Upregulation of KCC2 activity by zinc-mediated neurotransmission via the mZnR/GPR39 receptor

Journal of Neuroscience

Volumn 31, Issue 36, 2011, Pages 12916-12926

  Chorin, Ehud ^a   Vinograd, Ofir ^a   Fleidervish, Ilya ^a   Gilad, David ^a   Herrmann, Sharon ^a   Sekler, Israel ^a   Aizenman, Elias ^a,b   Hershfinkel, Michal ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CHLORIDE ION; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 39; METABOTROPIC RECEPTOR; POTASSIUM CHLORIDE COTRANSPORTER; UNCLASSIFIED DRUG; ZINC; ZINC ION; ZINC SENSING RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CHANNEL GATING; CHLORIDE TRANSPORT; CONTROLLED STUDY; FEMALE; HIPPOCAMPAL MOSSY FIBER; HUMAN; HUMAN CELL; HYPERPOLARIZATION; MALE; MOUSE; NERVE CELL; NEUROTRANSMISSION; NEWBORN; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; UPREGULATION;

ANIMALS; BLOTTING, WESTERN; CA3 REGION, HIPPOCAMPAL; ELECTROPHYSIOLOGICAL PHENOMENA; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GENOTYPE; MALE; MICE; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; MOSSY FIBERS, HIPPOCAMPAL; PATCH-CLAMP TECHNIQUES; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, GABA-A; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SYMPORTERS; SYNAPSES; SYNAPTIC TRANSMISSION; UP-REGULATION; ZINC;

EID: 80052567863     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2205-11.2011     Document Type: Article

References (95)

1. Aizenman E, Stout AK, Hartnett KA, Dineley KE, McLaughlin B, Reynolds IJ (2000) Induction of neuronal apoptosis by thiol oxidation: putative role of intracellular zinc release. J Neurochem 75:1878-1878.
2. Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571-571.
3. Amaral DG, Scharfman HE, Lavenex P (2007) The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 163:3-3.
4. Banke TG, Gegelashvili G (2008) Tonic activation of group I mGluRs modulates inhibitory synaptic strength by regulating KCC2 activity. J Physiol 586:4925-4934.
5. Beierlein M, Fall CP, Rinzel J, Yuste R (2002) Thalamocortical bursts trigger recurrent activity in neocortical networks: layer 4 as a frequencydependent gate. J Neurosci 22:9885-9885.
6. Belloni-Olivi L, Marshall C, Laal B, Andrews GK, Bressler J (2009) Localization of zip1 and zip4 mRNA in the adult rat brain. J Neurosci Res 87:3221-3221.
7. Ben-Ari Y, Cherubini E (1991) Zinc and GABA in developing brain. Nature 353:220-220.
8. Besser L, Chorin E, Sekler I, Silverman WF, Atkin S, Russell JT, Hershfinkel M (2009) Synaptically released zinc triggers metabotropic signaling via a zinc-sensing receptor in the hippocampus. J Neurosci 29:2890-2890.
9. 2+ rises in hippocampal pyramidal cells. J Neurophysiol 81:2903-2903.
10. Bischofberger J, Engel D, Li L, Geiger JR, Jonas P (2006) Patch-clamp recording from mossy fiber terminals in hippocampal slices. Nat Protoc 1:2075-2075.
11. Blaesse P, Airaksinen MS, Rivera C, Kaila K (2009) Cation-chloride cotransporters and neuronal function. Neuron 61:820-820.
12. Blanton MG, Lo Turco JJ, Kriegstein AR (1989) Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex. J Neurosci Methods 30:203-203.
13. Blasco-Ibáñez JM, Poza-Aznar J, Crespo C, Marqués-Marí AI, Gracia-Llanes FJ, Martínez-Guijarro FJ (2004) Chelation of synaptic zinc induces overexcitation in the hilar mossy cells of the rat hippocampus. Neurosci Lett 355:101-101.
14. Bonnet U, Wiemann M (1999) Ammonium prepulse: effects on intracellular pH and bioelectric activity of CA3-neurones in guinea pig hippocampal slices. Brain Res 840:16-16.
15. Buzsáki G, Freund TF, Bayardo F, Somogyi P (1989) Ischemia-induced changes in the electrical activity of the hippocampus. Exp Brain Res 78:268-268.
16. 2+ release and accumulation. J Cereb Blood Flow Metab 31:1073-1073.
17. Chudotvorova I, Ivanov A, Rama S, Hübner CA, Pellegrino C, Ben-Ari Y, Medina I (2005) Early expression of KCC2 in rat hippocampal cultures augments expression of functional GABA synapses. J Physiol 566:671-679.
18. Cole TB, Wenzel HJ, Kafer KE, Schwartzkroin PA, Palmiter RD (1999) Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene. Proc Natl Acad Sci U S A 96:1716-1716.
19. Cole TB, Robbins CA, Wenzel HJ, Schwartzkroin PA, Palmiter RD (2000) Seizures and neuronal damage in mice lacking vesicular zinc. Epilepsy Res 39:153-153.
20. 2+ influx is critical for some forms of spreading depression in brain slices. J Neurosci 28:8014-8014.
21. Doering P, Danscher G, Larsen A, Bruhn M, Søndergaard C, Stoltenberg M (2007) Changes in the vesicular zinc pattern following traumatic brain injury. Neuroscience 150:93-93.
22. Elsas SM, Hazany S, Gregory WL, Mody I (2009) Hippocampal zinc infusion delays the development of afterdischarges and seizures in a kindling model of epilepsy. Epilepsia 50:870-870.
23. 2+-dependent regulation of KCC2 function. Neuron 48:773-773.
24. Frederickson CJ, Howell GA, Frederickson MH (1981) Zinc dithizonate staining in the cat hippocampus: relationship to the mossy-fiber neuropil and postnatal development. Exp Neurol 73:812-823.
25. Frederickson CJ, Giblin LJ 3rd, Rengarajan B, Masalha R, Frederickson CJ, Zeng Y, Lopez EV, Koh JY, Chorin U, Besser L, Hershfinkel M, Li Y, Thompson RB, Krezel A (2006) Synaptic release of zinc from brain slices: factors governing release, imaging, and accurate calculation of concentration. J Neurosci Methods 154:19-19.
26. Fukahori M, Itoh M (1990) Effects of dietary zinc status on seizure susceptibility and hippocampal zinc content in the El (epilepsy) mouse. Brain Res 529:16-16.
27. Galeffi F, Sah R, Pond BB, George A, Schwartz-Bloom RD (2004) Changes in intracellular chloride after oxygen-glucose deprivation of the adult hippocampal slice: effect of diazepam. J Neurosci 24:4478-4478.
28. Ganesh R, Janakiraman L (2008) Serum zinc levels in children with simple febrile seizure. Clin Pediatr (Phila) 47:164-164.
29. Goldberg HJ, Sheehy EM (1982) Fifth day fits: an acute zinc deficiency syndrome? Arch Dis Child 57:633-635.
30. Haas HL, Schaerer B, Vosmansky M (1979) A simple perfusion chamber for the study of nervous tissue slices in vitro. J Neurosci Methods 1:323-323.
31. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391:85-85.
32. 2+ and regulates ion transport. Proc Natl Acad Sci U S A 98:11749-11749.
33. Hershfinkel M, Silverman WF, Sekler I (2007) The zinc sensing receptor, a link between zinc and cell signaling. Mol Med 13:331-331.
34. Hershfinkel M, Kandler K, Knoch ME, Dagan-Rabin M, Aras MA, Abramovitch-Dahan C, Sekler I, Aizenman E (2009) Intracellular zinc inhibits KCC2 transporter activity. Nat Neurosci 12:725-725.
35. Hosie AM, Dunne EL, Harvey RJ, Smart TG (2003) Zinc-mediated inhibition of GABA(A) receptors: discrete binding sites underlie subtype specificity. Nat Neurosci 6:362-362.
36. Huberfeld G, Wittner L, Clemenceau S, Baulac M, Kaila K, Miles R, Rivera C (2007) Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy. J Neurosci 27:9866-9866.
37. Jackson VR, Nothacker HP, Civelli O (2006) GPR39 receptor expression in the mouse brain. Neuroreport 17:813-816.
38. Kahle KT, Rinehart J, Lifton RP (2010) Phosphoregulation of the Na-K-2Cl and K-Cl cotransporters by the WNK kinases. Biochim Biophys Acta 1802:1150-1150.
39. Kan I, Ben-Zur T, Barhum Y, Levy YS, Burstein A, Charlow T, Bulvik S, Melamed E, Offen D (2007) Dopaminergic differentiation of human mesenchymal stem cells- utilization of bioassay for tyrosine hydroxylase expression. Neurosci Lett 419:28-28.
40. 2+ release in CA3 pyramidal neurons via a metabotropic glutamate receptor pathway. Neuroscience 107:59-59.
41. Khirug S, Ahmad F, Puskarjov M, Afzalov R, Kaila K, Blaesse P (2010) A single seizure episode leads to rapid functional activation of KCC2 in the neonatal rat hippocampus. J Neurosci 30:12028-12028.
42. Laube B, Kuhse J, Rundström N, Kirsch J, Schmieden V, Betz H (1995) Modulation by zinc ions of native rat and recombinant human inhibitory glycine receptors. J Physiol 483:613-619.
43. Lee H, Chen CX, Liu YJ, Aizenman E, Kandler K (2005) KCC2 expression in immature rat cortical neurons is sufficient to switch the polarity of GABA responses. Eur J Neurosci 21:2593-2593.
44. Lee HH, Walker JA, Williams JR, Goodier RJ, Payne JA, Moss SJ (2007) Direct protein kinase C-dependent phosphorylation regulates the cell surface Stability and activity of the potassium chloride cotransporter KCC2. J Biol Chem 282:29777-29777.
45. Lee HH, Jurd R, Moss SJ (2010) Tyrosine phosphorylation regulates the membrane trafficking of the potassium chloride co-transporter KCC2. Mol Cell Neurosci 45:173-173.
46. Liguz-Lecznar M, Nowicka D, Czupryn A, Skangiel-Kramska J (2005) Dissociation of synaptic zinc level and zinc transporter 3 expression during postnatal development and after sensory deprivation in the barrel cortex of mice. Brain Res Bull 66:106-106.
47. Lopantsev V, Wenzel HJ, Cole TB, Palmiter RD, Schwartzkroin PA (2003) Lack of vesicular zinc in mossy fibers does not affect synaptic excitability of CA3 pyramidal cells in zinc transporter 3 knockout mice. Neuroscience 116:237-237.
48. Lu J, Karadsheh M, Delpire E (1999) Developmental regulation of the neuronal-specific isoform of K-Cl cotransporter KCC2 in postnatal rat brains. J Neurobiol 39:558-558.
49. 2+ and NR1 antagonist. Proc Natl Acad Sci U S A 105:12563-12563.
50. Marandi N, Konnerth A, Garaschuk O (2002) Two-photon chloride imaging in neurons of brain slices. Pflugers Arch 445:357-357.
51. Moechars D, Depoortere I, Moreaux B, de Smet B, Goris I, Hoskens L, Daneels G, Kass S, Ver Donck L, Peeters T, Coulie B (2006) Altered gastrointestinal and metabolic function in the GPR39-obestatin receptorknockout mouse. Gastroenterology 131:1131-1131.
52. Nitzan YB, Sekler I, Hershfinkel M, Moran A, Silverman WF (2002) Postnatal regulation of ZnT-1 expression in the mouse brain. Brain Res Dev Brain Res 137:149-149.
53. Palmiter RD, Cole TB, Quaife CJ, Findley SD (1996) ZnT-3, a putative transporter of zinc into synaptic vesicles. Proc Natl Acad Sci U S A 93:14934-14934.
54. Paoletti P, Vergnano AM, Barbour B, Casado M (2009) Zinc at glutamatergic synapses. Neuroscience 158:126-126.
55. Papp E, Rivera C, Kaila K, Freund TF (2008) Relationship between neuronal vulnerability and potassium-chloride cotransporter 2 immunoreactivity in hippocampus following transient forebrain ischemia. Neuroscience 154:677-689.
56. Pond BB, Galeffi F, Ahrens R, Schwartz-Bloom RD (2004) Chloride transport inhibitors influence recovery from oxygen-glucose deprivationinduced cellular injury in adult hippocampus. Neuropharmacology 47:253-253.
57. Qian J, Noebels JL (2005) Visualization of transmitter release with zinc fluorescence detection at the mouse hippocampal mossy fibre synapse. J Physiol 566:747-747.
58. Qian J, Noebels JL (2006) Exocytosis of vesicular zinc reveals persistent depression of neurotransmitter release during metabotropic glutamate receptor long-term depression at the hippocampal CA3-CA1 synapse. J Neurosci 26:6089-6089.
59. Qian J, Xu K, Yoo J, Chen TT, Andrews G, Noebels JL (2011) Knockout of Zn transporters Zip-1 and Zip-3 attenuates seizure-induced CA1 neurodegeneration. J Neurosci 31:97-97.
60. Redman PT, Hartnett KA, Aras MA, Levitan ES, Aizenman E (2009) Regulation of apoptotic potassium currents by coordinated zinc-dependent signalling. J Physiol 587:4393-4404.
61. Reynolds IJ (2001) Measurement of cation movement in primary cultures using fluorescent dyes. Curr Protoc Neurosci Chapter 7:Unit7.11.
62. Rinehart J, Maksimova YD, Tanis JE, Stone KL, Hodson CA, Zhang J, Risinger M, Pan W, Wu D, Colangelo CM, Forbush B, Joiner CH, Gulcicek EE, Gallagher PG, Lifton RP (2009) Sites of regulated phosphorylation that control K-Cl cotransporter activity. Cell 138:525-525.
63. Ritucci NA, Erlichman JS, Dean JB, Putnam RW (1996) A fluorescence technique to measure intracellular pH of single neurons in brainstem slices. J Neurosci Methods 68:149-149.
64. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251-251.
65. - extrusion. J Cell Biol 159:747-747.
66. Rivera C, Voipio J, Thomas-Crusells J, Li H, Emri Z, Sipilä S, Payne JA, Minichiello L, Saarma M, Kaila K (2004) Mechanism of activitydependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J Neurosci 24:4683-4691.
67. Ruusuvuori E, Li H, Huttu K, Palva JM, Smirnov S, Rivera C, Kaila K, Voipio J (2004) Carbonic anhydrase isoform VII acts as a molecular switch in the development of synchronous gamma-frequency firing of hippocampal CA1 pyramidal cells. J Neurosci 24:2699-2699.
68. 2+-store-dependent short-term plasticity at hippocampal mossy fiber synapses. J Neurosci 28:13139-13139.
69. 2+ uptake and persistent mitochondrial dysfunction. Eur J Neurosci 12:3813-3813.
70. Sensi SL, Paoletti P, Bush AI, Sekler I (2009) Zinc in the physiology and pathology of the CNS. Nat Rev Neurosci 10:780-780.
71. - cotransporter in human nasal epithelia. J Biol Chem 279:18567-18567.
72. Sindreu CB, Varoqui H, Erickson JD, Pérez-Clausell J (2003) Boutons containing vesicular zinc define a subpopulation of synapses with low AMPAR content in rat hippocampus. Cereb Cortex 13:823-829.
73. Sindreu C, Palmiter RD, Storm DR (2011) Zinc transporter ZnT-3 regulates presynaptic Erk1/2 signaling and hippocampus-dependent memory. Proc Natl Acad Sci U S A 108:3366-3366.
74. Smart TG, Moss SJ, Xie X, Huganir RL (1991) GABAA receptors are differentially sensitive to zinc: dependence on subunit composition. Br J Pharmacol 103:1837-1837.
75. 2+ ions: modulators of excitatory and inhibitory synaptic activity. Neuroscientist 10:432-442.
76. Strange K, Singer TD, Morrison R, Delpire E (2000) Dependence of KCC2 K-Cl cotransporter activity on a conserved carboxy terminus tyrosine residue. Am J Physiol Cell Physiol 279:C860-C867.
77. Stuart GJ, Dodt HU, Sakmann B (1993) Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflugers Arch 423:511-511.
78. Takeda A, Tamano H, Nagayoshi A, Yamada K, Oku N (2005) Increase in hippocampal cell death after treatment with kainate in zinc deficiency. Neurochem Int 47:539-539.
79. Thomas-Crusells J, Vieira A, Saarma M, Rivera C (2003) Anovel method for monitoring surface membrane trafficking on hippocampal acute slice preparation. J Neurosci Methods 125:159-159.
80. Titz S, Hormuzdi S, Lewen A, Monyer H, Misgeld U (2006) Intracellular acidification in neurons induced by ammonium depends on KCC2 function. Eur J Neurosci 23:454-454.
81. Trapp S, Lückermann M, Brooks PA, Ballanyi K (1996) Acidosis of rat dorsal vagal neurons in situ during spontaneous and evoked activity. J Physiol 496:695-695.
82. Tyzio R, Cossart R, Khalilov I, Minlebaev M, Hübner CA, Represa A, Ben-Ari Y, Khazipov R (2006) Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 314:1788-1788.
83. Verkman AS (1990) Development and biological applications of chloridesensitive fluorescent indicators. Am J Physiol 259:C375-375.
84. Vogt K, Mellor J, Tong G, Nicoll R (2000) The actions of synaptically released zinc at hippocampal mossy fiber synapses. Neuron 26:187-187.
85. Wake H, Watanabe M, Moorhouse AJ, Kanematsu T, Horibe S, Matsukawa N, Asai K, Ojika K, Hirata M, Nabekura J (2007) Early changes in KCC2 phosphorylation in response to neuronal stress result in functional downregulation. J Neurosci 27:1642-1642.
86. - cotransporters in lipid rafts by tyrosine phosphorylation. J Biol Chem 284:27980-27980.
87. Wenzel HJ, Cole TB, Born DE, Schwartzkroin PA, Palmiter RD (1997) Ultrastructural localization of zinc transporter-3 (ZnT-3) to synaptic vesicle membranes within mossy fiber boutons in the hippocampus of mouse and monkey. Proc Natl Acad Sci U S A 94:12676-12676.
88. Werman R (1966) Criteria for identification of a central nervous system transmitter. Comp Biochem Physiol 18:745-745.
89. Woo NS, Lu J, England R, McClellan R, Dufour S, Mount DB, Deutch AY, Lovinger DM, Delpire E (2002) Hyperexcitability and epilepsy associated with disruption of the mouse neuronal-specific K-Cl cotransporter gene. Hippocampus 12:258-258.
90. Woodin MA, Ganguly K, Poo MM (2003) Coincident pre-and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cltransporter activity. Neuron 39:807-820.
91. 2+ as an endogenous agonist of GPR39 from fetal bovine serum. J Recept Signal Transduct Res 27:235-235.
92. Zhang JV, Ren PG, Avsian-Kretchmer O, Luo CW, Rauch R, Klein C, Hsueh AJ (2005) Obestatin, a peptide encoded by the ghrelin gene, opposes ghrelin's effects on food intake. Science 310:996-996.
93. Zhang Y, Wang H, Li J, Jimenez DA, Levitan ES, Aizenman E, Rosenberg PA (2004) Peroxynitrite-induced neuronal apoptosis is mediated by intracellular zinc release and 12-lipoxygenase activation. J Neurosci 24:10616-10616.
94. Zhang Y, Wang H, Li J, Dong L, Xu P, Chen W, Neve RL, Volpe JJ, Rosenberg PA (2006) Intracellular zinc release and ERK phosphorylation are required upstream of 12-lipoxygenase activation in peroxynitrite toxicity to mature rat oligodendrocytes. J Biol Chem 281:9460-9460.
95. Zhao B, Wong AY, Murshid A, Bowie D, Presley JF, Bedford FK (2008) Identification of a novel di-leucine motif mediating K(+)/Cl(-) cotransporter KCC2 constitutive endocytosis. Cell Signal 20:1769-1779.