Probing TARP modulation of AMPA receptor conductance with polyamine toxins

Journal of Neuroscience

Volumn 31, Issue 20, 2011, Pages 7511-7520

  Jackson, Alexander C ^a   Milstein, Aaron D ^a,b,d   Soto, David ^c,e   Farrant, Mark ^c   Cull Candy, Stuart G ^c   Nicoll, Roger A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMIC ACID; KAINIC ACID; PHILANTHOTOXIN; PHILANTHOTOXIN 74; POLYAMINE TOXIN; PROTEIN GLUA2; RECOMBINANT GLUA2; RECOMBINANT PROTEIN; TOXIN; TRANSMEMBRANE AMPAR REGULATORY PROTEIN; TRANSMEMBRANE AMPAR REGULATORY PROTEIN GAMMA 2; TRANSMEMBRANE AMPAR REGULATORY PROTEIN GAMMA 3; TRANSMEMBRANE AMPAR REGULATORY PROTEIN GAMMA 4; TRANSMEMBRANE AMPAR REGULATORY PROTEIN GAMMA 8; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DESENSITIZATION; DRUG ACTIVITY; DRUG EFFICACY; DRUG PROTEIN BINDING; EMBRYO; HUMAN; HUMAN CELL; HUMAN TISSUE; MOLECULAR PROBE; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; SYNAPTIC POTENTIAL;

ANIMALS; CELLS, CULTURED; FEMALE; HEK293 CELLS; HUMANS; MALE; MEMBRANE PROTEINS; MICE; MICE, MUTANT STRAINS; PHENOLS; POLYAMINES; RECEPTORS, AMPA; XENOPUS LAEVIS;

EID: 79955086359     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6688-10.2011     Document Type: Article

References (77)

1. Andersen TF, Tikhonov DB, Bolcho U, Bolshakov K, Nelson JK, Pluteanu F, Mellor IR, Egebjerg J, Stromgaard K (2006) Uncompetitive antagonism of AMPA receptors: mechanistic insights from studies of polyamine toxin derivatives. J Med Chem 49:5414-5423.
2. Ascher P, Nowak L (1988) Quisqualate-and kainate-activated channels in mouse central neurones in culture. J Physiol 399:227-245.
3. Ayalon G, Stern-Bach Y (2001) Functional assembly of AMPA and kainate receptors is mediated by several discrete protein-protein interactions. Neuron 31:103-113.
4. Bähring R, Mayer ML (1998) An analysis of philanthotoxin block for recombinant rat GluR6(Q) glutamate receptor channels. J Physiol 509:635-650.
5. Bähring R, Bowie D, Benveniste M, Mayer ML (1997) Permeation and block of rat GluR6 glutamate receptor channels by internal and external polyamines. J Physiol 502:575-589.
6. Benke TA, Luthi A, Isaac JT, Collingridge GL (1998) Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393:793-797.
7. Blaschke M, Keller BU, Rivosecchi R, Hollmann M, Heinemann S, Konnerth A (1993) A single amino acid determines the subunit-specific spider toxin block of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate/ kainate receptor channels. Proc Natl Acad Sci U S A 90:6528-6532.
8. Bowie D, Mayer ML (1995) Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 15:453-462.
9. Bowie D, Lange GD, Mayer ML (1998) Activity-dependent modulation of glutamate receptors by polyamines. J Neurosci 18:8175-8185.
10. Brackley PT, Bell DR, Choi SK, Nakanishi K, Usherwood PN (1993) Selective antagonism of native and cloned kainate and NMDA receptors by polyamine-containing toxins. J Pharmacol Exp Ther 266:1573-1580.
11. Bredt DS, Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40:361-379.
12. Burgess DL, Gefrides LA, Poreman PJ, Noebels JL (2001) A cluster of three novel Ca2+channel γ subunit genes on chromosome 19q13.4: evolution and expression profile of the γ subunit gene family. Genomics 71:339-350.
13. Burnashev N, Schoepfer R, Monyer H, Ruppersberg JP, Gunther W, Seeburg PH, Sakmann B (1992) Control by asparagine residues of calcium permeability and magnesium blockade in the NMDA receptor. Science 257:1415-1419.
14. Chen L, Chetkovich DM, Petralia RS, Sweeney NT, Kawasaki Y, Wenthold RJ, Bredt DS, Nicoll RA (2000) Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408:936-943.
15. Cho CH, St-Gelais F, Zhang W, Tomita S, Howe JR (2007) Two families of TARP isoforms that have distinct effects on the kinetic properties of AMPA receptors and synaptic currents. Neuron 55:890-904.
16. Coombs ID, Cull-Candy SG (2009) Transmembrane AMPA receptor regulatory proteins and AMPA receptor function in the cerebellum. Neuroscience 162:656-665.
17. Cull-Candy SG, Usowicz MM (1987) Multiple-conductance channels activated by excitatory amino acids in cerebellar neurons. Nature 325:525-528.
18. Cull-Candy S, Kelly L, Farrant M (2006) Regulation of Ca2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr Opin Neurobiol 16:288-297.
19. Derkach V, Barria A, Soderling TR (1999) Ca2+/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc Natl Acad Sci U S A 96:3269-3274.
20. Fucile S, Miledi R, Eusebi F (2006) Effects of cyclothiazide on GluR1/AMPA receptors. Proc Natl Acad Sci U S A 103:2943-2947.
21. Gebhardt C, Cull-Candy SG (2006) Influence of agonist concentration on AMPA and kainate channels in CA1 pyramidal cells in rat hippocampal slices. J Physiol 573:371-394.
22. Greger IH, Ziff EB, Penn AC (2007) Molecular determinants of AMPA receptor subunit assembly. Trends Neurosci 30:407-416.
23. Herlitze S, Raditsch M, Ruppersberg JP, Jahn W, Monyer H, Schoepfer R, Witzemann V (1993) Argiotoxin detects molecular differences in AMPA receptor channels. Neuron 10:1131-1140.
24. Hollmann M, Hartley M, Heinemann S (1991) Ca2+ permeability of KAAMPA-gated glutamate receptor channels depends on subunit composition. Science 252:851-853.
25. Isaac JT, Ashby M, McBain CJ (2007) The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54:859-871.
26. Jackson AC, Nicoll RA (2011a) Stargazin (TARP gamma-2) is required for compartment-specific AMPA receptor trafficking and synaptic plasticity in cerebellar stellate cells. J Neurosci 31:3939-3952.
27. Jackson AC, Nicoll RA (2011b) The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits. Neuron 70:178-199.
28. Jahr CE, Stevens CF (1987) Glutamate activates multiple single channel conductances in hippocampal neurons. Nature 325:522-525.
29. Jin R, Banke TG, Mayer ML, Traynelis SF, Gouaux E (2003) Structural basis for partial agonist action at ionotropic glutamate receptors. Nat Neurosci 6:803-810.
30. Jonas P, Major G, Sakmann B (1993) Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cell of rat hippocampus. J Physiol 472:615-663.
31. Kamboj SK, Swanson GT, Cull-Candy SG (1995) Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J Physiol 486:297-303.
32. Kato AS, Zhou W, Milstein AD, Knierman MD, Siuda ER, Dotzlaf JE, Yu H, Hale JE, Nisenbaum ES, Nicoll RA, Bredt DS (2007) New transmembrane AMPA receptor regulatory protein isoform, gamma-7, differentially regulates AMPA receptors. J Neurosci 27:4969-4977.
33. Kato AS, Siuda ER, Nisenbaum ES, Bredt DS (2008) AMPA receptor subunit-specific regulation by a distinct family of type II TARPs. Neuron 59:986-996.
34. Kim KS, Yan D, Tomita S (2010) Assembly and stoichiometry of the AMPA receptor and transmembrane AMPA receptor regulatory protein complex. J Neurosci 30:1064-1072.
35. Klugbauer N, Dai S, Specht V, Lacinová L, Marais E, Bohn G, Hofmann F (2000) A family of gamma-like calcium channel subunits. FEBS Lett 470:189-197.
36. Koh DS, Burnashev N, Jonas P (1995) Block of native Ca(2+)-permeable AMP Areceptors in rat brain by intracellular polyamines generates double rectification. J Physiol 486:305-312.
37. Kott C, Sager C, Tapken D, Werner M, Hollmann M (2009) Comparative analysis of the pharmacology of GluR1 in complex with transmembrane AMPA receptor regulatory proteins γ2, γ3, γ4 and γ8. Neuroscience 158:77-88.
38. Kromann H, Krikstolaityte S, Andersen AJ, Andersen K, Krogsgaard-Larsen P, Jaroszewski JW, Egebjerg J, Strømgaard K (2002) Solid-phase synthesis of polyamine toxin analogues: potent and selective antagonists of Ca2+-permeable AMPA receptors. J Med Chem 45:5745-5754.
39. Lu W, Shi Y, Jackson AC, Bjorgan K, During MJ, Sprengel R, Seeburg PH, Nicoll RA (2009) Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62:254-268.
40. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
41. Menuz K, Stroud RM, Nicoll RA, Hays FA (2007) TARP auxiliary subunits switch AMPA receptor antagonists into partial agonists. Science 318:815-817.
42. Milstein AD, Nicoll RA (2008) Regulation of AMPA receptor gating and pharmacology by TARP auxiliary subunits. Trends Pharmacol Sci 29:333-339.
43. Milstein AD, Nicoll RA (2009) TARP modulation of synaptic AMPA receptor trafficking and gating depends on multiple intracellular domains. Proc Natl Acad Sci U S A 27:11348-11351.
44. Milstein AD, Zhou W, Karimzadegan S, Bredt DS, Nicoll RA (2007) TARP subtypes differentially and dose-dependently control synaptic AMPA receptor gating. Neuron 55:905-918.
45. Mosbacher J, Schoepfer R, Monyer H, Burnashev N, Seeburg PH, Ruppersberg JP (1994) A molecular determinant for submillisecond desensitization in glutamate receptors. Science 266:1059-1062.
46. Nicoll RA, Tomita S, Bredt DS (2006) Auxiliary subunits assist AMPA-type glutamate receptors. Science 311:1253-1256.
47. Nilsen A, England PM (2007) A subtype-selective, use-dependent inhibitor of native AMPA receptors. J Am Chem Soc 129:4902-4903.
48. Panchenko VA, Glasser CR, Partin KM, Mayer ML (1999) Amino acid substitutions in the pore of rat glutamate receptors at sites influencing block by polyamines. J Physiol 520:337-357.
49. Partin KM, Bowie D, Mayer ML (1995) Structural determinants of allosteric regulation in alternatively spliced AMPA receptors. Neuron 14:833-843.
50. Priel A, Selak S, Lerma J, Stern-Bach Y (2006) Block of kainate receptor desensitization uncovers a key trafficking checkpoint. Neuron 52:1037-1046.
51. Prieto ML, Wollmuth LP (2010) Gating modes in AMPA receptors. J Neurosci 30:4449-4459.
52. Robinson HP, Sahara Y, Kawai N (1991) Nonstationary fluctuation analysis and direct resolution of single channel currents at postsynaptic sites. Biophysical J 59:295-304.
53. Rosenmund C, Stern-Bach Y, Stevens SF (1998) The tetrameric structure of a glutamate receptor channel. Science 280:1596-1599.
54. Sager C, Tapken D, Kott S, Hollmann M (2009) Functional modulation of AMPA receptors by transmembrane AMPA receptor regulatory proteins. Neuroscience 158:45-54.
55. Shi Y, Lu W, Milstein AD, Nicoll RA (2009) The stoichiometry of AMPA receptors and TARPs varies by neuronal cell type. Neuron 62:633-640.
56. Sigworth FJ (1980) The variance of sodium current fluctuations at the node of Ranvier. J Physiol 307:97-129.
57. Smith TC, Howe JR (2000) Concentration-dependent substate behavior of native AMPA receptors. Nat Neurosci 3:992-997.
58. Sobolevsky AI, Rosconi MP, Gouaux E (2009) X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462: 745-756.
59. Sommer B, Kohler M, Sprengel R, Seeburg PH (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67:11-19.
60. Soto D, Coombs ID, Kelly L, Farrant M, Cull-Candy SG (2007) Stargazin attenuates intracellular polyamine block of calcium-permeable AMPA receptors. Nat Neurosci 10:1260-1267.
61. Soto D, Coombs ID, Renzi M, Zonouzi M, Farrant M, Cull-Candy SG (2009) Selective regulation of long-form calcium-permeable AMPA receptors by an atypical TARP, gamma-5. Nat Neurosci 12:277-285.
62. Strømgaard K, Mellor I (2004) AMPA receptor ligands: synthetic and pharmacological studies of polyamines and polyamine toxins. Med Res Rev 24:589-620.
63. Strømgaard K, Jensen LS, Vogensen SB (2005) Polyamine toxins: development of selective ligands for ionotropic receptors. Toxicon 45:249-254.
64. Suzuki E, Kessler M, Arai AC (2008) The fast kinetics of AMPA GluR3 receptors is selectively modulated by the TARPs gamma 4 and gamma 8. Mol Cell Neurosci 38:117-123.
65. Swanson GT, Kamboj SK, Cull-Candy SG (1997) Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J Neurosci 17:58-69.
66. Tikhonov DB (2007) Ion channels of glutamate receptors: structural modeling. Mol Membr Biol 24:135-147.
67. Tomita S, Chen L, Kawasaki Y, Petralia RS, Wenthold RJ, Nicoll RA, Bredt DS (2003) Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J Cell Biol 161:805-816.
68. Tomita S, Adesnik H, Sekiguchi M, Zhang W, Wada K, Howe JR, Nicoll RA, Bredt DS (2005) Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 435:1052-1058.
69. Toth K, McBain CJ (1998) Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons. Nat Neurosci 1:572-578.
70. Traynelis SF, Silver RA, Cull-Candy SG (1993) Estimated conductance of glutamate receptor channels activated during EPSCs at the cerebellar mossy fiber-granule cell synapse. Neuron 11:279-289.
71. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, Dingledine R, Sibley D (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62:405-496.
72. Turetsky D, Garringer E, Patneau DK (2005) Stargazin modulates native AMPAreceptor functional properties by two distinct mechanisms. J Neurosci 25:7438-7448.
73. Washburn MS, Dingledine R (1996) Block of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors by polyamines and polyamine toxins. J Pharmacol Exp Ther 278:669-678.
74. Washburn MS, Numberger M, Zhang S, Dingledine R (1997) Differential dependence on GluR2 expression of three characteristic features of AMPA receptors. J Neurosci 17:9393-9406.
75. Zhang W, Robert A, Vogensen SB, Howe JR (2006) The relationship between agonist potency and AMPA receptor kinetics. Biophys J 91:1336-1346.
76. Zhang W, Cho Y, Lolis E, Howe JR (2008) Structural and single-channel results indicate that the rates of ligand binding domain closing and opening directly impact AMPA receptor gating. J Neurosci 28:932-943.
77. Ziff EB (2007) TARPs and the AMPA receptor trafficking paradox. Neuron 53:627-633.