2003b) Glycine transporter isoforms in the mammalian central nervous system: structures, functions and therapeutic promises. Curr. Opin. Drug Discov. Devel. 6, 675-682. (Pubitemid 37287936)
16. Gomeza J., Ohno K., Hulsmann S., Armsen W., Eulenburg V., Richter D. W., Laube B., and, Betz H., (2003c) Deletion of the mouse glycine transporter 2 results in a hyperekplexia phenotype and postnatal lethality. Neuron 40, 797-806. (Pubitemid 37431039)
17. Grossman T. R., and, Nelson N., (2003) Effect of sodium lithium and proton concentrations on the electrophysiological properties of the four mouse GABA transporters expressed in Xenopus oocytes. Neurochem. Int. 43, 431-443. (Pubitemid 36561297)
18. Harding M. M., (2002) Metal-ligand geometry relevant to proteins and in proteins: sodium and potassium. Acta Crystallogr. D Biol. Crystallogr. 58, 872-874. (Pubitemid 34557307)
19. Harvey R. J., Topf M., Harvey K., and, Rees M. I., (2008) The genetics of hyperekplexia: more than startle! Trends Genet. 24, 439-447.
20. Humphrey W., Dalke A., and, Schulten K., (1996) VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38, 27-38. (Pubitemid 26152973)
21. Javitt D. C., (2004) Glutamate as a therapeutic target in psychiatric disorders. Mol. Psychiatry 9, 984-997, 979. (Pubitemid 39524288)
22. Jimenez E., Zafra F., Perez-Sen R., Delicado E. G., Miras-Portugal M. T., Aragon C., and, Lopez-Corcuera B., (2011) P2Y purinergic regulation of the glycine neurotransmitter transporters. J. Biol. Chem. 286, 10712-10724.
23. Kanner B. I., (2003) Transmembrane domain I of the gamma-aminobutyric acid transporter GAT-1 plays a crucial role in the transition between cation leak and transport modes. J. Biol. Chem. 278, 3705-3712. (Pubitemid 36801095)
24. Kanner B. I., and, Zomot E., (2008) Sodium-coupled neurotransmitter transporters. Chem. Rev. 108, 1654-1668. (Pubitemid 351796403)
25. Liu Q. R., Lopez-Corcuera B., Mandiyan S., Nelson H., and, Nelson N., (1993) Cloning and expression of a spinal cord- and brain-specific glycine transporter with novel structural features. J. Biol. Chem. 268, 22802-22808. (Pubitemid 23318342)
26. Lopez-Corcuera B., Martinez-Maza R., Nunez E., Roux M., Supplisson S., and, Aragon C., (1998) Differential properties of two stably expressed brain-specific glycine transporters. J. Neurochem. 71, 2211-2219. (Pubitemid 28491580)
27. MacAulay N., Bendahan A., Loland C. J., Zeuthen T., Kanner B. I., and, Gether U., (2001) Engineered Zn(2+) switches in the gamma-aminobutyric acid (GABA) transporter-1. Differential effects on GABA uptake and currents. J. Biol. Chem. 276, 40476-40485.
28. MacAulay N., Zeuthen T., and, Gether U., (2002) Conformational basis for the Li(+)-induced leak current in the rat gamma-aminobutyric acid (GABA) transporter-1. J. Physiol. 544, 447-458. (Pubitemid 35244261)
29. Mager S., Kleinberger-Doron N., Keshet G. I., Davidson N., Kanner B. I., and, Lester H. A., (1996) Ion binding and permeation at the GABA transporter GAT1. J. Neurosci. 16, 5405-5414. (Pubitemid 26277869)
30. Meinild A. K., Loo D. D., Skovstrup S., Gether U., and, MacAulay N., (2009) Elucidating conformational changes in the gamma-aminobutyric acid transporter-1. J. Biol. Chem. 284, 16226-16235.
31. Noskov S. Y., and, Roux B., (2008) Control of ion selectivity in LeuT: two Na+ binding sites with two different mechanisms. J. Mol. Biol. 377, 804-818.
32. Phillips J. C., Braun R., Wang W., Gumbart J., Tajkhorshid E., Villa E., Chipot C., Skeel R. D., Kalé L., and, Schulten K., (2005) Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802. (Pubitemid 43078511)
33. Rees M. I., Harvey K., Pearce B. R., et al. (2006) Mutations in the gene encoding GlyT2 (SLC6A5) define a presynaptic component of human startle disease. Nat. Genet. 38, 801-806. (Pubitemid 43980601)
34. Roux M. J., and, Supplisson S., (2000) Neuronal and glial glycine transporters have different stoichiometries. Neuron 25, 373-383.
35. Sali A., and, Blundell T. L., (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815. (Pubitemid 24007801)
36. Smith K. E., Borden L. A., Hartig P. R., Branchek T., and, Weinshank R. L., (1992) Cloning and expression of a glycine transporter reveal colocalization with NMDA receptors. Neuron 8, 927-935.
37. Tsai G., Ralph-Williams R. J., Martina M., Bergeron R., Berger-Sweeney J., Dunham K. S., Jiang Z., Caine S. B., and, Coyle J. T., (2004) Gene knockout of glycine transporter 1: characterization of the behavioral phenotype. Proc. Natl Acad. Sci. USA 101, 8485-8490. (Pubitemid 38736601)
38. Vandenberg R. J., Shaddick K., and, Ju P., (2007) Molecular basis for substrate discrimination by glycine transporters. J. Biol. Chem. 282, 14447-14453. (Pubitemid 47100462)
39. Wenthur C. J., Rodriguez G. J., Kuntz C. P., and, Barker E. L., (2010) Conformational flexibility of transmembrane helix VII of the human serotonin transporter impacts ion dependence and transport. Biochem. Pharmacol. 80, 1418-1426.
40. Yamashita A., Singh S. K., Kawate T., Jin Y., and, Gouaux E., (2005) Crystal structure of a bacterial homologue of Na+/Cl-dependent neurotransmitter transporters. Nature 437, 215-223. (Pubitemid 41294479)
41. Yee B. K., Balic E., Singer P., et al. (2006) Disruption of glycine transporter 1 restricted to forebrain neurons is associated with a procognitive and antipsychotic phenotypic profile. J. Neurosci. 26, 3169-3181.
42. Zhou Y., Zomot E., and, Kanner B. I., (2006) Identification of a lithium interaction site in the gamma-aminobutyric acid (GABA) transporter GAT-1. J. Biol. Chem. 281, 22092-22099. (Pubitemid 44181913)
43. Zomot E., Bendahan A., Quick M., Zhao Y., Javitch J. A., and, Kanner B. I., (2007) Mechanism of chloride interaction with neurotransmitter:sodium symporters. Nature 449, 726-730. (Pubitemid 47552085)