SNARE-dependent upregulation of potassium chloride co-transporter 2 activity after metabotropic zinc receptor activation in rat cortical neurons in vitro

Neuroscience

Volumn 210, Issue , 2012, Pages 38-46

  Saadi, R A ^a   He, K ^a   Hartnett, K A ^a   Kandler, K ^a   Hershfinkel, M ^b   Aizenman, E ^a,b  

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

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Botulinum toxin; GPR39; KCC2; Metabotropic zinc receptor; SNARE; Zinc

Indexed keywords

4 AMINOBUTYRIC ACID; AMMONIA; BOTULINUM TOXIN; BOTULINUM TOXIN C1; CALCIUM ION; METABOTROPIC ZINC RECEPTOR; POTASSIUM CHLORIDE COTRANSPORTER; POTASSIUM CHLORIDE COTRANSPORTER 2; RECEPTOR; SNARE PROTEIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; UNCLASSIFIED DRUG; ZINC ION;

ANIMAL CELL; ARTICLE; BRAIN CELL; CALCIUM SIGNALING; CELL LEVEL; CELL PH; CONTROLLED STUDY; GENETIC TRANSFECTION; HIPPOCAMPUS; IN VITRO STUDY; NERVE POTENTIAL; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; UPREGULATION; WILD TYPE; ZINC CELL LEVEL;

ANIMALS; BLOTTING, WESTERN; CEREBRAL CORTEX; IMMUNOBLOTTING; MICE; MICE, KNOCKOUT; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; SNARE PROTEINS; SYMPORTERS; TRANSFECTION; UP-REGULATION; ZINC;

EID: 84861202732     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.03.001     Document Type: Article

References (50)

1. Balakrishnan V., Becker M., Löhrke S., Nothwang H.G., Guresir E., Friauf E. Expression and function of chloride transporters during development of inhibitory neurotransmission in the auditory brainstem. J Neurosci 2003, 23:4134-4145.
2. Balasubramanian L., Sham J.S., Yip K.P. Calcium signaling in vasopressin-induced aquaporin-2 trafficking. Pflugers Arch 2008, 456:747-754.
3. +-ATPase in cultured inner medullary collecting duct cells. Am J Physiol Cell Physiol 2001, 280:C775-C781.
4. Besser L., Chorin E., Sekler I., Silverman W.F., Atkin S., Russell J.T., Hershfinkel M. Synaptically released zinc triggers metabotropic signaling via a zinc-sensing receptor in the hippocampus. J Neurosci 2009, 29:2890-2901.
5. Blasco-Ibanez J.M., Poza-Aznar J., Crespo C., Marques-Mari A.I., Gracia-Llanes F.J., Martinez-Guijarro F.J. Chelation of synaptic zinc induces overexcitation in the hilar mossy cells of the rat hippocampus. Neurosci Lett 2004, 355:101-104.
6. Chorin E., Vinograd O., Fleidervish I., Gilad D., Herrmann S., Sekler I., Aizenman E., Hershfinkel M. Upregulation of KCC2 activity by zinc-mediated neurotransmission via the mZnR/GPR39 receptor. J Neurosci 2011, 31:12916-12926.
7. Cole T.B., Robbins C.A., Wenzel H.J., Schwartzkroin P.A., Palmiter R.D. Seizures and neuronal damage in mice lacking vesicular zinc. Epilepsy Res 2000, 39:153-169.
8. Elsas S.M., Hazany S., Gregory W.L., Mody I. Hippocampal zinc infusion delays the development of afterdischarges and seizures in a kindling model of epilepsy. Epilepsia 2009, 50:870-879.
9. Farrant M., Kaila K. The cellular, molecular and ionic basis of GABA(A) receptor signalling. Prog Brain Res 2007, 160:59-87.
10. Frederickson C.J., Koh J.Y., Bush A.I. The neurobiology of zinc in health and disease. Nat Rev Neurosci 2005, 6:449-462.
11. Fukahori M., Itoh M. Effects of dietary zinc status on seizure susceptibility and hippocampal zinc content in the El (epilepsy) mouse. Brain Res 1990, 529:16-22.
12. Ganesh R., Janakiraman L. Serum zinc levels in children with simple febrile seizure. Clin Pediatr (Phila) 2008, 47:164-166.
13. Goldberg H.J., Sheehy E.M. Fifth day fits: an acute zinc deficiency syndrome?. Arch Dis Child 1982, 57:633-635.
14. 2+-free solutions in rat cortical neurons in vitro. J Neurochem 1997, 68:1836-1845.
15. Hershfinkel M., Kandler K., Knoch M.E., Dagan-Rabin M., Aras M.A., Abramovitch-Dahan C., Sekler I., Aizenman E. Intracellular zinc inhibits KCC2 transporter activity. Nat Neurosci 2009, 12:725-727.
16. 2+ and regulates ion transport. Proc Natl Acad Sci U S A 2001, 98:11749-11754.
17. Hosie A.M., Dunne E.L., Harvey R.J., Smart T.G. Zinc-mediated inhibition of GABA(A) receptors: discrete binding sites underlie subtype specificity. Nat Neurosci 2003, 6:362-369.
18. Huberfeld G., Wittner L., Clemenceau S., Baulac M., Kaila K., Miles R., Rivera C. Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy. J Neurosci 2007, 27:9866-9873.
19. Jaenisch N., Witte O.W., Frahm C. Downregulation of potassium chloride cotransporter KCC2 after transient focal cerebral ischemia. Stroke 2010, 41:e151-e159.
20. Khirug S., Ahmad F., Puskarjov M., Afzalov R., Kaila K., Blaesse P. A single seizure episode leads to rapid functional activation of KCC2 in the neonatal rat hippocampus. J Neurosci 2010, 30:12028-12035.
21. Lau C.G., Takayasu Y., Rodenas-Ruano A., Paternain A.V., Lerma J., Bennett M.V., Zukin R.S. SNAP-25 is a target of protein kinase C phosphorylation critical to NMDA receptor trafficking. J Neurosci 2010, 30:242-254.
22. 2+ sensitivity of a subpopulation of presynaptic vesicles at hippocampal mossy fiber terminals. J Neurosci 2011, 31:18251-18265.
23. Lee H., Chen C.X., Liu Y.J., Aizenman E., Kandler K. KCC2 expression in immature rat cortical neurons is sufficient to switch the polarity of GABA responses. Eur J Neurosci 2005, 21:2593-2599.
24. Lee H.H., Deeb T.Z., Walker J.A., Davies P.A., Moss S.J. NMDA receptor activity downregulates KCC2 resulting in depolarizing GABAA receptor-mediated currents. Nat Neurosci 2011, 14:736-743.
25. Lee H.H., Jurd R., Moss S.J. Tyrosine phosphorylation regulates the membrane trafficking of the potassium chloride co-transporter KCC2. Mol Cell Neurosci 2010, 45:173-179.
26. Lee H.H., Walker J.A., Williams J.R., Goodier R.J., Payne J.A., Moss S.J. Direct protein kinase C-dependent phosphorylation regulates the cell surface stability and activity of the potassium chloride cotransporter KCC2. J Biol Chem 2007, 282:29777-29784.
27. Lu J., Karadsheh M., Delpire E. Developmental regulation of the neuronal-specific isoform of K-Cl cotransporter KCC2 in postnatal rat brains. J Neurobiol 1999, 39:558-568.
28. Moechars D., Depoortere I., Moreaux B., de Smet B., Goris I., Hoskens L., Daneels G., Kass S., Ver Donck L., Peeters T., Coulie B. Altered gastrointestinal and metabolic function in the GPR39-obestatin receptor-knockout mouse. Gastroenterology 2006, 131:1131-1141.
29. Nicoletti F., Bockaert J., Collingridge G.L., Conn P.J., Ferraguti F., Schoepp D.D., Wroblewski J.T., Pin J.P. Metabotropic glutamate receptors: from the workbench to the bedside. Neuropharmacology 2011, 60:1017-1041.
30. + channels. Cell Death Differ 2006, 13:661-667.
31. Paoletti P., Vergnano A.M., Barbour B., Casado M. Zinc at glutamatergic synapses. Neuroscience 2009, 158:126-136.
32. Qian J., Noebels J.L. Visualization of transmitter release with zinc fluorescence detection at the mouse hippocampal mossy fibre synapse. J Physiol 2005, 566:747-758.
33. Qian J., Noebels J.L. 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 2006, 26:6089-6095.
34. Rachline J., Perin-Dureau F., Le Goff A., Neyton J., Paoletti P. The micromolar zinc-binding domain on the NMDA receptor subunit NR2B. J Neurosci 2005, 25:308-317.
35. Rinehart J., Maksimova Y.D., Tanis J.E., Stone K.L., Hodson C.A., Zhang J., Risinger M., Pan W., Wu D., Colangelo C.M., Forbush B., Joiner C.H., Gulcicek E.E., Gallagher P.G., Lifton R.P. Sites of regulated phosphorylation that control K-Cl cotransporter activity. Cell 2009, 138:525-536.
36. - extrusion. J Cell Biol 2002, 159:747-752.
37. Rivera C., Voipio J., Thomas-Crusells J., Li H., Emri Z., Sipila S., Payne J.A., Minichiello L., Saarma M., Kaila K. Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J Neurosci 2004, 24:4683-4691.
38. Santos S., Aizenman E. Functional expression of muscle-type nicotinic acetylcholine receptors in rat forebrain neurons in vitro. Methods Find Exp Clin Pharmacol 2002, 24:63-66.
39. Selak S., Paternain A.V., Aller M.I., Pico E., Rivera R., Lerma J. A role for SNAP25 in internalization of kainate receptors and synaptic plasticity. Neuron 2009, 63:357-371.
40. Sensi S.L., Paoletti P., Bush A.I., Sekler I. Zinc in the physiology and pathology of the CNS. Nat Rev Neurosci 2009, 10:780-791.
41. 2+ ions: modulators of excitatory and inhibitory synaptic activity. Neuroscientist 2004, 10:432-442.
42. Strange K., Singer T.D., Morrison R., Delpire E. Dependence of KCC2 K-Cl cotransporter activity on a conserved carboxy terminus tyrosine residue. Am J Physiol Cell Physiol 2000, 279:C860-C867.
43. Takasaki J., Saito T., Taniguchi M., Kawasaki T., Moritani Y., Hayashi K., Kobori M. A novel Galphaq/11-selective inhibitor. J Biol Chem 2004, 279:47438-47445.
44. Takeda A., Yamada K., Minami A., Nagano T., Oku N. Enhanced excitability of hippocampal mossy fibers and CA3 neurons under dietary zinc deficiency. Epilepsy Res 2005, 63:77-84.
45. Titz S., Hormuzdi S., Lewen A., Monyer H., Misgeld U. Intracellular acidification in neurons induced by ammonium depends on KCC2 function. Eur J Neurosci 2006, 23:454-464.
46. van Dam E.J., Kamal A., Artola A., de Graan P.N., Gispen W.H., Ramakers G.M. Group I metabotropic glutamate receptors regulate the frequency-response function of hippocampal CA1 synapses for the induction of LTP and LTD. Eur J Neurosci 2004, 19:112-118.
47. Viitanen T., Ruusuvuori E., Kaila K., Voipio J. The K+-Cl cotransporter KCC2 promotes GABAergic excitation in the mature rat hippocampus. J Physiol 2010, 588:1527-1540.
48. Vogt K., Mellor J., Tong G., Nicoll R. The actions of synaptically released zinc at hippocampal mossy fiber synapses. Neuron 2000, 26:187-196.
49. Zhang W., Liu L.Y., Xu T.L. Reduced potassium-chloride co-transporter expression in spinal cord dorsal horn neurons contributes to inflammatory pain hypersensitivity in rats. Neuroscience 2008, 152:502-510.
50. Zhu L., Polley N., Mathews G.C., Delpire E. NKCC1 and KCC2 prevent hyperexcitability in the mouse hippocampus. Epilepsy Res 2008, 79:201-212.