Single particle tracking of α7 nicotinic AChR in hippocampal neurons reveals regulated confinement at glutamatergic and GABAergic perisynaptic sites

PLoS ONE

Volumn 5, Issue 7, 2010, Pages 1-14

  Bürli, Thomas ^a   Baer, Kristin ^b   Ewers, Helge ^c   Sidler, Corinne ^a   Fuhrer, Christian ^a   Fritschy, Jean Marc ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b SWANSEA UNIVERSITY   (United Kingdom)

^c ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BUNGAROTOXIN RECEPTOR; QUANTUM DOT; 4 AMINOBUTYRIC ACID; BUNGAROTOXIN; FUSED HETEROCYCLIC RINGS; GLUTAMIC ACID; LATRUNCULIN A; NICOTINIC RECEPTOR; NOCODAZOLE; THIAZOLIDINE DERIVATIVE;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL AGGREGATION; CELL CULTURE; CHOLINERGIC SYNAPSE; CONTROLLED STUDY; CYTOSKELETON; DIFFUSION COEFFICIENT; EMBRYO; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; HIPPOCAMPUS; IMMUNOFLUORESCENCE TEST; INTERNEURON; MICROTUBULE; NERVE CELL; NERVE CELL INHIBITION; NONHUMAN; POSTSYNAPTIC MEMBRANE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS; RAT; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; CYTOLOGY; DRUG EFFECT; FEMALE; IMMUNOHISTOCHEMISTRY; METABOLISM; MICROSCOPY; PREGNANCY; SYNAPSE; WISTAR RAT;

ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; BUNGAROTOXINS; CELLS, CULTURED; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICROSCOPY; NEURONS; NOCODAZOLE; PREGNANCY; QUANTUM DOTS; RATS; RATS, WISTAR; RECEPTORS, NICOTINIC; SYNAPSES; THIAZOLIDINES;

EID: 77955397870     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011507     Document Type: Article

References (60)

1. Couturier S, Bertrand D, Matter JM, Hernandez MC, Bertrand S, et al. (1990) A neuronal nicotinic acetylcholine receptor subunit (alpha7) is developmentally regulated and forms a homo-oligomeric channel blocked by alpha-Btx. Neuron 5: 847-856.
2. Bertrand D, Galzi JL, Devillers-Thiery A, Bertrand S, Changeux JP (1993) Stratification of the channel domain in neurotransmitter receptors. Cur Opin Cell Biol 5: 688-693.
3. Seguela P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW (1993) Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium. J Neurosci 13: 596-604.
4. Jones S, Sudweeks S, Yakel JL (1999) Nicotinic receptors in the brain: correlating physiology with function. Trends Neurosci 22: 555-561.
5. Chen D, Patrick JW (1997) The alpha-bungarotoxin-binding nicotinic acetylcholine receptor from rat brain contains only the alpha7 subunit. J Biol Chem 272: 24024-24029.
6. Levin ED, McClernon FJ, Rezvani AH (2006) Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacol 184: 523-539.
7. Van Kampen M, Selbach K, Schneider R, Schiegel E, Boess F, et al. (2004) ARR 17779 improves social recognition in rats by activation of nicotinic alpha7 receptors. Psychopharmacol 172: 375-383.
8. Young JW, Crawford N, Kelly JS, Kerr LE, Marston HM, et al. (2007) Impaired attention is central to the cognitive deficits observed in alpha 7 deficient mice. Eur Neuropsychopharmacol 17: 145-155.
9. Cincotta SL, Yorek MS, Moschak TM, Lewis SR, Rodefer JS (2008) Selective nicotinic acetylcholine receptor agonists: potential therapies for neuropsychiatric disorders with cognitive dysfunction. Curr Opin Investig Drugs 9: 47-56.
10. Freedman R, Wetmore C, Stromberg I, Leonard S, Olson L (1993) Alphabungarotoxin binding to hippocampal interneurons: immunocytochemical characterization and effects on growth factor expression. J Neurosci 13: 1965-1975.
11. Frazier CJ, Buhler AV, Weiner JL, Dunwiddie TV (1998) Synaptic potentials mediated via alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors in rat hippocampal interneurons. J Neurosci 18: 8228-8235.
12. Frazier CJ, Strowbridge BW, Papke RL (2003) Nicotinic receptors on local circuit neurons in dentate gyrus: a potential role in regulation of granule cell excitability. J Neurophysiol 89: 3018-3028.
13. Fabian-Fine R, Skehel P, Errington ML, Davies HA, Sher E, et al. (2001) Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus. J Neurosci 21: 7993-8003.
14. Levy RB, Aoki C (2002) Alpha7 nicotinic acetylcholine receptors occur at postsynaptic densities of AMPA receptor-positive and -negative excitatory synapses in rat sensory cortex. J Neurosci 22: 5001-5015.
15. Alkondon M, Pereira EF, Barbosa CT, Albuquerque EX (1997) Neuronal nicotinic acetylcholine receptor activation modulates gamma-aminobutyric acid release from CA1 neurons of rat hippocampal slices. J Pharmacol Exp Ther 283: 1396-1411.
16. Li X, Rainnie DG, McCarley RW, Greene RW (1998) Presynaptic nicotinic receptors facilitate monoaminergic transmission. J Neurosci 18: 1904-1912.
17. Maggi L, Sher E, Cherubini E (2001) Regulation of GABA release by nicotinic acetylcholine receptors in the neonatal rat hippocampus. J Physiol 536: 89-100.
18. McGehee DS, Heath MJ, Gelber S, Devay P, Role LW (1995) Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269: 1692-1696.
19. Kawai H, Zago W, Berg DK (2002) Nicotinic alpha 7 receptor clusters on hippocampal GABAergic neurons: regulation by synaptic activity and neurotrophins. J Neurosci 22: 7903-7912.
20. Baer K, Bürli T, Huh KH, Wiesner A, Erb-Vögtli S, et al. (2007) PICK1 interacts with α7 neuronal nicotinic acetylcholine receptors and controls their clustering. Mol Cell Neurosci 35: 339-355.
21. Renner M, Specht CG, Triller A (2008) Molecular dynamics of postsynaptic receptors and scaffold proteins. Curr Opin Neurobiol 18: 532-540.
22. Newpher TM, Ehlers MD (2008) Glutamate receptor dynamics in dendritic microdomains. Neuron 58: 472-497.
23. Triller A, Choquet D (2008) New concepts in synaptic biology derived from single-molecule imaging. Neuron 59: 359-374.
24. Blanpied TA, Scott DB, Ehlers MD (2002) Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron 36: 435-449.
25. Racz B, Blanpied TA, Ehlers MD, Weinberg RJ (2004) Lateral organization of endocytic machinery in dendritic spines. Nature Neurosci 7: 917-918.
26. Lu J, Helton TD, Blanpied TA, Racz B, Newpher TM, et al. (2007) Postsynaptic positioning of endocytic zones and AMPA receptor cycling by physical coupling of dynamin-3 to Homer. Neuron 55: 874-889.
27. Groc L, Choquet D (2008) Measurement and characteristics of neurotransmitter receptor surface trafficking. Mol Membr Biol 25: 344-352.
28. Heine M, Groc L, Frischknecht R, Beique JC, Lounis B, et al. (2008) Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science 320: 201-205.
29. Groc L, Heine M, Cognet L, Brickley K, Stephenson FA, et al. (2004) Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nat Neurosci 7: 695-696.
30. Alcor D, Gouzer G, Triller A (2009) Single-particle tracking methods for the study of membrane receptors dynamics. Eur J Neurosci 30: 987-997.
31. Ehlers MD, Heine M, Groc L, Lee MC, Choquet D (2007) Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron 54: 447-460.
32. Lévi S, Schweizer C, Bannai H, Pascual O, Charrier C, et al. (2008) Homeostatic regulation of synaptic GlyR numbers driven by lateral diffusion. Neuron 59: 261-273.
33. Charrier C, Ehrensperger MV, Dahan M, Lévi S, Triller A (2006) Cytoskeleton regulation of glycine receptor number at synapses and diffusion in the plasma membrane. J Neurosci 26: 8502-8511.
34. Buerli T, Pellegrino C, Baer K, Lardi-Studler B, Chudotvorova I, et al. (2007) Efficient transfection of DNA or shRNA vectors into neurons using magnetofection. Nature Protocols 2: 3090-3101.
35. Bats C, Groc L, Choquet D (2007) The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 53: 719-734.
36. Lardi-Studler B, Smolinsky B, Petitjean CM, Koenig F, Sidler C, et al. (2007) Vertebrate-specific sequences in the gephyrin E-domain regulate cytosolic aggregation and postsynaptic clustering. J Cell Sci 120: 1371-1382.
37. Sage D, Neumann FR, Hediger F, Gasser SM, Unser M (2005) Automatic tracking of individual fluorescence particles: application to the study of chromosome dynamics. IEEE Trans Image Process 14: 1372-1383.
38. Sbalzarini IF, Koumoutsakos P (2005) Feature point tracking and trajectory analysis for video imaging in cell biology. J Struct Biol 151: 182-195.
39. Saxton MJ, Jacobson K (1997) Single-particle tracking: applications to membrane dynamics. Annu Rev Biophys Biomol Struct 26: 373-399.
40. Meier J, Vannier C, Sergé A, Triller A, Choquet D (2001) Fast and reversible trapping of surface glycine receptors by gephyrin. Nature Neurosci 4: 253-260.
41. Simson R, Sheets ED, Jacobson K (1995) Detection of temporary lateral confinement of membrane proteins using single-particle tracking analysis. Biophys J 69: 989-993.
42. Kusumi A, Sako Y, Yamamoto M (1993) Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys J 65: 2021-2040.
43. Fritschy JM, Harvey RJ, Schwarz G (2008) Gephyrin: where do we stand, where do we go? Trends Neurosci 31: 257-264.
44. Xiao B, Tu JC, Petralia RS, Yuan JP, Doan A, et al. (1998) Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of homer-related, synaptic proteins. Neuron 21: 707-716.
45. Gulyas AI, Megias M, Emri Z, Freund TF (1999) Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus. J Neurosci 19: 10082-10097.
46. Ward JM, Cockcroft VB, Lunt GG, Smillie FS, Wonnacott S (1990) Methyllycaconitine: a selective probe for neuronal alpha-bungarotoxin binding sites. FEBS Lett 270: 45-48.
47. Allison DW, Gelfand VI, Spector I, Craig AM (1998) Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J Neurosci 18: 2423-2436.
48. Ehrensperger MV, Hanus C, Vannier C, Triller A, Dahan M (2007) Multiple association states between glycine receptors and gephyrin identified by SPT analysis. Biophys J 92: 3706-3718.
49. Dahan M, Levi S, Luccardini C, Rostaing P, Riveau B, et al. (2003) Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science 302: 442-445.
50. Groc L, Lafourcade M, Heine M, Renner M, Racine V, et al. (2007) Surface trafficking of neurotransmitter receptor: comparison between single-molecule/quantum dot strategies. J Neurosci 27: 12433-12437.
51. Tardin C, Cognet L, Bats C, Lounis B, Choquet D (2003) Direct imaging of lateral movements of AMPA receptors inside synapses. Embo J 22: 4656-4665.
52. Hanley JG (2008) PICK1: a multi-talented modulator of AMPA receptor trafficking. Pharmacol Ther 118: 152-160.
53. Bennett V, Gilligan DM (1993) The spectrin-based membrane skeleton and micron-scale organization of the plasma membrane. Annu Rev Cell Biol 9: 27-66.
54. Bruses JL, Chauvet N, Rutishauser U (2001) Membrane lipid rafts are necessary for the maintenance of the (alpha)7 nicotinic acetylcholine receptor in somatic spines of ciliary neurons. J Neurosci 21: 504-512.
55. Wanaverbecq N, Semyanov A, Pavlov I, Walker MC, Kullmann DM (2007) Cholinergic axons modulate GABAergic signaling among hippocampal interneurons via postsynaptic alpha 7 nicotinic receptors. J Neurosci 27: 5683-5693.
56. Rozsa B, Katona G, Kaszas A, Szipocs R, Vizi ES (2008) Dendritic nicotinic receptors modulate backpropagating action potentials and long-term plasticity of interneurons. Eur J Neurosci 27: 364-377.
57. Dani JA, Bertrand D (2007) Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu Rev Pharmacol Toxicol 47: 699-729.
58. Zhang J, Berg DK (2007) Reversible inhibition of GABAA receptors by alpha7-containing nicotinic receptors on the vertebrate postsynaptic neurons. J Physiol 579: 753-763.
59. Gaiarsa JL, Caillard O, Ben-Ari Y (2002) Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance. Trends Neurosci 25: 564-570.
60. Nugent FS, Kauer JA (2008) LTP of GABAergic synapses in the ventral tegmental area and beyond. J Physiol 586: 1487-1493.