Advertisement

Kainate Receptor Modulation by Sodium and Chloride

  • Andrew J. R. PlestedEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 717)

Abstract

The kainate-type glutamate receptor displays strong modulation by monovalent anions and cations. This modulation is independent of permeation of the ion channel. Instead, structural, computational and biophysical evidence shows that receptor activity is controlled by binding of sodium and chloride ions at sites that stabilize active dimers of glutamate binding domains. Modulation by monovalent ions is a surprisingly general property across ion channel families. However, evidence of a physiological role for ion-dependent effects on glutamate receptors is lacking, perhaps reflecting the adventitious use of ions as structural components of the kainate receptor.

“ergo, Hercules, vita humanior sine sale non quit degree […]” “Heaven known, a civilized life is impossible without salt” —Pliny the Elder, Natural History XXXI 88

Keywords

AMPA Receptor Cation Site Anion Site Domoic Acid Dime Interface 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Miller DJ. Sydney Ringer; physiological saline, calcium and the contraction of the heart. J Physiol 2004; 555:585–587.PubMedGoogle Scholar
  2. 2.
    Jordan J, Shannon JR, Grogan E et al. A potent pressor response elicited by drinking water. Lancet 1999; 353:723.PubMedGoogle Scholar
  3. 3.
    Wells CM, Di Cera E. Thrombin is a Na(+)-activated enzyme. Biochemistry 1992; 31:11721–11730.PubMedGoogle Scholar
  4. 4.
    Perutz MF, Shih DT, Williamson D. The chloride effect in human haemoglobin. A new kind of allosteric mechanism. J Mol Biol 1994; 239:555–560.PubMedGoogle Scholar
  5. 5.
    Hille B. Ion Channels of Excitable Membranes, 3rd Edition. Sunderland, MA, USA: Sinauer Associates; 2001.Google Scholar
  6. 6.
    Eisenman G. Cation selective glass electrodes and their mode of operation. Biophys J 1962; 2:259–323.PubMedGoogle Scholar
  7. 7.
    Nagem RA, Dauter Z, Polikarpov I. Protein crystal structure solution by fast incorporation of negatively and positively charged anomalous scatterers. Acta Crystallogr D Biol Crystallogr 2001; 57:996–1002.PubMedGoogle Scholar
  8. 8.
    Harding MM. Small revisions to predicted distances around metal sites in proteins. Acta Crystallogr D Biol Crystallogr 2006; 62:678–682.PubMedGoogle Scholar
  9. 9.
    Noskov SY, Roux B. Control of ion selectivity in LeuT: two Na+ binding sites with two different mechanisms. J Mol Biol 2008; 377:804–818.PubMedGoogle Scholar
  10. 10.
    Müller P, Köpke S, Sheldrick GM. Is the bond-valence method able to identify metal atoms in protein structures? Acta Crystallogr D Biol Crystallogr 2003; 59:32–37.PubMedGoogle Scholar
  11. 11.
    Nayal M, Cera ED. Valence screening of water in protein crystals reveals potential Na+ binding sites. J Mol Biol 1996; 256:228–234.PubMedGoogle Scholar
  12. 12.
    Pidcock E, Moore GR. Structural characteristics of protein binding sites for calcium and lanthanide ions. J Biol Inorg Chem 2001; 6:479–489.PubMedGoogle Scholar
  13. 13.
    Erreger K, Chen PE, Wyllie DJ et al. Glutamate receptor gating. Crit Rev Neurobiol 2004; 16:187–224.PubMedGoogle Scholar
  14. 14.
    Mayer ML. Glutamate receptor ion channels. Curr Opin Neurobiol 2005; 15:282–288.PubMedGoogle Scholar
  15. 15.
    Sobolevsky AI, Rosconi MP, Gouaux E. X-ray structure, symmetry and mechanism of an AMPA-sub-type glutamate receptor. Nature 2009; 462:745–756.PubMedGoogle Scholar
  16. 16.
    Das U, Kumar J, Mayer ML et al. Domain organization and function in GluK2 subtype kainate receptors. Proc Natl Acad Sci USA 2010:-.Google Scholar
  17. 17.
    Rosenmund C, Stern-Bach Y, Stevens CF. The tetrameric structure of a glutamate receptor channel. Science 1998; 280:1596–1599.PubMedGoogle Scholar
  18. 18.
    Jin R, Banke TG, Mayer ML et al. Structural basis for partial agonist action at ionotropic glutamate receptors. Nat Neurosci 2003; 6:803–810.PubMedGoogle Scholar
  19. 19.
    Verdoorn TA, Burnashev N, Monyer H et al. Structural determinants of ion flow through recombinant glutamate receptor channels. Science 1991; 252:1715–1718.PubMedGoogle Scholar
  20. 20.
    Burnashev N, Zhou Z, Neher E et al. Fractional calcium currents through recombinant GluR channels of the NMDA, AMPA and kainate receptor subtypes. J Physiol 1995; 485 (Pt 2):403–418.PubMedGoogle Scholar
  21. 21.
    Burnashev N, Villarroel A, Sakmann B. Dimensions and ion selectivity of recombinant AMPA and kainate receptor channels and their dependence on Q/R site residues. J Physiol 1996; 496 (Pt 1):165–173.PubMedGoogle Scholar
  22. 22.
    Köhler M, Burnashev N, Sakmann B et al. Determinants of Ca2+ permeability in both TM1 and TM2 of high affinity kainate receptor channels: diversity by RNA editing. Neuron 1993; 10:491–500.PubMedGoogle Scholar
  23. 23.
    Stern-Bach Y, Bettler B, Hartley M et al. Agonist selectivity of glutamate receptors is specified by two domains structurally related to bacterial amino acid-binding proteins. Neuron 1994; 13:1345–1357.PubMedGoogle Scholar
  24. 24.
    Ayalon G, Segev E, Elgavish S et al. Two regions in the N-terminal domain of ionotropic glutamate receptor 3 form the subunit oligomerization interfaces that control subtype-specific receptor assembly. J Biol Chem 2005; 280:15053–15060.PubMedGoogle Scholar
  25. 25.
    Frischknecht R, Heine M, Perrais D et al. Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 2009; 12:897–904.PubMedGoogle Scholar
  26. 26.
    Saglietti L, Dequidt C, Kamieniarz K et al. Extracellular interactions between GluR2 and N-cadherin in spine regulation. Neuron 2007; 54:461–477.PubMedGoogle Scholar
  27. 27.
    Kumar J, Schuck P, Jin R et al. The N-terminal domain of GluR6-subtype glutamate receptor ion channels. Nat Struct Mol Biol 2009; 16:631–638.PubMedGoogle Scholar
  28. 28.
    Nanao MH, Green T, Stern-Bach Y et al. Structure of the kainate receptor subunit GluR6 agonist-binding domain complexed with domoic acid. Proceedings of the National Academy of Sciences of the United States of America 2005; 102:1708–1713.PubMedGoogle Scholar
  29. 29.
    Clayton A, Siebold C, Gilbert RJC et al. Crystal Structure of the GluR2 Amino-Terminal Domain Provides Insights into the Architecture and Assembly of Ionotropic Glutamate Receptors. J Mol Biol 2009; 392:1125–1132.PubMedGoogle Scholar
  30. 30.
    Horning MS, Mayer ML. Regulation of AMPA receptor gating by ligand binding core dimers. Neuron 2004; 41:379–388.PubMedGoogle Scholar
  31. 31.
    Plested AJR, Mayer ML. Structure and mechanism of kainate receptor modulation by anions. Neuron 2007; 53:829–841.PubMedGoogle Scholar
  32. 32.
    Gielen M, Le Goff A, Stroebel D et al. Structural rearrangements of NR1/NR2A NMDA receptors during allosteric inhibition. Neuron 2008; 57:80–93.PubMedGoogle Scholar
  33. 33.
    Gielen M, Siegler Retchless B, Mony L et al. Mechanism of differential control of NMDA receptor activity by NR2 subunits. Nature 2009; 459:703–707.PubMedGoogle Scholar
  34. 34.
    Anson LC, Chen PE, Wyllie DJ et al. Identification of amino acid residues of the NR2A subunit that control glutamate potency in recombinant NR1/NR2A NMDA receptors. J Neurosci 1998; 18:581–589.PubMedGoogle Scholar
  35. 35.
    Jin R, Clark S, Weeks AM et al. Mechanism of positive allosteric modulators acting on AMPA receptors. J Neurosci 2005; 25:9027–9036.PubMedGoogle Scholar
  36. 36.
    Sun Y, Olson R, Horning M et al. Mechanism of glutamate receptor desensitization. Nature 2002; 417:245–253.PubMedGoogle Scholar
  37. 37.
    Mayer ML. Crystal structures of the GluR5 and GluR6 ligand binding cores: molecular mechanisms underlying kainate receptor selectivity. Neuron 2005; 45:539–552.PubMedGoogle Scholar
  38. 38.
    Mayer ML, Ghosal A, Dolman NP et al. Crystal structures of the kainate receptor GluR5 ligand binding core dimer with novel GluR5-selective antagonists. J Neurosci 2006; 26:2852–2861.PubMedGoogle Scholar
  39. 39.
    Plested AJR, Vijayan R, Biggin PC et al. Molecular basis of kainate receptor modulation by sodium. Neuron 2008; 58:720–735.PubMedGoogle Scholar
  40. 40.
    Chaudhry C, Weston MC, Schuck P et al. Stability of ligand-binding domain dimer assembly controls kainate receptor desensitization. EMBO J 2009; 28:1518–1530.PubMedGoogle Scholar
  41. 41.
    Chaudhry C, Plested AJ, Schuck P et al. Energetics of glutamate receptor ligand binding domain dimer assembly are modulated by allosteric ions. Proc Natl Acad Sci USA 2009; 106:12329–12334.PubMedGoogle Scholar
  42. 42.
    Fleck MW, Cornell E, Mah SJ. Amino-acid residues involved in glutamate receptor 6 kainate receptor gating and desensitization. J Neurosci 2003; 23:1219–1227.PubMedGoogle Scholar
  43. 43.
    Perouansky M, Grantyn R. Separation of quisqualate-and kainate-selective glutamate receptors in cultured neurons from the rat superior colliculus. J Neurosci 1989; 9:70–80.PubMedGoogle Scholar
  44. 44.
    Egebjerg J, Bettler B, Hermans-Borgmeyer I et al. Cloning of a cDNA for a glutamate receptor subunit activated by kainate but not AMPA. Nature 1991; 351:745–748.PubMedGoogle Scholar
  45. 45.
    Bowie D, Lange GD. Functional stoichiometry of glutamate receptor desensitization. J Neurosci 2002; 22:3392–3403.PubMedGoogle Scholar
  46. 46.
    Bowie D. External anions and cations distinguish between AMPA and kainate receptor gating mechanisms. J Physiol 2002; 539:725.PubMedGoogle Scholar
  47. 47.
    Balannik V, Menniti FS, Paternain AV et al. Molecular mechanism of AMPA receptor noncompetitive antagonism. Neuron 2005; 48:279–288.PubMedGoogle Scholar
  48. 48.
    Paternain AV, Cohen A, Stern-Bach Y et al. A role for extracellular Na+ in the channel gating of native and recombinant kainate receptors. J Neurosci 2003; 23:8641–8648.PubMedGoogle Scholar
  49. 49.
    Gonzalez J, Du M, Parameshwaran K et al. Role of dimer interface in activation and desensitization in AMPA receptors. Proc Natl Acad Sci USA 2010; 107:9891–9896.PubMedGoogle Scholar
  50. 50.
    Plested AJ, Mayer ML. AMPA receptor ligand binding domain mobility revealed by functional cross linking. J Neurosci 2009; 29:11912–11923.PubMedGoogle Scholar
  51. 51.
    Armstrong N, Jasti J, Beich-Frandsen M et al. Measurement of conformational changes accompanying desensitization in an ionotropic glutamate receptor. Cell 2006; 127:85–97.PubMedGoogle Scholar
  52. 52.
    Weston MC, Schuck P, Ghosal A et al. Conformational restriction blocks glutamate receptor desensitization. Nat Struct Mol Biol 2006; 13:1120–1127.PubMedGoogle Scholar
  53. 53.
    Stern-Bach Y, Russo S, Neuman M et al. A point mutation in the glutamate binding site blocks desensitization of AMPA receptors. Neuron 1998; 21:907–918.PubMedGoogle Scholar
  54. 54.
    Zhang Y, Nayeem N, Nanao MH et al. Interface interactions modulating desensitization of the kainate-selective ionotropic glutamate receptor subunit GluR6. J Neurosci 2006; 26:10033–10042.PubMedGoogle Scholar
  55. 55.
    Nayeem N, Zhang Y, Schweppe DK et al. A nondesensitizing kainate receptor point mutant. Mol Pharmacol 2009; 76:534–542.PubMedGoogle Scholar
  56. 56.
    Vijayan R, Plested AJ, Mayer ML et al. Selectivity and cooperativity of modulatory ions in a neurotransmitter receptor. Biophys J 2009; 96:1751–1760.PubMedGoogle Scholar
  57. 57.
    Wong AY, MacLean DM, Bowie D. Na+/VCl dipole couples agonist binding to kainate receptor activation. J Neurosci 2007; 27:6800–6809.PubMedGoogle Scholar
  58. 58.
    Plested AJ, Mayer ML. Engineering a high-affinity allosteric binding site for divalent cations in kainate receptors. Neuropharmacology 2009; 56:114–120.PubMedGoogle Scholar
  59. 59.
    Wollmuth LP, Kuner T, Jatzke C et al. The Lurcher mutation identifies delta 2 as an AMPA/kainate receptor-like channel that is potentiated by Ca(2+). J Neurosci 2000; 20:5973–5980.PubMedGoogle Scholar
  60. 60.
    Hansen KB, Naur P, Kurtkaya NL et al. Modulation of the dimer interface at ionotropic glutamate-like receptor delta 2 by D-serine and extracellular calcium. Journal of Neuroscience 2009; 29:907.PubMedGoogle Scholar
  61. 61.
    Koshland Jr DE. Application of a theory of enzyme specificity to protein synthesis. Proc Natl Acad Sci USA 1958; 44:98.PubMedGoogle Scholar
  62. 62.
    Wong AY, Fay AM, Bowie D. External ions are coactivators of kainate receptors. J Neurosci 2006; 26:5750–5755.PubMedGoogle Scholar
  63. 63.
    Ozawa S, Iino M, Tsuzuki K. Suppression by extracellular K+ of N-methyl-D-aspartate responses in cultured rat hippocampal neurons. J Neurophysiol 1990; 64:1361–1367.PubMedGoogle Scholar
  64. 64.
    Nahum-Levy R, Tam E, Shavit S et al. Glutamate but not glycine agonist affinity for NMDA receptors is influenced by small cations. J Neurosci 2002; 22:2550–2560.PubMedGoogle Scholar
  65. 65.
    Schneggenburger R, Ascher P. Coupling of permeation and gating in an NMDA-channel pore mutant. Neuron 1997; 18:167–177.PubMedGoogle Scholar
  66. 66.
    Karakas E, Simorowski N, Furukawa H. Structure of the zinc-bound amino-terminal domain of the NMDA receptor NR2B subunit. EMBO J 2009; 28:3910–3920.PubMedGoogle Scholar
  67. 67.
    Pitt SJ, Sivilotti LG, Beato M. High intracellular chloride slows the decay of glycinergic currents. J Neurosci 2008; 28:11454–11467.PubMedGoogle Scholar
  68. 68.
    Houston CM, Bright DP, Sivilotti LG et al. Intracellular chloride ions regulate the time course of GABA-mediated inhibitory synaptic transmission. J Neurosci 2009; 29:10416–10423.PubMedGoogle Scholar
  69. 69.
    Rivera C, Voipio J, Payne JA et al. The K+/Cl cotransporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 1999; 397:251–255.PubMedGoogle Scholar
  70. 70.
    Gill SB, Veruki ML, Hartveit E. Functional properties of spontaneous IPSCs and glycine receptors in rod amacrine (AII) cells in the rat retina. J Physiol 2006; 575:739–759.PubMedGoogle Scholar
  71. 71.
    Burzomato V, Beato M, Groot-Kormelink PJ et al. Single-channel behavior of heteromeric alpha1beta glycine receptors: an attempt to detect a conformational change before the channel opens. J Neurosci 2004; 24:10924–10940.PubMedGoogle Scholar
  72. 72.
    Manthey AA. Delay of desensitization onset by potassium ion in voltage-clamped frog muscle fibers. Am J Physiol Cell Physiol 1985; 249:C435–C446.Google Scholar
  73. 73.
    Akk G, Auerbach A. Inorganic, monovalent cations compete with agonists for the transmitter binding site of nicotinic acetylcholine receptors. Biophys J 1996; 70:2652–2658.PubMedGoogle Scholar
  74. 74.
    Akk G, Zhou M, Auerbach A. A mutational analysis of the acetylcholine receptor channel transmitter binding site. Biophysical Journal 1999; 76:207–218.PubMedGoogle Scholar
  75. 75.
    Riedel T, Schmalzing G, Markwardt F. Influence of extracellular monovalent cations on pore and gating properties of P2X7 receptor-operated single-channel currents. Biophys J 2007; 93:846–858.PubMedGoogle Scholar
  76. 76.
    Ma W, Korngreen A, Uzlaner N et al. Extracellular sodium regulates airway ciliary motility by inhibiting a P2X receptor. Nature 1999; 400:894–897.PubMedGoogle Scholar
  77. 77.
    Kawate T, Michel JC, Birdsong WT et al. Crystal structure of the ATP-gated P2X(4) ion channel in the closed state. Nature 2009; 460:592–598.PubMedGoogle Scholar
  78. 78.
    Jasti J, Furukawa H, Gonzales EB et al. Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature 2007; 449:316–323.PubMedGoogle Scholar
  79. 79.
    Babai N, Kanevsky N, Dascal N et al. Anion-sensitive regions of L-type CaV1.2 calcium channels expressed in HEK293 cells. PLoS One 2010; 5:e8602.PubMedGoogle Scholar
  80. 80.
    Bekar LK, Loewen ME, Forsyth GW et al. Chloride concentration affects Kv channel voltage-gating kinetics: Importance of experimental anion concentrations. Brain Res Bull 2005; 67:142–146.PubMedGoogle Scholar
  81. 81.
    Paternain AV, Rodriguez-Moreno A, Villarroel A et al. Activation and desensitization properties of native and recombinant kainate receptors. Neuropharmacology 1998; 37:1249–1259.PubMedGoogle Scholar
  82. 82.
    DeVries SH, Schwartz EA. Kainate receptors mediate synaptic transmission between cones and ‘Off’ bipolar cells in a mammalian retina. Nature 1999; 397:157–160.PubMedGoogle Scholar
  83. 83.
    DeVries SH. Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 2000; 28:847–856.PubMedGoogle Scholar
  84. 84.
    Zhang W, St-Gelais F, Grabner CP et al. A transmembrane accessory subunit that modulates kainate-type glutamate receptors. Neuron 2009; 61:385–396.PubMedGoogle Scholar
  85. 85.
    Kim KS, Yan D, Tomita S. Assembly and stoichiometry of the AMPA receptor and transmembrane AMPA receptor regulatory protein complex. J Neurosci 2010; 30:1064–1072.PubMedGoogle Scholar
  86. 86.
    Morimoto-Tomita M, Zhang W, Straub C et al. Autoinactivation of neuronal AMPA receptors via glutamate-regulated TARP interaction. Neuron 2009; 61:101–112.PubMedGoogle Scholar
  87. 87.
    Penn AC, Williams SR, Greger IH. Gating motions underlie AMPA receptor secretion from the endoplasmic reticulum. EMBO J 2008; 27:3056–3068.PubMedGoogle Scholar
  88. 88.
    Greger IH, Akamine P, Khatri L et al. Developmentally regulated, combinatorial RNA processing modulates AMPA receptor biogenesis. Neuron 2006; 51:85–97.PubMedGoogle Scholar
  89. 89.
    Mah SJ, Cornell E, Mitchell NA et al. Glutamate receptor trafficking: endoplasmic reticulum quality control involves ligand binding and receptor function. J Neurosci 2005; 25:2215–2225.PubMedGoogle Scholar
  90. 90.
    Valluru L, Xu J, Zhu Y et al. Ligand binding is a critical requirement for plasma membrane expression of heteromeric kainate receptors. J Biol Chem 2005; 280:6085–6093.PubMedGoogle Scholar
  91. 91.
    Sylantyev S, Savtchenko LP, Niu YP et al. Electric fields due to synaptic currents sharpen excitatory transmission. Science (New York, N.Y.) 2008; 319:1845–1849.Google Scholar
  92. 92.
    Breustedt J, Schmitz D. Assessing the role of GLUK5 and GLUK6 at hippocampal mossy fiber synapses. J Neurosci 2004; 24:10093–10098.PubMedGoogle Scholar
  93. 93.
    Chittajallu R, Vignes M, Dev KK et al. Regulation of glutamate release by presynaptic kainate receptors in the hippocampus. Nature 1996; 379:78–81.PubMedGoogle Scholar
  94. 94.
    Sachidhanandam S, Blanchet C, Jeantet Y et al. Kainate receptors act as conditional amplifiers of spike transmission at hippocampal mossy fiber synapses. J Neurosci 2009; 29:5000–5008.PubMedGoogle Scholar
  95. 95.
    Orlov SN, Mongin AA. Salt-sensing mechanisms in blood pressure regulation and hypertension. Am J Physiol Heart Circ Physiol 2007; 293:H2039–H2053.PubMedGoogle Scholar
  96. 96.
    de Wardener HE. The hypothalamus and hypertension. Physiol Rev 2001; 81:1599–1658.PubMedGoogle Scholar
  97. 97.
    Hiyama TY, Watanabe E, Ono K et al. Na(x) channel involved in CNS sodium-level sensing. Nat Neurosci 2002; 5:511–512.PubMedGoogle Scholar
  98. 98.
    Hiyama TY, Watanabe E, Okado H et al. The subfornical organ is the primary locus of sodium-level sensing by Na(x) sodium channels for the control of salt-intake behavior. J Neurosci 2004; 24:9276–9281.PubMedGoogle Scholar
  99. 99.
    Shimizu H, Watanabe E, Hiyama TY et al. Glial Nax channels control lactate signaling to neurons for brain [Na+] sensing. Neuron 2007; 54:59–72.PubMedGoogle Scholar
  100. 100.
    Nagakura A, Hiyama TY, Noda M. Na(x)-deficient mice show normal vasopressin response to dehydration. Neurosci Lett 2010; 472:161–165.PubMedGoogle Scholar
  101. 101.
    Swenson KL, Badre SE, Morsette DJ et al. N-methyl-D-aspartic acid stimulation of vasopressin release: role in osmotic regulation and modulation by gonadal steroids. J Neuroendocrinol 1998; 10:679–685.PubMedGoogle Scholar
  102. 102.
    Sladek CD, Badre SE, Morsette DJ et al. Role of nonNMDA receptors in osmotic and glutamate stimulation of vasopressin release: effect of rapid receptor desensitization. J Neuroendocrinol 1998; 10:897–903.PubMedGoogle Scholar
  103. 103.
    Xu SH, Inenaga K, Honda E et al. Glutamatergic synaptic inputs activate neurons in the subfornical organ through nonNMDA receptors. J Auton Nerv Syst 2000; 78:177–180.PubMedGoogle Scholar
  104. 104.
    Morsette DJ, Swenson KL, Badre SE et al. Regulation of vasopressin release by ionotropic glutamate receptor agonists. Adv Exp Med Biol 1998; 449:129–130.PubMedGoogle Scholar
  105. 105.
    Morsette DJ, Sidorowicz H, Sladek CD. Role of nonNMDA receptors in vasopressin and oxytocin release from rat hypothalamo-neurohypophysial explants. Am J Physiol Regul Integr Comp Physiol 2001; 280:R313–R322.PubMedGoogle Scholar
  106. 106.
    Chaudhari N, Yang H, Lamp C et al. The taste of monosodium glutamate: membrane receptors in taste buds. J Neurosci 1996; 16:3817–3826.PubMedGoogle Scholar
  107. 107.
    Chaudhari N, Pereira E, Roper SD. Taste receptors for umami: the case for multiple receptors. Am J Clin Nutr 2009; 90:738S–742S.PubMedGoogle Scholar
  108. 108.
    Chung KM, Lee SB, Heur R et al. Glutamate-induced cobalt uptake elicited by kainate receptors in rat taste bud cells. Chem Senses 2005; 30:137–143.PubMedGoogle Scholar
  109. 109.
    Caicedo A, Jafri MS, Roper SD. In situ Ca2+ imaging reveals neurotransmitter receptors for glutamate in taste receptor cells. J Neurosci 2000; 20:7978–7985.PubMedGoogle Scholar
  110. 110.
    O’Mahony M, Kingsley L, Harji A et al. What sensation signals the salt taste threshold? Chem. Senses 1976; 2:177–188.Google Scholar
  111. 111.
    Roper SD. Signal transduction and information processing in mammalian taste buds. Pflugers Arch 2007; 454:759–776.PubMedGoogle Scholar
  112. 112.
    Chandrashekar J, Kuhn C, Oka Y et al. The cells and peripheral representation of sodium taste in mice. Nature 2010; 464:297–301.PubMedGoogle Scholar
  113. 113.
    Christie LA, Russell TA, Xu J et al. Contractor A. AMPA receptor desensitization mutation results in severe developmental phenotypes and early postnatal lethality. Proc Natl Acad Sci USA 2010; 107:9412–9417.PubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Leibniz-Institut für Molekulare Pharmakologie (FMP)BerlinGermany

Personalised recommendations