Residues at the tip of the pore loop of NR3B-containing NMDA receptors determine Ca2+ permeability and Mg2+ block

BMC Neuroscience

Volumn 11, Issue , 2010, Pages

  Cavara, Nora A ^a   Orth, Angela ^a   Hicking, Gordon ^a   Seebohm, Guiscard ^a   Hollmann, Michael ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; COMPLEMENTARY RNA; DNA; MAGNESIUM ION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR SUBUNIT; CALCIUM; MAGNESIUM; NR1 NMDA RECEPTOR; NR3B NMDA RECEPTOR;

ANIMAL CELL; ARTICLE; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION; MOLECULAR DYNAMICS; NEUROTRANSMISSION; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; POLYMERASE CHAIN REACTION; RNA SYNTHESIS; SITE DIRECTED MUTAGENESIS; XENOPUS; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; DRUG ANTAGONISM; DRUG EFFECT; ELECTROPHYSIOLOGY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; PERMEABILITY; PHYSIOLOGY; PROTEIN CONFORMATION;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; ELECTROPHYSIOLOGY; HUMANS; MAGNESIUM; MODELS, NEUROLOGICAL; MOLECULAR SEQUENCE DATA; OOCYTES; PERMEABILITY; PROTEIN CONFORMATION; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, COMPLEMENTARY; XENOPUS;

EID: 77957901389     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-11-133     Document Type: Article

References (37)

1. Burnashev N, Schoepfer R, Monyer H, Ruppersberg JP, Gunther W, Seeburg PH, Sakmann B. Control by asparagine residues of calcium permeability and magnesium blockade in the NMDA receptor. Science 1992, 257(5075):1415-1419. 10.1126/science.1382314, 1382314.
2. Sakurada K, Masu M, Nakanishi S. Alteration of Ca2+ permeability and sensitivity to Mg2+ and channel blockers by a single amino acid substitution in the N-methyl-D-aspartate receptor. J Biol Chem 1993, 268(1):410-415.
3. Wollmuth LP, Kuner T, Sakmann B. Adjacent asparagines in the NR2 subunit of the NMDA receptor channel control the voltage-dependent block by extracellular Mg2+. J Physiol 1998, 506(Pt 1):13-32. 10.1111/j.1469-7793.1998.013bx.x, 2230696, 9481670.
4. Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuno N, Nakanishi S. Molecular cloning and characterization of the rat NMDA receptor. Nature 1991, 354(6348):31-37. 10.1038/354031a0, 1834949.
5. Karp SJ, Masu M, Eki T, Ozawa K, Nakanishi S. Molecular cloning and chromosomal localization of the key subunit of the human N-methyl-D-aspartate receptor. J Biol Chem 1993, 268(5):3728-3733.
6. Wollmuth LP, Kuner T, Seeburg PH, Sakmann B. Differential contribution of the NR1- and NR2A-subunits to the selectivity filter of recombinant NMDA receptor channels. J Physiol 1996, 491(Pt 3):779-797. 1158818, 8815211.
7. Ciabarra AM, Sullivan JM, Gahn LG, Pecht G, Heinemann S, Sevarino KA. Cloning and characterization of chi-1: a developmentally regulated member of a novel class of the ionotropic glutamate receptor family. J Neurosci 1995, 15(10):6498-6508.
8. Sucher NJ, Akbarian S, Chi CL, Leclerc CL, Awobuluyi M, Deitcher DL, Wu MK, Yuan JP, Jones EG, Lipton SA. Developmental and regional expression pattern of a novel NMDA receptor-like subunit (NMDAR-L) in the rodent brain. J Neurosci 1995, 15(10):6509-6520.
9. Nishi M, Hinds H, Lu HP, Kawata M, Hayashi Y. Motoneuron-specific expression of NR3B, a novel NMDA-type glutamate receptor subunit that works in a dominant-negative manner. J Neurosci 2001, 21(23):RC185.
10. Andersson O, Stenqvist A, Attersand A, von Euler G. Nucleotide sequence, genomic organization, and chromosomal localization of genes encoding the human NMDA receptor subunits NR3A and NR3B. Genomics 2001, 78(3):178-184. 10.1006/geno.2001.6666, 11735224.
11. Matsuda K, Kamiya Y, Matsuda S, Yuzaki M. Cloning and characterization of a novel NMDA receptor subunit NR3B: a dominant subunit that reduces calcium permeability. Brain Res Mol Brain Res 2002, 100(1-2):43-52. 10.1016/S0169-328X(02)00173-0, 12008020.
12. Matsuda K, Fletcher M, Kamiya Y, Yuzaki M. Specific assembly with the NMDA receptor 3B subunit controls surface expression and calcium permeability of NMDA receptors. J Neurosci 2003, 23(31):10064-10073.
13. Sasaki YF, Rothe T, Premkumar LS, Das S, Cui J, Talantova MV, Wong HK, Gong X, Chan SF, Zhang D, Nakanishi N, Sucher NJ, Lipton SA. Characterization and comparison of the NR3A subunit of the NMDA receptor in recombinant systems and primary cortical neurons. J Neurophysiol 2002, 87(4):2052-2063.
14. Tong G, Takahashi H, Tu S, Shin Y, Talantova M, Zago W, Xia P, Nie Z, Goetz T, Zhang D, Lipton SA, Nakanishi N. Modulation of NMDA receptor properties and synaptic transmission by the NR3A subunit in mouse hippocampal and cerebrocortical neurons. J Neurophysiol 2008, 99(1):122-132. 10.1152/jn.01044.2006, 18003876.
15. Chatterton JE, Awobuluyi M, Premkumar LS, Takahashi H, Talantova M, Shin Y, Cui J, Tu S, Sevarino KA, Nakanishi N, Sucher NJ, Lipton SA. Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 2002, 415(6873):793-798.
16. Yamakura T, Askalany AR, Petrenko AB, Kohno T, Baba H, Sakimura K. The NR3B subunit does not alter the anesthetic sensitivities of recombinant N-methyl-D-aspartate receptors. Anesth Analg 2005, 100(6):1687-1692. 10.1213/01.ANE.0000152324.30272.49, 15920196.
17. Liman ER, Tytgat J, Hess P. Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs. Neuron 1992, 9(5):861-871. 10.1016/0896-6273(92)90239-A, 1419000.
18. Villmann C, Strutz N, Morth T, Hollmann M. Investigation by ion channel domain transplantation of rat glutamate receptor subunits, orphan receptors and a putative NMDA receptor subunit. Eur J Neurosci 1999, 11(5):1765-1778. 10.1046/j.1460-9568.1999.00594.x, 10215929.
19. Iino M, Ozawa S, Tsuzuki K. Permeation of calcium through excitatory amino acid receptor channels in cultured rat hippocampal neurones. J Physiol 1990, 424:151-165. 1189806, 1697342.
20. Egebjerg J, Heinemann SF. Ca2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc Natl Acad Sci USA 1993, 90(2):755-759. 10.1073/pnas.90.2.755, 45744, 7678465.
21. Cavara NA, Orth A, Hollmann M. Effects of NR1 splicing on NR1/NR3B-type excitatory glycine receptors. BMC Neurosci 2009, 10:32. 10.1186/1471-2202-10-32, 2669480, 19348678.
22. Altschul SF, Madden TL, Schaeffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
23. Krieger E, Joo K, Lee J, Raman S, Thompsn J, Tyka M, Baker D, Karplus K. Improving physical realism, stereochemistry and side-chain accuracy in homology modeling: Four approaches that performed well in CASP8. Proteins 2009, 77(Suppl 9):114-122. 2922016, 19768677.
24. Hooft RW, Vriend G, Sander C, Abola EE. Errors in protein structures. Nature 1996, 381(6580):272. 10.1038/381272a0, 8692262.
25. Hooft RW, Sander C, Vriend G. The PDBFINDER database: A summary of PDB, DSSP and HSSP information with added value. CABIOS/Bioinformatics 1996, 12:525-529.
26. King RD, Sternberg MJE. Identification and application of the concepts important for accurate and reliable protein secondary structure prediction. Prot Sci 1996, 5:2298-2310.
27. Qiu J, Elber R. SSALN: An alignment algorithm using structure-dependent substitution matrices and gap penalties learned from structurally aligned protein pairs. Proteins 2006, 62:881-891. 10.1002/prot.20854, 16385554.
28. Canutescu AA, Shelenkov AA, Dunbrack RL. A graph-theory algorithm for rapid proteins side chain prediction. Prot Sci 2003, 12:2001-2014.
29. Krieger E, Darden T, Nabuurs S, Finkelstein A, Vriend G. Making optimal use of empirical energy functions: force field parameterization in crystal space. Proteins 2004, 57:678-683. 10.1002/prot.20251, 15390263.
30. Duan Y, Wu C, Chowdhury S, Lee MC, Xiong G, Zhang W, Yang R, Cieplak P, Luo R, Lee T. A Point-Charge Force Field for Molecular Mechanics Simulations of Proteins. J.Comput.Chem 2003, 24:1999-2012. 10.1002/jcc.10349, 14531054.
31. Schmidt C, Hollmann M. Molecular and functional characterization of Xenopus laevis N-methyl-d-aspartate receptors. Mol Cell Neurosci 2009, 42(2):116-127. 10.1016/j.mcn.2009.06.004, 19524674.
32. Wada A, Takahashi H, Lipton SA, Chen HS. NR3A modulates the outer vestibule of the "NMDA" receptor channel. J Neurosci 2006, 26(51):13156-13166. 10.1523/JNEUROSCI.2552-06.2006, 17182766.
33. Madry C, Mesic I, Bartholomäus I, Nicke A, Betz H, Laube B. Principal role of NR3 subunits in NR1/NR3 excitatory glycine receptor function. BBRC 2007, 453(1):102-108.
34. Ulbrich MH, Isacoff EY. Rules of engagement for NMDA receptor subunits. PNAS 2008, 105(37):14163-14168. 10.1073/pnas.0802075105, 2544595, 18779583.
35. Meddows E, Le Bourdelles B, Grimwood S, Wafford K, Sandhu S, Whiting P, McIlhinney RA. Identification of molecular determinants that are important in the assembly of N-methyl-D-aspartate receptors. J Biol Chem 2001, 276(22):18795-18803. 10.1074/jbc.M101382200, 11279200.
36. Das S, Sasaki YF, Rothe T, Premkumar LS, Takasu M, Crandall JE, Dikkes P, Conner DA, Rayudu PV, Cheung W, Chen HS, Lipton SA, Nakanishi N. Increased NMDA current and spine density in mice lacking the NMDA receptor subunit NR3A. Nature 1998, 393(6683):377-381. 10.1038/30748, 9620802.
37. Perez-Otano I, Schulteis CT, Contractor A, Lipton SA, Trimmer JS, Sucher NJ, Heinemann SF. Assembly with the NR1 subunit is required for surface expression of NR3A-containing NMDA receptors. J Neurosci 2001, 21(4):1228-1237.