Stargazin attenuates intracellular polyamine block of calcium-permeable AMPA receptors

Nature Neuroscience

Volumn 10, Issue 10, 2007, Pages 1260-1267

  Soto, David ^a   Coombs, Ian D ^a   Kelly, Leah ^a   Farrant, Mark ^a   Cull Candy, Stuart G ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE RECEPTOR; MEMBRANE PROTEIN; POLYAMINE DERIVATIVE; REGULATOR PROTEIN; STARGAZIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CEREBELLUM CORTEX; CHANNEL GATING; CONTROLLED STUDY; CYTOPLASM; DESENSITIZATION; EXCITATORY POSTSYNAPTIC POTENTIAL; HUMAN; HUMAN CELL; INTRACELLULAR MEMBRANE; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CALCIUM; CALCIUM CHANNELS; CEREBELLUM; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; HUMANS; ION CHANNEL GATING; MEMBRANE POTENTIALS; NEURONS; PATCH-CLAMP TECHNIQUES; POLYAMINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, GLUTAMATE; SPERMINE; TRANSFECTION;

EID: 34748849546     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1966     Document Type: Article

References (50)

1. Seeburg, P.H. & Hartner, J. Regulation of ion channel/ neurotransmitter receptor function by RNA editing. Curr. Opin. Neurobiol. 13, 279-283 (2003).
2. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193-204 (1995).
3. Swanson, G.T., Kamboj, S.K. & Cull-Candy, S.G. Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J. Neurosci. 17, 58-69 (1997).
4. Feldmeyer, D. et al. Neurological dysfunctions in mice expressing different levels of the Q/R site-unedited AMPAR subunit GluR-B. Nat. Neurosci. 2, 57-64 (1999).
5. Bowie, D. & Mayer, M.L. Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 15, 453-462 (1995).
6. Kamboj, S.K., Swanson, G.T. & Cull-Candy, S.G. Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J. Physiol. (Lond.) 486, 297-303 (1995).
7. 2+-permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification. J. Physiol. (Lond.) 486, 305-312 (1995).
8. Bowie, D., Lange, G.D. & Mayer, M.L. Activity-dependent modulation of glutamate receptors by polyamines. J. Neurosci. 18, 8175-8185 (1998).
9. Rozov, A. & Burnashev, N. Polyamine-dependent facilitation of postsynaptic AMPA receptors counteracts paired-pulse depression. Nature 401, 594-598 (1999).
10. Plant, K. et al. Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 9, 602-604 (2006).
11. Adesnik, H. & Nicoll, R.A. Conservation of glutamate receptor 2-containing AMPA receptors during long-term potentiation. J. Neurosci. 27, 4598-4602 (2007).
12. Colbourne, F., Grooms, S.Y., Zukin, R.S., Buchan, A.M. & Bennett, M.V. Hypothermia rescues hippocampal CA1 neurons and attenuates downregulation of the AMPA receptor GluR2 subunit after forebrain ischemia. Proc. Natl. Acad. Sci. USA 100, 2906-2910 (2003).
13. Kawahara, Y. et al. Glutamate receptors: RNA editing and death of motor neurons. Nature 427, 801 (2004).
14. Kwak, S. & Weiss, J.H. Calcium-permeable AMPA channels in neurodegenerative disease and ischemia. Curr. Opin. Neurobiol. 16, 281-287 (2006).
15. 2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr. Opin. Neurobiol. 16, 288-297 (2006).
16. Liu, S.Q. & Cull-Candy, S.G. Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 405, 454-458 (2000).
17. Lei, S. & McBain, C.J. Distinct NMDA receptors provide differential modes of transmission at mossy fiber-interneuron synapses. Neuron 33, 921-933 (2002).
18. Gardner, S.M. et al. Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF. Neuron 45, 903-915 (2005).
19. Bellone, C. & Luscher, C. Cocaine triggered AMPA receptor redistribution is reversed in vivo by mGluR-dependent long-term depression. Nat. Neurosci. 9, 636-641 (2006).
20. Chen, L. et al. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408, 936-943 (2000).
21. Nicoll, R.A., Tomita, S. & Bredt, D.S. Auxiliary subunits assist AMPA-type glutamate receptors. Science 311, 1253-1256 (2006).
22. Ziff, E.B. TARPs and the AMPA receptor trafficking paradox. Neuron 53, 627-633 (2007).
23. Bats, C., Groc, L. & Choquet, D. The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 53, 719-734 (2007).
24. Tomita, S., Fukata, M., Nicoll, R.A. & Bredt, D.S. Dynamic interaction of stargazin-like TARPs with cycling AMPA receptors at synapses. Science 303, 1508-1511 (2004).
25. Priel, A. et al. Stargazin reduces desensitization and slows deactivation of the AMPA-type glutamate receptors. J. Neurosci. 25, 2682-2686 (2005).
26. Tomita, S. et al. Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 435, 1052-1058 (2005).
27. Turetsky, D., Garringer, E. & Patneau, D.K. Stargazin modulates native AMPA receptor functional properties by two distinct mechanisms. J. Neurosci. 25, 7438-7448 (2005).
28. Bedoukian, M.A., Weeks, A.M. & Partin, K.M. Different domains of the AMPA receptor direct stargazin-mediated trafficking and stargazin-mediated modulation of kinetics. J. Biol. Chem. 281, 23908-23921 (2006).
29. Kott, S., Werner, M., Korber, C. & Hollmann, M. Electrophysiological properties of AMPA receptors are differentially modulated depending on the associated member of the TARP family. J. Neurosci. 27, 3780-3789 (2007).
30. Yamazaki, M. et al. A novel action of stargazin as an enhancer of AMPA receptor activity. Neurosci. Res. 50, 369-374 (2004).
31. 2+ permeability of AMPARs at cerebellar synapses. Nat. Neurosci. 8, 768-775 (2005).
32. Sharp, A.H. et al. Biochemical and anatomical evidence for specialized voltage-dependent calcium channel γ isoform expression in the epileptic and ataxic mouse, stargazer. Neuroscience 105, 599-617 (2001).
33. Tomita, S. et al. Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J. Cell Biol. 161, 805-816 (2003).
34. V2.1 voltage-dependent calcium channels expressed in Xenopus oocytes. BMC Neurosci. 4, 23 (2003).
35. Cu, C., Bahring, R. & Mayer, M.L. The role of hydrophobic interactions in binding of polyamines to non-NMDA receptor ion channels. Neuropharmacology 37, 1381-1391 (1998).
36. 2+-permeable AMPA receptor channels by activity-dependent relief from polyamine block. J. Physiol. (Lond.) 511, 361-377 (1998).
37. Keinanen, K. et al. A family of AMPA-selective glutamate receptors. Science 249, 556-560 (1990).
38. Petralia, R.S., Wang, Y.X., Mayat, E. & Wenthold, R.J. Glutamate receptor subunit 2-selective antibody shows a differential distribution of calcium-impermeable AMPA receptors among populations of neurons. J. Comp. Neurol. 385, 456-476 (1997).
39. Traynelis, S.F., Silver, R.A. & Cull-Candy, S.G. Estimated conductance of glutamate receptor channels activated during EPSCs at the cerebellar mossy fiber-granule cell synapse. Neuron 11, 279-289 (1993).
40. Soler-Llavina, G.J. & Sabatini, B.L. Synapse-specific plasticity and compartmentalized signaling in cerebellar stellate cells. Nat. Neurosci. 9, 798-806 (2006).
41. Beierlein, M. & Regehr, W.G. Local interneurons regulate synaptic strength by retrograde release of endocannabinoids. J. Neurosci. 26, 9935-9943 (2006).
42. Shin, J., Shen, F. & Huguenard, J.R. Polyamines modulate AMPA receptor-dependent synaptic responses in immature layer V pyramidal neurons. J. Neurophysiol. 93, 2634-2643 (2005).
43. Aizenman, C.D., Munoz-Elias, G. & Cline, H.T. Visually driven modulation of glutamatergic synaptic transmission is mediated by the regulation of intracellular polyamines. Neuron 34, 623-634 (2002).
44. Jonas, P. The time course of signaling at central glutamatergic synapses. News Physiol. Sci. 15, 83-89 (2000).
45. Lawrence, J.J. & McBain, C.J. Interneuron diversity series: containing the detonation-feedforward inhibition in the CA3 hippocampus. Trends Neurosci. 26, 631-640 (2003).
46. Bischofberger, J. & Jonas, P. TwoB or not twoB: differential transmission at glutamatergic mossy fiber-interneuron synapses in the hippocampus. Trends Neurosci. 25, 600-603 (2002).
47. Colquhoun, D., Jonas, P. & Sakmann, B. Action of brief pulses of glutamate on AMPA/kainate receptors in patches from different neurones of rat hippocampal slices. J. Physiol. (Lond.) 458, 261-287 (1992).
48. Sigworth, F.J. The variance of sodium current fluctuations at the node of Ranvier. J. Physiol. (Lond.) 307, 97-129 (1980).
49. Clark, B.A. & Cull-Candy, S.G. Activity-dependent recruitment of extrasynaptic NMDA receptor activation at an AMPA receptor-only synapse. J. Neurosci. 22, 4428-4436 (2002).
50. Clements, J.D. & Bekkers, J.M. Detection of spontaneous synaptic events with an optimally scaled template. Biophys. J. 73, 220-229 (1997).