Calcium permeability of ligand-gated Ca2+ channels

European Journal of Pharmacology

Volumn 739, Issue C, 2014, Pages 60-73

  Pankratov, Yuriy ^a   Lalo, Ulyana ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Ca2+ signalling; Calcium permeability; Calmodulin; CaMKII; Glia neuron interaction; GluN3 subunit; Lateral diffusion; Neurotransmitter release; Nicotinic receptor; NMDA receptor; P2X receptor; PKC; Presynaptic receptor; Synaptic plasticity; Trafficking; VILIP1

Indexed keywords

ARGININE; ASPARAGINE; BUNGAROTOXIN RECEPTOR; CALCIUM ION; CHOLINERGIC RECEPTOR; GLUTAMINE; LIGAND GATED CALCIUM ION CHANNEL; LIGAND GATED ION CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINIC RECEPTOR ALPHA4BETA2; POTASSIUM ION; PURINERGIC P2X RECEPTOR; SODIUM ION; UNCLASSIFIED DRUG; CALCIUM; CALCIUM CHANNEL;

AMINO ACID SUBSTITUTION; BINDING SITE; CALCIUM BINDING; CALCIUM TRANSPORT; CELL INTERACTION; GLIA CELL; HIPPOCAMPAL CA1 REGION; HUMAN; LEARNING; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PURKINJE CELL; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TISSUE DISTRIBUTION; UPREGULATION; ANIMAL; CHEMISTRY; METABOLISM; PERMEABILITY;

ANIMALS; CALCIUM; CALCIUM CHANNELS; HUMANS; LIGAND-GATED ION CHANNELS; PERMEABILITY;

EID: 84925032183     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2013.11.017     Document Type: Review

References (144)

1. E.X. Albuquerque, E.F. Pereira, M. Alkondon, and S.W. Rogers Mammalian nicotinic acetylcholine receptors: from structure to function Physiol. Rev. 89 2009 73 120
2. M. Alkondon, E.F. Pereira, H.M. Eisenberg, and E.X. Albuquerque Choline and selective antagonists identify two subtypes of nicotinic acetylcholine receptors that modulate GABA release from CA1 interneurons in rat hippocampal slices J. Neurosci. 19 1999 2693 2705
3. M. Alkondon, and E.X. Albuquerque The nicotinic acetylcholine receptor subtypes and their function in the hippocampus and cerebral cortex Prog. Brain Res. 145 2004 109 120
4. R.C. Allsopp, U. Lalo, and R.J. Evans Lipid raft association and cholesterol sensitivity of P2X1-4 receptors for ATP: chimeras and point mutants identify intracellular amino-terminal residues involved in lipid regulation of P2X1 receptors J. Biol. Chem. 285 2010 32770 32777
5. J. Arredondo, A.I. Chernyavsky, D.L. Jolkovsky, K.E. Pinkerton, and S.A. Grando Receptor-mediated tobacco toxicity: cooperation of the Ras/Raf-1/MEK1/ERK and JAK-2/STAT-3 pathways downstream of alpha7 nicotinic receptor in oral keratinocytes FASEB J. 20 2006 2093 2101
6. L. Bard, and L. Groc Glutamate receptor dynamics and protein interaction: lessons from the NMDA receptor Mol. Cell. Neurosci. 48 2011 298 307
7. C. Beck, L.P. Wollmuth, P.H. Seeburg, B. Sakmann, and T. Kuner NMDA receptor channel segments forming the extracellular vestibule inferred from the accessibility of substituted cysteines Neuron 22 1999 559 570
8. X. Bian, J. Ren, M. DeVries, B. Schnegelsberg, D.A. Cockayne, A.P. Ford, and J.J. Galligan Peristalsis is impaired in the small intestine of mice lacking the P2×3 subunit J. Physiol. 551 Pt 1 2003 309 322
9. W.T. Birdsong, L. Fierro, F.G. Williams, V. Spelta, L.A. Naves, M. Knowles, and E.W. McCleskey Sensing muscle ischemia: coincident detection of acid and ATP via interplay of two ion channels Neuron 68 2010 739 749
10. L.K. Bobanovic, S.J. Royle, and R.D. Murrell-Lagnado P2X receptor trafficking in neurons is subunit specific J. Neurosci. 22 2002 4814 4824
11. E. Boue-Grabot, E. Toulme, M.B. Emerit, and M. Garret Subunit-specific coupling between gamma-aminobutyric acid type A and P2X2 receptor channels J. Biol. Chem. 279 2004 52517 52525
12. L.E. Browne, L.H. Jiang, and R.A. North New structure enlivens interest in P2X receptors Trends Pharmacol. Sci. 31 2010 229 237
13. D.A. Brown, and D.I. Yule Protein kinase a regulation of P2X(4) receptors: requirement for a specific motif in the C-terminus Biochim. Biophys. Acta 1803 2010 275 287
14. D.H. Brunzell, D.S. Russell, and M.R. Picciotto In vivo nicotine treatment regulates mesocorticolimbic CREB and ERK signalling in C57Bl/6J mice J. Neurochem. 84 2003 1431 1441
15. N. Burnashev, R. Schoepfer, H. Monyer, J.P. Ruppersberg, W. Gunther.; P.H. Seeburg, and B. Sakmann Control by asparagine residues of calcium permeability and magnesium blockade in the NMDA receptor Science 257 1992 1415 1419
16. Burnashev, N.; Zhou, Z.; Neher, E.; Sakmann, B.; 1995. Fractional calcium currents through recombinant GluR channels of the NMDA, AMPA and kainate receptor subtypes. J. Physiol. 485, 403-418.
17. G. Burnstock Physiology and pathophysiology of purinergic neurotransmission Physiol. Rev. 87 2007 659 797
18. V. Burzomato, G. Frugier, I. Perez-Otano, J.T. Kittler, and D. Attwell The receptor subunits generating NMDA receptor mediated currents in oligodendrocytes J. Physiol. 588 2010 3403 3414
19. F. Canal, O. Palygin, Y. Pankratov, S.A. Correa, and J. Muller Compartmentalization of the MAPK scaffold protein KSR1 modulates synaptic plasticity in hippocampal neurons FASEB J. 25 2011 2362 2372
20. N.G. Castro, and E.X. Albuquerque alpha-Bungarotoxin-sensitive hippocampal nicotinic receptor channel has a high calcium permeability Biophys. J. 68 1995 516 524
21. G. Chen, P. Chen, H. Tan, D. Ma, F. Dou, J. Feng, and Z. Yan Regulation of the NMDA receptor-mediated synaptic response by acetylcholinesterase inhibitors and its impairment in an animal model of Alzheimer's disease Neurobiol. Aging 29 2008 1795 1804
22. K.T. Chang, and D.K. Berg Voltage-gated channels block nicotinic regulation of CREB phosphorylation and gene expression in neurons Neuron 32 2001 855 865
23. S. Chaumont, V. Compan, E. Toulme, E. Richler, G.D. Housley, F. Rassendren, and B.S. Khakh Regulation of P2X2 receptors by the neuronal calcium sensor VILIP1 Sci. Signal. 1 2008 (ra8)
24. G.L. Collingridge, J.T. Isaac, and Y.T. Wang Receptor trafficking and synaptic plasticity Nat. Rev. Neurosci. 5 2004 952 962
25. 2+ by speeding recovery of P2X receptors from desensitization J. Neurosci. 18 1998 9238 9244
26. R. Corlew, D.J. Brasier, D.E. Feldman, and B.D. Philpot Presynaptic NMDA receptors: newly appreciated roles in cortical synaptic function and plasticity Neuroscientist 14 2008 609 625
27. P.J. Corringer, S. Bertrand, J.L. Galzi, A. Devillers-Thiery, J.P. Changeux, and D. Bertrand Mutational analysis of the charge selectivity filter of the alpha7 nicotinic acetylcholine receptor Neuron 22 1999 831 843
28. M.I. Damaj The involvement of spinal Ca(2+)/calmodulin-protein kinase II in nicotine-induced antinociception in mice Eur. J. Pharmacol. 404 2000 103 110
29. E.R. Decker, and J.A. Dani Calcium permeability of the nicotinic acetylcholine receptor: the single-channel calcium influx is significant J. Neurosci. 10 1990 3413 3420
30. 2+ influx Cell Calcium 44 2008 521 532
31. I.C. Duguid Presynaptic NMDA receptors: are they dendritic receptors in disguise? Brain Res. Bull. 93 2013 4 9
32. I.C. Duguid, Y. Pankratov, G.W. Moss, and T.G. Smart Somatodendritic release of glutamate regulates synaptic inhibition in cerebellar Purkinje cells via autocrine mGluR1 activation J. Neurosci. 27 2007 12464 12474
33. F.A. Edwards, S.J. Robertson, and A.J. Gibb Properties of ATP receptor-mediated synaptic transmission in the rat medial habenula Neuropharmacology 36 1997 1253 1268
34. T.M. Egan, and B.S. Khakh Contribution of calcium ions to P2X channel responses J. Neurosci. 24 2004 3413 3420
35. J. Egebjerg, and S.F. Heinemann Ca2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6 Proc. Natl. Acad. Sci. USA 90 1993 755 759
36. R.J. Evans, V. Derkach, and A. Surprenant ATP mediates fast synaptic transmission in mammalian neurons Nature 357 1992 503 505
37. R.J. Evans, C. Lewis, C. Virginio, K. Lundstrom, G. Buell, A. Surprenant, and R.A. North Ionic permeability of, and divalent cation effects on, two ATP-gated cation channels (P2X receptors) expressed in mammalian cells J. Physiol. 497 1996 413 422
38. C.P. Fenster, M.L. Beckman, J.C. Parker, E.B. Sheffield, T.L. Whitworth, M.W. Quick, and R.A. Lester Regulation of α4β2 nicotinic receptor desensitization by calcium and protein kinase C Mol. Pharmacol. 55 1999 432 443
39. 2+ permeable Proc. Natl. Acad. Sci. USA 97 2000 3643 3648
40. S. Fucile, M. Renzi, P. Lax, and F. Eusebi Fractional Ca(2+) current through human neuronal alpha7 nicotinic acetylcholine receptors Cell Calcium 34 2003 205 209
41. L.C. Gahring, K. Persiyanov, and S.W. Rogers Mouse strain-specific changes in nicotinic receptor expression with age Neurobiol. Aging 26 2005 973 980
42. 2+ currents through somatic and dendritic glutamate receptor channels of rat hippocampal CA1 pyramidal neurones J. Physiol. 491 1996 757 772
43. R. Giniatullin, A. Nistri, and E. Fabbretti Molecular mechanisms of sensitization of pain-transducing P2X3 receptors by the migraine mediators CGRP and NGF Mol. Neurobiol. 37 2008 83 90
44. R. Girod, G. Crabtree, G. Ernstrom, J. Ramirez-Latorre, D. McGehee, J. Turner, and L. Role Heteromeric complexes of alpha 5 and/or alpha 7 subunits: effects of calcium and potential role in nicotine-induced presynaptic facilitation Ann. N. Y. Acad. Sci. 868 1999 578 590
45. G.R. Gordon, K.J. Iremonger, S. Kantevari, G.C. Ellis-Davies, B.A. MacVicar, and J.S. Bains Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses Neuron 64 2009 391 403
46. R. Gray, A.S. Rajan, K.A. Radcliffe, M. Yakehiro, and J.A. Dani Hippocampal synaptic transmission enhanced by low concentrations of nicotine Nature 383 1996 713 716
47. W.R. Haines, G.E. Torres, M.M. Voigt, and T.M. Egan Properties of the novel ATP-gated ionotropic receptor composed of the P2X(1) and P2X(5) isoforms Mol. Pharmacol. 56 1999 720 727
48. S.C. Harney, D.E. Jane, and R. Anwyl Extrasynaptic NR2D-containing NMDARs are recruited to the synapse during LTP of NMDAR-EPSCs J. Neurosci. 28 2008 11685 11694
49. Hattori, M.; Gouaux, E.; 2012. Molecular mechanism of ATP binding and ion channel activation in P2X receptors. Nature 485, 207-212.
50. B. Hechler, N. Lenain, P. Marchese, C. Vial, V. Heim, M. Freund, J.P. Cazenave, M. Cattaneo, Z.M. Ruggeri, R. Evans, and C. Gachet A role of the fast ATP-gated P2X1 cation channel in thrombosis of small arteries in vivo J. Exp. Med. 198 2003 661 667
51. D.L. Hunt, and P.E. Castillo Synaptic plasticity of NMDA receptors: mechanisms and functional implications Curr. Opin. Neurobiol. 22 2012 496 508
52. D.L. Hunt, N. Puente, P. Grandes, and P.E. Castillo Bidirectional NMDA receptor plasticity controls CA3 output and heterosynaptic metaplasticity Nat. Neurosci. 16 2013 1049 1059
53. P. Illes, A. Verkhratsky, G. Burnstock, and H. Franke P2X receptors and their roles in astroglia in the central and peripheral nervous system Neuroscientist 18 2012 422 438
54. 2+-permeable AMPA-type glutamate receptor channels in rat neocortical neurons J. Neurophysiol. 78 1997 2592 2601
55. T.C. Jacob, S.J. Moss, and R. Jurd GABA(A) receptor trafficking and its role in the dynamic modulation of neuronal inhibition Nat. Rev. Neurosci. 9 2008 331 343
56. P. Jourdain, L.H. Bergersen, K. Bhaukaurally, P. Bezzi, M. Santello, M. Domercq, C. Matute, F. Tonello, V. Gundersen, and A. Volterra Glutamate exocytosis from astrocytes controls synaptic strength Nat. Neurosci. 10 2007 331 339
57. J.N. Jovanovic, P. Thomas, J.T. Kittler, T.G. Smart, and S.J. Moss Brain-derived neurotrophic factor modulates fast synaptic inhibition by regulating GABA(A) receptor phosphorylation, activity, and cell-surface stability J. Neurosci. 24 2004 522 530
58. T. Kawate, J.C. Michel, W.T. Birdsong, and E. Gouaux Crystal structure of the ATP-gated P2X(4) ion channel in the closed state Nature 460 2009 592 598
59. B.S. Khakh, X.R. Bao, C. Labarca, and H.A. Lester Neuronal P2X transmitter-gated cation channels change their ion selectivity in seconds Nat. Neurosci. 2 1999 322 330
60. B.S. Khakh, X. Zhou, J. Sydes, J.J. Galligan, and H.A. Lester State-dependent cross-inhibition between transmitter-gated cation channels Nature 406 2000 405 410
61. B.S. Khakh, D. Gittermann, D.A. Cockayne, and A. Jones ATP modulation of excitatory synapses onto interneurons J. Neurosci. 23 2003 7426 7437
62. B.S. Khakh, and R.A. North Neuromodulation by extracellular ATP and P2X receptors in the CNS Neuron 76 2012 51 69
63. 2+ regulation of nicotinic acetylcholine receptor channels in rat hippocampal CA1 neurons J. Neurosci. 23 2003 9024 9031
64. R.C. Klein, and J.L. Yakel Paired-pulse potentiation of alpha7-containing nAChRs in rat hippocampal CA1 stratum radiatum interneurones J. Physiol. 568 2005 881 889
65. J.J. Krupp, B. Vissel, S.F. Heinemann, and G.L. Westbrook N-terminal domains in the NR2 subunit control desensitization of NMDA receptors Neuron 20 1998 317 327
66. H.B. Kwon, and P.E. Castillo Long-term potentiation selectively expressed by NMDA receptors at hippocampal mossy fiber synapses Neuron 57 2008 108 120
67. U. Lalo, Y. Pankratov, F. Kirchhoff, R.A. North, and A. Verkhratsky NMDA receptors mediate neuron-to-glia signaling in mouse cortical astrocytes J. Neurosci. 26 2006 2673 2683
68. U. Lalo, Y. Pankratov, S.P. Wichert, M.J. Rossner, R.A. North, F. Kirchhoff, and A. Verkhratsky P2×1 and P2×5 subunits form the functional P2X receptor in mouse cortical astrocytes J. Neurosci. 28 2008 5473 5480
69. 2+-dependent modulation of GABAA and NMDA receptors by extracellular ATP: implication for function of tripartite synapse Biochem. Soc. Trans. 37 2009 1407 1411
70. U. Lalo, R.C. Allsopp, M.P. Mahaut-Smith, and R.J. Evans P2X1 receptor mobility and trafficking; regulation by receptor insertion and activation J. Neurochem. 113 2010 1177 1187
71. U. Lalo, A. Verkhratsky, and Y. Pankratov Ionotropic ATP receptors in neuronal-glial communication Semin. Cell. Dev. Biol. 22 2011 220 228
72. U. Lalo, O. Palygin, R.A. North, A. Verkhratsky, and Y. Pankratov Age-dependent remodelling of ionotropic signalling in cortical astroglia Aging Cell 10 2011 392 402
73. U. Lalo, J.A. Roberts, and R.J. Evans Identification of human P2X1 receptor-interacting proteins reveals a role of the cytoskeleton in receptor regulation J. Biol. Chem. 286 2011 30591 30599
74. U. Lalo, S. Jones, J.A. Roberts, M.P. Mahaut-Smith, and R.J. Evans Heat shock protein 90 inhibitors reduce trafficking of ATP-gated P2X1 receptors and human platelet responsiveness J. Biol. Chem. 287 2012 32747 32754
75. Lewis, C.; Neidhart, S.; Holy, C.; North, R.A.; Buell, G.; Surprenant, A.; 1995. Coexpression of P2X2 and P2X3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 377, 432-435.
76. G.H. Li, E.M. Lee, D. Blair, C. Holding, P. Poronnik, D.I. Cook, J.A. Barden, and M.R. Bennett The distribution of P2X receptor clusters on individual neurons in sympathetic ganglia and their redistribution on agonist activation J. Biol. Chem. 275 2000 29107 29112
77. R.C. Malenka, and M.F. Bear LTP and LTD: an embarrassment of riches Neuron 44 2004 5 21
78. H.D. Mansvelder, and D.S. McGehee Cellular and synaptic mechanisms of nicotine addiction J. Neurobiol. 53 2002 606 617
79. M. Marchi, F. Risso, C. Viola, P. Cavazzani, and M. Raiteri Direct evidence that release-stimulating alpha7 nicotinic cholinergic receptors are localized on human and rat brain glutamatergic axon terminals J. Neurochem. 80 2002 1071 1078
80. K. Matsuda, M. Fletcher, Y. Kamiya, and M. Yuzaki Specific assembly with the NMDA receptor 3B subunit controls surface expression and calcium permeability of NMDA receptors J. Neurosci. 23 2003 10064 10073
81. I. Micu, Q. Jiang, E. Coderre, A. Ridsdale, L. Zhang, J. Woulfe, X. Yin, B.D. Trapp, J.E. McRory, R. Rehak, G.W. Zamponi, W. Wang, and P.K. Stys NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia Nature 439 2006 988 992
82. M. Migaud, P. Charlesworth, M. Dempster, L.C. Webster, A.M. Watabe, M. Makhinson, Y. He, M.F. Ramsay, R.G. Morris, J.H. Morrison, T.J. O'Dell, and S.G. Grant Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein Nature 396 1998 433 439
83. K. Migita, W.R. Haines, M.M. Voigt, and T.M. Egan Polar residues of the second transmembrane domain influence cation permeability of the ATP-gated P2X(2) receptor J. Biol. Chem. 276 2001 30934 30941
84. N.S. Millar, and P.C. Harkness Assembly and trafficking of nicotinic acetylcholine receptors Mol. Membr. Biol. 25 2008 279 292
85. R. Min, and T. Nevian Astrocyte signaling controls spike timing-dependent depression at neocortical synapses Nat. Neurosci. 15 2012 746 753
86. H. Mori, H. Masaki, T. Yamakura, and M. Mishina Identification by mutagenesis of a Mg(2+)-block site of the NMDA receptor channel Nature 358 1992 673 675
87. C. Mulle, D. Choquet, H. Korn, and J.P. Changeux Calcium influx through nicotinic receptor in rat central neurons: its relevance to cellular regulation Neuron 8 1992 135 143
88. K. Mulryan, D.P. Gitterman, C.J. Lewis, C. Vial, B.J. Leckie, A.L. Cobb, J.E. Brown, E.C. Conley, G. Buell, C.A. Pritchard, and R.J. Evans Reduced vas deferens contraction and male infertility in mice lacking P2X1 receptors Nature 403 2000 86 89
89. K. Nakazawa ATP-activated current and its interaction with acetylcholine-activated current in rat sympathetic neurons J. Neurosci 14 1994 740 750
90. R.A. North Molecular physiology of P2X receptors Physiol. Rev. 82 2002 1013 1067
91. S. Pachernegg, N. Strutz-Seebohm, and M. Hollmann GluN3 subunit-containing NMDA receptors: not just one-trick ponies Trends Neurosci. 35 2012 240 249
92. O. Palygin, U. Lalo, and Y. Pankratov Distinct pharmacological and functional properties of NMDA receptors in mouse cortical astrocytes Br. J. Pharmacol. 163 2011 1755 1766
93. 2+ signalling in cortical astrocytes Cell Calcium 48 2010 225 231
94. Y. Pankratov, U. Lalo, O. Krishtal, and A. Verkhratsky Ionotropic P2X purinoreceptors mediate synaptic transmission in rat pyramidal neurones of layer II/III of somato-sensory cortex J. Physiol. 542 2002 529 536
95. Y.V. Pankratov, U.V. Lalo, and O.A. Krishtal b Role for P2X receptors in long-term potentiation J. Neurosci. 22 2002 8363 8369
96. Y. Pankratov, U. Lalo, A. Verkhratsky, and R.A. North Vesicular release of ATP at central synapses Pflugers Arch. 452 2006 589 597
97. Y. Pankratov, U. Lalo, A. Verkhratsky, and R.A. North Quantal release of ATP in mouse cortex J. Gen. Physiol. 129 2007 257 265
98. Pankratov, Y.; Lalo, U.; Krishtal, O.A.; Verkhratsky, A.; 2009. P2X receptors and synaptic plasticity. Neuroscience 158, 137-148.
99. P. Paoletti, C. Bellone, and Q. Zhou NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease Nat. Rev. Neurosci. 14 2013 383 400
100. I. Perez-Otano, R. Lujan, S.J. Tavalin, M. Plomann, J. Modregger, X.B. Liu, E.G. Jones, S.F. Heinemann, D.C. Lo, and M.D. Ehlers Endocytosis and synaptic removal of NR3A-containing NMDA receptors by PACSIN1/syndapin1 Nat. Neurosci. 9 2006 611 621
101. R.S. Petralia, R.A. Al-Hallaq, and R.J. Wenthold Trafficking and Targeting of NMDA Receptors A.M. Van Dongen, Biology of the NMDA Receptor 2009 Boca Raton FL
102. V.I. Pidoplichko, M. DeBiasi, J.T. Williams, and J.A. Dani Nicotine activates and desensitizes midbrain dopamine neurons Nature 390 1997 401 404
103. A.J. Pocklington, M. Cumiskey, J.D. Armstrong, and S.G. Grant The proteomes of neurotransmitter receptor complexes form modular networks with distributed functionality underlying plasticity and behaviour Mol. Syst. Biol. 2 2006 2006 2023
104. L.S. Premkumar, and A. Auerbach Identification of a high affinity divalent cation binding site near the entrance of the NMDA receptor channel Neuron 16 1996 869 880
105. N. Rebola, R. Lujan, R.A. Cunha, and C. Mulle Adenosine A2A receptors are essential for long-term potentiation of NMDA-EPSCs at hippocampal mossy fiber synapses Neuron 57 2008 121 134
106. J.S. Rhee, Z.M. Wang, J. Nabekura, K. Inoue, and N. Akaike ATP facilitates spontaneous glycinergic IPSC frequency at dissociated rat dorsal horn interneuron synapses J. Physiol. 524 Pt 2 2000 471 483
107. A.C. Roberts, J. Diez-Garcia, R.M. Rodriguiz, I.P. Lopez, R. Lujan, R. Martinez-Turrillas, E. Pico, M.A. Henson, D.R. Bernardo, T.M. Jarrett, D.J. Clendeninn, L. Lopez-Mascaraque, G. Feng, D.C. Lo, J.F. Wesseling, W.C. Wetsel, B.D. Philpot, and I. Perez-Otano Downregulation of NR3A-containing NMDARs is required for synapse maturation and memory consolidation Neuron 63 2009 342 356
108. S. Roger, P. Pelegrin, and A. Surprenant Facilitation of P2X7 receptor currents and membrane blebbing via constitutive and dynamic calmodulin binding J. Neurosci. 28 2008 6393 6401
109. 2+ influx on functional responses in human platelets Thromb. Haemost. 88 2002 495 502
110. M.E. Rubio, and F. Soto Distinct localization of P2X receptors at excitatory postsynaptic specializations J. Neurosci. 21 2001 641 653
111. B.K. Rycroft, and A.J. Gibb Inhibitory interactions of calcineurin (phosphatase 2B) and calmodulin on rat hippocampal NMDA receptors Neuropharmacology 47 2004 505 514
112. M.G. Salter, and R. Fern NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury Nature 438 2005 1167 1171
113. D.S. Samways, and T.M. Egan Acidic amino acids impart enhanced Ca2+ permeability and flux in two members of the ATP-gated P2X receptor family J. Gen. Physiol. 129 2007 245 256
114. D.S. Samways, B.S. Khakh, S. Dutertre, and T.M. Egan Preferential use of unobstructed lateral portals as the access route to the pore of human ATP-gated ion channels (P2X receptors) Proc. Natl. Acad. Sci. USA 108 2011 13800 13805
115. 2+ flux in ligand-gated cation channel (P2X4) by actions on lateral portals J. Biol. Chem. 287 2012 7594 7602
116. Y.F. Sasaki, T. Rothe, L.S. Premkumar, S. Das, J. Cui, M.V. Talantova, H.K. Wong, X. Gong, S.F. Chan, D. Zhang, N. Nakanishi, N.J. Sucher, and S.A. Lipton Characterization and comparison of the NR3A subunit of the NMDA receptor in recombinant systems and primary cortical neurons J. Neurophysiol. 87 2002 2052 2063
117. T.J. Searl, R.S. Redman, and E.M. Silinsky Mutual occlusion of P2X ATP receptors and nicotinic receptors on sympathetic neurons of the guinea-pig J. Physiol. 510 1998 783 791
118. G. Sharma, and C.F. Stevens Interactions between two divalent ion binding sites in N-methyl-d-aspartate receptor channels Proc. Natl. Acad. Sci. USA 93 1996 14170 14175
119. G. Sharma, and S. Vijayaraghavan Nicotinic cholinergic signaling in hippocampal astrocytes involves calcium-induced calcium release from intracellular stores Proc. Natl. Acad. Sci. USA 98 2001 4148 4153
120. J.D. Shepherd, and R.L. Huganir The cell biology of synaptic plasticity: AMPA receptor trafficking Annu. Rev. Cell Dev. Biol. 23 2007 613 643
121. 2+ entry through presynaptic P2X receptors elicits postsynaptic firing in the brainstem autonomic network J. Neurosci. 24 2004 3125 3135
122. B. Siegler Retchless, W. Gao, and J.W. Johnson A single GluN2 subunit residue controls NMDA receptor channel properties via intersubunit interaction Nat. Neurosci. 15 406-413 2012 S401 S402
123. J.A. Sim, S. Chaumont, J. Jo, L. Ulmann, M.T. Young, K. Cho, G. Buell, R.A. North, and F. Rassendren Altered hippocampal synaptic potentiation in P2X4 knock-out mice J. Neurosci. 26 2006 9006 9009
124. 2+ current. Neuron 53, 17-24.
125. A.I. Sobolevsky, M.P. Rosconi, and E. Gouaux X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor Nature 462 2009 745 756
126. F. Soto, M. Garcia-Guzman, J.M. Gomez-Hernandez, M. Hollmann, C. Karschin, and W. Stuhmer P2X4: an ATP-activated ionotropic receptor cloned from rat brain Proc. Natl. Acad. Sci. USA 93 1996 3684 3688
127. N. Spruston, P. Jonas, and B. Sakmann Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons J. Physiol. 482 1995 325 352
128. D. Stanchev, M. Blosa, D. Milius, Z. Gerevich, P. Rubini, G. Schmalzing, K. Eschrich, M. Schaefer, K. Wirkner, and P. Illes Cross-inhibition between native and recombinant TRPV1 and P2X(3) receptors Pain 143 2009 26 36
129. P. Stern, M. Cik, D. Colquhoun, and F.A. Stephenson Single channel properties of cloned NMDA receptors in a human cell line: comparison with results from Xenopus oocytes J. Physiol. 476 1994 391 397
130. T. Suzuki, I. Hide, A. Matsubara, C. Hama, K. Harada, K. Miyano, M. Andra, H. Matsubayashi, N. Sakai, S. Kohsaka, K. Inoue, and Y. Nakata Microglial alpha7 nicotinic acetylcholine receptors drive a phospholipase C/IP3 pathway and modulate the cell activation toward a neuroprotective role J. Neurosci. Res. 83 2006 1461 1470
131. G.T. Swanson, D. Feldmeyer, M. Kaneda, and S.G. Cull-Candy Effect of RNA editing and subunit co-assembly single-channel properties of recombinant kainate receptors J. Physiol. 492 1996 129 142
132. G.T. Swanson, S.K. Kamboj, and S.G. Cull-Candy Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition J. Neurosci. 17 1997 58 69
133. N. Unwin Refined structure of the nicotinic acetylcholine receptor at 4A resolution J. Mol. Biol. 346 2005 967 989
134. F. Vacca, M. Giustizieri, M.T. Ciotti, N.B. Mercuri, and C. Volonte Rapid constitutive and ligand-activated endocytic trafficking of P2X receptor J. Neurochem. 109 2009 1031 1041
135. Valera, S.; Hussy, N.; Evans, R.J.; Adami, N.; North, R.A.; Surprenant, A.; Buell, G.; 1994. A new class of ligand-gated ion channel defined by P2x receptor for extracellular ATP. Nature 371, 516-519.
136. C. Virginio, D. Church, R.A. North, and A. Surprenant Effects of divalent cations, protons and calmidazolium at the rat P2X7 receptor Neuropharmacology 36 1997 1285 1294
137. C. Virginio, R.A. North, and A. Surprenant Calcium permeability and block at homomeric and heteromeric P2X2 and P2X3 receptors, and P2X receptors in rat nodose neurones J. Physiol. 510 1998 27 35
138. C.L. Walters, J.N. Cleck, Y.C. Kuo, and J.A. Blendy Mu-opioid receptor and CREB activation are required for nicotine reward Neuron 46 2005 933 943
139. 2+ flux rates in NMDA receptor channels J. Neurosci. 22 2002 10209 10216
140. 2+-permeable AMPA glutamate receptor channels J. Gen. Physiol. 112 1998 623 636
141. J.R. Wooltorton, V.I. Pidoplichko, R.S. Broide, and J.A. Dani Differential desensitization and distribution of nicotinic acetylcholine receptor subtypes in midbrain dopamine areas J. Neurosci. 23 2003 3176 3185
142. 2+/calmodulin-dependent protein kinase II potentiates ATP responses by promoting trafficking of P2X receptors Proc. Natl. Acad. Sci. USA 101 2004 11868 11873
143. K. Yamamoto, T. Sokabe, T. Matsumoto, K. Yoshimura, M. Shibata, N. Ohura, T. Fukuda, T. Sato, K. Sekine, S. Kato, M. Isshiki, T. Fujita, M. Kobayashi, K. Kawamura, H. Masuda, A. Kamiya, and J. Ando Impaired flow-dependent control of vascular tone and remodeling in P2X4-deficient mice Nat. Med. 12 2006 133 137
144. 2+ sensor VILIP-1 leads to the upregulation of functional alpha4beta2 nicotinic acetylcholine receptors in hippocampal neurons Mol. Cell Neurosci. 40 2009 280 292