Regulation of single NMDA receptor channel activity by alpha-actinin and calmodulin in rat hippocampal granule cells

Journal of Physiology

Volumn 557, Issue 3, 2004, Pages 795-808

  Rycroft, Beth K ^a   Gibb, Alasdair J ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; CALCIUM SENSING RECEPTOR; CALMODULIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR SUBUNIT; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHANNEL GATING; CONCENTRATION RESPONSE; CONTROLLED STUDY; GRANULAR CELL; HIPPOCAMPUS; MEMBRANE CHANNEL; MEMBRANE CONDUCTANCE; MEMBRANE CURRENT; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RAT; RECEPTOR BINDING; RECEPTOR OCCUPANCY; REGULATORY MECHANISM; BINDING AFFINITY; BINDING SITE; CELL MEMBRANE CONDUCTANCE; CELL TRANSPORT; GRANULE CELL; MOLECULAR DYNAMICS; PROTEIN DETERMINATION; PROTEIN FUNCTION; SYNAPTIC TRANSMISSION;

ACTININ; ANIMALS; CALMODULIN; CYTOPLASMIC GRANULES; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MEMBRANE POTENTIALS; MITOCHONDRIA; PATCH-CLAMP TECHNIQUES; RABBITS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SUPEROXIDES; SYNAPSES;

EID: 3242698860     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2003.059212     Document Type: Article

References (64)

1. Allison DW, Gelfand VI, Spector I & Craig AM (1998). Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurones. J Neurosci 18, 2423-2436.
2. Anson LC, Schoepfer R, Colquhoun D & Wyllie DJ (2000). Single-channel analysis of an NMDA receptor possessing a mutation in the region of the glutamate binding site. J Physiol 527, 225-237.
3. Banke TG & Traynelis SF (2003). Activation of NR1/NR2B NMDA receptors. Nat Neurosci 6, 144-152.
4. Bear MF & Malenka RC (1994). Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 4, 389-399.
5. Bliss TVP & Collingridge GL (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
6. Bliss TVP & Collingridge GL (1995). Memories of NMDA receptor and LTP. Trends Neurosci 28, 54-56.
7. Carroll RC & Zukin RS (2002). NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity. Trends Neurosci 25, 571-577.
8. Chen L & Huang LY (1992). PKC decreases magnesium block of the NMDA receptor channels as a mechanism of modulation. Nature 356, 521-523.
9. Clapham DE (1995). Calcium signalling. Cell 80, 259-268.
10. Colquhoun D & Sigworth FJ (1995). Fitting and statistical analysis of single-channel records. In Single-Channel Recording, 2nd edn, ed. Sakmann B & Neher E, pp. 483-587. Plenum Press, New York.
11. Edwards FA, Konnerth A, Sakmann B & Takahashi T (1989). A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflugers Arch 414, 600-612.
12. Ehlers MD, Fung ET, O'Brien RJ & Huganir RL (1998). Splice variant-specific interaction of the NMDA receptor subunit NR1 with neuronal intermediate filaments. J Neurosci 18, 720-730.
13. Ehlers MD, Zhang S, Bernhardt JP & Huganir RL (1996). Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 84, 745-755.
14. Fabiato A (1988). Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Meth Enzymol 157, 378-417.
15. Gaertner TR, Putkey JA & Waxham MN (2002). Kinetics of calmodulin binding to RC3/neurogranin. Soc Neuro Abstracts 436, 15.
16. Gibb AJ & Colquhoun D (1991). Glutamate activation of a single NMDA receptor-channel produces a cluster of channel openings. Proc R Soc Lond B Biol Sci 243, 39-45.
17. Gibb AJ & Colquhoun D (1992). Activation of N-methyl-D-aspartate receptors by 1-glutamate in cells dissociated from adult rat hippocampus. J Physiol 456, 143-179.
18. Haiech J, Klee CB & Demaille JG (1981). Effects of cations on affinity of calmodulin: ordered binding of calcium ions allows the specific activation of calmodulin-stimulated enzymes. Biochem 20, 3890-3897.
19. Hisatsune C, Umemori H, Inoue T, Michikawa T, Kohda K, Mikoshiba K et al. (1997). Phosphorylation-dependent regulation of N-methyl-D-aspartate receptors by calmodulin. J Chem Biol 272, 20805-20810.
20. Holmes WR (2000). Models of calmodulin trapping and CaM kinase II activation in a dendritic spine. J Comput Neurosci 81, 65-85.
21. Howe JR, Cull-Candy SG & Colquhoun D (1991). Currents through single glutamate receptor channels in outside-out patches from rat cerebellar granule cells. J Physiol 432, 143-202.
22. James P, Vorherr T & Carafoli E (1995). Calmodulin-binding domains: just two faced or multi-faceted. Trends Biol Sci 20, 38-42.
23. Kakalis LT, Kennedy M, Sikkink R, Rusnak F & Armitage IM (1995). Characterisation of the calcium-binding sites of calcineurin B. FEBS Lett 362, 55-58.
24. Kakiuchi S, Yasuda S, Yamazaki R, Teshima Y, Kanda K, Kakiuchi R et al. (1982). Quantitative determinations of calmodulin in the supernatant and particulate fractions of mammalian tissues. J Biochem (Tokyo) 92, 1041-1048.
25. Kennedy MB (2000). Signal-processing machines at the postsynaptic density. Science 290, 750-754.
26. Kim JH & Huganir RL (1999). Organization and regulation of proteins at synapses. Curr Opin Cell Biol 11, 248-254.
27. 2+ -permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus. J Physiol 485, 383-402.
28. Krupp JJ, Vissel B, Heinemann SF & Westbrook GL (1996). Calcium-dependent inactivation of recombinant N-methyl-D-aspartate receptors is NR2 subunit specific. Mol Pharmacol 50, 1680-1688.
29. Krupp JJ, Vissel B, Thomas CG, Heinemann SF & Westbrook GL (1999). Interactions of calmodulin and α-actinin with the NRJ subunit modulate calcium-dependent inactivation of NMDA receptors. J Neurosci 19, 1165-1178.
30. Lan J-Y, Skeberdis VA, Jover T, Grooms SY, Lin Y, Araneda RC et al. (2001). Protein kinase C modulates NMDA receptor trafficking and gating. Nat Neurosci 4, 382-390.
31. Legendre P, Rosenmund C & Westbrook GL (1993). Inactivation of NMDA channels in cultured hippocampal neurons by intracellular calcium. J Neurosci 13, 674-684.
32. Leonard AS, Bayer KU, Merrill MA, Lim IA, Shea MA, Schulman H et al. (2002). Regulation of calcium/calmodulin-dependent protein kinase II docking to N-methyl-D-aspartate receptors by calcium/calmodulin and alpha-actinin. J Biol Chem 277, 48441-48448.
33. Leonard AS & Hell JW (1997). Cyclic AMP-dependent protein kinase and protein kinase C phosphorylate N-methyl-D-aspartate receptors at different sites. J Biol Chem 272, 12107-12115.
34. Lester RA & Jahr CE (1992). NMDA channel behavior depends on agonist affinity. J Neurosci 12, 635-643.
35. 2+-dependent phosphatase. Nature 369, 235-239.
36. Lin JW, Wyszynski M, Madavan R, Sealock R, Kim JU & Sheng M (1998). Yotiao, a novel protein of neuromuscular junction and brain that interacts with specific splice variants of NMDA receptor subunit NR1. J Neurosci 18, 2017-2027.
37. Lisman JE (1989). A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc Natl Acad Sci USA 86, 9574-9578.
38. 2+ levels affect plasticity differently: the LTP zone, the LTD zone and no man's land. J Physiol 532, 285.
39. Lu WY, Xiong ZG, Lei S, Orser BA, Dudek E, Browning MD et al. (1999). G-protein-coupled receptors act via protein kinase C and Src to regulate NMDA receptors. Nat Neurosci 2, 331-338.
40. Matsuda S & Hirai H (1999). The clustering of NMDA receptor NR1 subunit is regulated by the interaction between the C-terminal exon cassettes and the cytoskeleton. Neurosci Res 34, 157-163.
41. McManus OB, Blatz AL & Magleby KL (1987). Sampling, log binning, fitting, and plotting durations of open and shut intervals from single channels and the effects of noise. Pflugers Arch 410, 530-553.
42. Medina I, Leinekugel X & Ben-Ari Y (1999). Calcium-dependent inactivation of the monosynaptic NMDA EPSCs in rat hippocampal neurons in culture. Eur J Neurosci 11, 2422-2430.
43. Mosior M & Epand RM (1994). Characterisation of the calcium-binding site that regulates association of protein kinase C with phospholipid bilayers. J Biol Chem 19, 13798-13805.
44. Piña-Crespo JC & Gibb AJ (2002). Subtypes of NMDA receptors in new-born rat hippocampal granule cells. J Physiol 541, 41-64.
45. Rafiki A, Gozlan H, Ben-Ari Y, Khrestchatisky M & Medina I (1997). The calcium-dependent transient inactivation of recombinant NMDA receptor-channels does not involve the high affinity calmodulin binding site of the NR1 subunit. Neurosci Lett 223, 137-139.
46. Rosenmund C, Feltz A & Westbrook GL (1995). Calcium-dependent inactivation of synaptic NMDA receptors in hippocampal neurons. J Neurophysiol 73, 427-430.
47. Rosenmund C & Westbrook GL (1993). Calcium-induced actin depolymerisation reduces NMDA channel activity. Neuron 10, 805-814.
48. Rycroft BK & Gibb AJ (2002). Direct effects of calmodulin on NMDA receptor single channel gating in rat hippocampal granule cells. J Neurosci 22, 8860-8868.
49. Sattler R, Xiong Z, Lu WY, MacDonald JF & Tymianski M (2000). Distinct roles of synaptic and extrasynaptic NMDA receptors in excitotoxicity. J Neurosci 20, 22-33.
50. Sigworth FJ & Sine SM (1987). Data transformations from improved display and fitting of single-channel dwell time histograms. Biophys J 52, 1047-1054.
51. Slemmon JR, Feng B & Erhardt JA (2000). Small proteins that modulate calmodulin-dependent signal transduction: effects of PEP-19, neuromodulin, and neurogranin on enzyme activation and cellular homeostasis. Mol Neurobiol 22, 99-113.
52. Tingley WG, Ehlers MD, Kameyama K, Doherty C, Ptak JB, Riley CT et al. (1997). Characterisation of protein kinase A and protein kinase C phosphorylation of the N-methyl-D-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies. J Biol Chem 272, 5157-5166.
53. Tong G & Jahr CE (1994). Regulation of glycine-insensitive desensitisation of the NMDA receptor in outside-out patches. J Neurophysiol 71, 754-761.
54. Tong G, Shepherd D & Jahr CE (1995). Synaptic desensitization of NMDA receptors by calcineurin. Science 267, 1510-1512.
55. Umemiya M, Chen N, Raymond LA & Murphy TH (2001). A calcium-dependent feedback mechanism participates in shaping single NMDA miniature EPSCs. J Neurosci 21, 1-9.
56. 2+-sensitivity of cloned NMDA receptors. Neuropharmacol 35, 29-36.
57. Wechsler A & Teichberg VI (1998). Brain spectrin binding to the NMDA receptor is regulated by phosphorylation, calcium and calmodulin. EMBO J 17, 3931-3939.
58. Weiss DS & Magleby KL (1989). Gating scheme for single GABA-activated Cl-channels determined from stability plots, dwell-time distributions, and adjacent-interval durations. J Neurosci 9, 1314-1324.
59. Wyllie DJ, Behe P & Colquhoun D (1998). Single-channel activations and concentration jumps: comparison of recombinant NR1a/NR2A and NR1a/NR2D NMDA receptors. J Physiol 510, 1-18.
60. Wyszynski M, Kharazia V, Shanghvi R, Rao A, Beggs AH, Craig AM et al. (1998). Differential regional expression and ultra-structural localisation of α-actinin-2 a putative NMDA receptor-anchoring protein, in rat brain. J Neurosci 18, 1383-1392.
61. Wyszynski M, Lin J, Rao A, Nigh E, Beggs AH, Craig AM et al. (1997). Competitive binding of the α-actinin-2 and calmodulin to the NMDA receptor. Nature 385, 439-442.
62. Xiong ZG, Raouf R, Lu WY, Wang LY, Orser BA, Dudek EM et al. (1998). Regulation of N-methyl-D-aspartate receptor function by consitutively active protein kinase C. Mol Pharmacol 54, 1055-1063.
63. Zar JH (1999). Comparing simple linear regression equations. In Biostatistical Analysis, 4th edn, ed. Zar JH, pp. 360-376. Prentice Hall, New Jersey.
64. Zhang S, Ehlers MD, Bernhardt JP, Su C-T & Huganir RL (1998). Calmodulin mediates calcium-dependent inactivation of N-methyl-D-aspartate receptors. Neuron 21, 443-453.