Direct effects of calmodulin on NMDA receptor single-channel gating in rat hippocampal granule cells

Journal of Neuroscience

Volumn 22, Issue 20, 2002, Pages 8860-8868

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

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Calmodulin; Dentate gyrus; Granule cells; Hippocampus; NMDA receptors; Patch clamp; Postnatal development; Rat brain

Indexed keywords

ALPHA ACTININ; CALCINEURIN; CALCIUM; CALMODULIN; GLUTAMIC ACID; ION CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE C;

AMPLITUDE MODULATION; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CHANNEL GATING; CONTROLLED STUDY; DENTATE GYRUS; GRANULE CELL; HIPPOCAMPUS; NERVE CELL PLASTICITY; NEWBORN; NONHUMAN; PATCH CLAMP; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

EID: 0037109755     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-20-08860.2002     Document Type: Article

References (55)

1. 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 (Lond) 527:225-237.
2. 2+. Proc Natl Acad Sci USA 96:14571-14576.
3. Ascher P, Nowak L (1988) The role of divalent cations in the N-methyl-D-aspartate responses of mouse central neurones in culture. J Physiol (Lond) 399:247-266.
4. Bear MF, Malenka RC (1994) Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 4:389-399.
5. Benveniste M, Clements J, Vyklicky Jr L, Mayer ML (1990) A kinetic analysis of the modulation of N-methyl-D-aspartic acid receptors by glycine in mouse cultured hippocampal neurones. J Physiol (Lond) 428:333-357.
6. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361:31-39.
7. Bliss TVP, Collingridge GL (1995) Memories of NMDA receptors and LTP. Trends Neurosci 28:54-56.
8. Chen L, Huang LY (1992) Protein kinase C decreases magnesium block of the NMDA receptor channels as a mechanism of modulation. Nature 356:521-523.
9. Clements JD, Westbrook GL (1991) Activation kinetics reveal the number of glutamate and glycine binding sites on the N-methyl-D-aspartate receptor. Neuron 7:605-613.
10. Colquhoun D, Hawkes AG (1995) A Q-matrix cookbook: How to write only one program to calculate the single channel and macroscopic predictions for any kinetic mechanism. In: Single-Channel Recording, Ed 2 (Sakmann B, Neher E, eds), pp 589-636. New York: Plenum.
11. Colquhoun D, Sakmann B (1985) Fast events in single-channel currents activated by acetylcholine and its analogues at the frog muscle endplate. J Physiol (Lond) 369:501-557.
12. Colquhoun D, Sigworth FJ (1995) Fitting and statistical analysis of single-channel records. In: Single-Channel Recording, Ed 2 (Sakmann B, Neher E, eds), pp 483-587. New York: Plenum.
13. 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. Pflügers Arch 414:600-612.
14. 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.
15. 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. Methods Enzymol 157:378-417.
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 L-glutamate in cells dissociated from adult rat hippocampus. J Physiol (Lond) 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. Biochemistry 20:3890-3897.
19. Hestrin S, Nicoll RA, Perkel DJ, Sah P (1990a) Analysis of excitatory synaptic action in the rat hippocampus using whole-cell recording from thin slices. J Physiol (Lond) 422:515-533.
20. Hestrin S, Sah P, Nicoll RA (1990b) Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices. Neuron 5:247-253.
21. Hisatsune C, Umemori H, Inoue T, Michikawa T, Kohda K, Mikoshiba K, Yamamoto T (1997) Phosphorylation-dependent regulation of N-methyl-D-aspartate receptors by calmodulin. J Biol Chem 272:20805-20810.
22. Jahr CE (1992) High probability opening of NMDA receptor channels by L-glutamate. Science 255:470-472.
23. James P, Vorherr T, Carafoli E (1995) Calmodulin-binding domains: Just two faced or multi-faceted. Trends Biochem Sci 20:38-42.
24. Kennedy MB (2000) Signal-processing machines at the postsynaptic density. Science 290:750-754.
25. Kim JH, Huganir RL (1999) Organization and regulation of proteins at synapses. Curr Opin Cell Biol 11:248-254.
26. 2+-permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus. J Physiol (Lond) 485:383-402.
27. Krupp JJ, Vissel B, Thomas CG, Heinemann SF, Westbrook GL (1999) Interactions of calmodulin and α-actinin with the NR1 subunit modulate calcium-dependent inactivation of NMDA receptors. J Neurosci 19:1165-1178.
28. Lan J-Y, Skeberdis VA, Jover T, Grooms SY, Lin Y, Araneda RC, Zheng X, Bennett MVL, Zukin RS (2001) Protein kinase C modulates NMDA receptor trafficking and gating. Nat Neurosci 4:382-390.
29. 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.
30. Lester RA, Jahr CE (1992) NMDA channel behavior depends on agonist affinity. J Neurosci 12:635-643.
31. Lester RA, Clements JD, Westbrook GL, Jahr CE (1990) Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents. Nature 346:565-567.
32. 2+-dependent phosphatase. Nature 369:235-239.
33. Lu W-Y, Jackson MF, Bai D, Orser BA, MacDonald JF (2000) In CA1 pyramidal neurons of the hippocampus protein kinase C regulates calcium-dependent inactivation of NMDA receptors. J Neurosci 20:4452-4461.
34. MacDermott AB, Mayer ML, Westbrook GL, Smith SJ, Barker JL (1986) NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321:519-522.
35. Markram H, Lubke J, Frotscher M, Sakman B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213-215.
36. Mayer ML, Westbrook GL (1987) The action of N-methyl-D-aspartic acid on mouse spinal neurones in culture. J Physiol (Lond) 361:65-90.
37. 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. Pflügers Arch 410:530-553.
38. 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.
39. Rafiki A, Gozlan H, Ben-Ari Y, Khrestchatisky M, Medina I (1997) The calcium-dependent transient inactivation of recombinant NMDA receptor-channel does not involve the high affinity calmodulin binding site of the NR1 subunit. Neurosci Lett 223:137-139.
40. Rosenmund C, Feltz A, Westbrook GL (1995) Calcium-dependent inactivation of synaptic NMDA receptors in hippocampal neurons. J Neurophysiol 73:427-430.
41. Sather W, Dieudonne S, MacDonald JF, Ascher P (1992) Activation and desensitization of N-methyl-D-aspartate receptors in nucleated outsideout patches from mouse neurones. J Physiol (Lond) 450:643-672.
42. Schneggenburger R, Zhou Z, Konnerth A, Neher E (1993) Fractional contribution of calcium to the cation current through glutamate receptor channels. Neuron 11:133-143.
43. Sheng M, Pak DT (2000) Ligand-gated ion channel interactions with cytoskeletal and signalling proteins. Annu Rev Physiol 62:755-778.
44. Sigworth FJ, Sine SM (1987) Data transformations from improved display and fitting of single-channel dwell time histograms. Biophys J 52:1047-1054.
45. Strecker GJ, Jackson MB, Dudek FE (1994) Blockade of NMDA-activated channels by magnesium in the immature rat hippocampus. J Neurophysiol 72:1538-1548.
46. Tingley WG, Ehlers MD, Kameyama K, Doherty C, Ptak JB, Riley CT, Huganir RL (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.
47. Tong G, Jahr CE (1994) Regulation of glycine-insensitive desensitisation of the NMDA receptor in outside-out patches. J Neurophysiol 71:754-761.
48. Tong G, Shepherd D, Jahr CE (1995) Synaptic desensitization of NMDA receptors by calcineurin. Science 267:1510-1512.
49. 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.
50. 2+-sensitivity of cloned NMDA receptors. Neuropharmacology 35:29-36.
51. 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.
52. 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 (Lond) 510:1-18.
53. Wyszynski M, Lin J, Rao A, Nigh E, Beggs AH, Craig AM, Sheng M (1997) Competitive binding of the α-actinin-2 and calmodulin to the NMDA receptor. Nature 385:439-442.
54. Xiong ZG, Raouf R, Lu WY, Wang LY, Orser BA, Dudek EM, Browning MD, MacDonald JF (1998) Regulation of N-methyl-D-aspartate receptor function by constitutively active protein kinase C. Mol Pharmacol 54:1055-1063.
55. 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.