Synaptic glutamate release is modulated by the Na+ -Driven Cl-/HCO-3 exchanger Slc4a8

Journal of Neuroscience

Volumn 31, Issue 20, 2011, Pages 7300-7311

  Sinning, Anne ^a   Liebmann, Lutz ^a   Kougioumtzes, Alexandra ^a   Westermann, Martin ^a   Bruehl, Claus ^b   Hübner, Christian A ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; PROTEIN SLC4A8; SODIUM PROTON EXCHANGE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENOTYPE; HIPPOCAMPUS; MOUSE; NERVE CELL; NERVE CELL EXCITABILITY; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; REGULATORY MECHANISM; STEADY STATE; SYNAPTIC TRANSMISSION; SYNAPTOSOME;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; CHLORIDE-BICARBONATE ANTIPORTERS; FEMALE; GLUTAMIC ACID; HYDROGEN-ION CONCENTRATION; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; PATCH-CLAMP TECHNIQUES; SODIUM; SODIUM-BICARBONATE SYMPORTERS; SYNAPSES;

EID: 79956330749     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0269-11.2011     Document Type: Article

References (64)

1. al-Baldawi NF, Abercrombie RF (1992) Cytoplasmic hydrogen ion diffusion coefficient. Biophys J 61:1470-1479.
2. +-independent SLC4 anion exchangers. J Exp Biol 212:1672-1683.
3. Aram JA, Lodge D (1987) Epileptiform activity induced by alkalosis in rat neocortical slices: block by antagonists of N-methyl-D-aspartate. Neurosci Lett 83:345-350.
4. Bai F, Witzmann FA (2007) Synaptosome proteomics. Subcell Biochem 43:77-98.
5. Baxter KA, Church J (1996) Characterization of acid extrusion mechanisms in cultured fetal rat hippocampal neurones. J Physiol 493:457-470.
6. Bevensee MO, Cummins TR, Haddad GG, Boron WF, Boyarsky G (1996) pH regulation in single CA1 neurons acutely isolated from the hippocampi of immature and mature rats. J Physiol 494:315-328.
7. Bonnet U, Leniger T, Wiemann M (2000) Alteration of intracellular pH and activity of CA3-pyramidal cells in guinea pig hippocampal slices by inhibition of transmembrane acid extrusion. Brain Res 872:116-124.
8. 3, and metabolic inhibitors. J Gen Physiol 67:91-112.
9. Boron WF, Chen L, Parker MD (2009) Modular structure of sodiumcoupled bicarbonate transporters. J Exp Biol 212:1697-1706.
10. 3. Am J Physiol 255:C844-C856.
11. Carlin RK, Grab DJ, Cohen RS, Siekevitz P (1980) Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J Cell Biol 86:831-845.
12. Casey JR, Grinstein S, Orlowski J (2010) Sensors and regulators of intracellular pH. Nat Rev Mol Cell Biol 11:50-61.
13. Chen JC, Chesler M (1992) pH transients evoked by excitatory synaptic transmission are increased by inhibition of extracellular carbonic anhydrase. Proc Natl Acad Sci U S A 89:7786-7790.
14. 3 exchanger (SLC4A8) in rodent CNS. Neuroscience 153:162-174.
15. Chesler M (2003) Regulation and modulation of pH in the brain. Physiol Rev 83:1183-1221.
16. Chesler M, Kaila K (1992) Modulation of pH by neuronal activity. Trends Neurosci 15:396-402.
17. Cordat E, Casey JR (2009) Bicarbonate transport in cell physiology and disease. Biochem J 417:423-439.
18. +-dependent anion transporters in selected human tissues. Am J Physiol Regul Integr Comp Physiol 293:R2136-R2146.
19. - export. J Biol Chem 285:26998-27007.
20. A signaling. J Neurosci 30:16044-16052.
21. 2 to cortical excitability via pH. Neuron 48:1011-1023.
22. Eisner DA, Kenning NA, O'Neill SC, Pocock G, Richards CD, Valdeolmillos M (1989) A novel method for absolute calibration of intracellular pH indicators. Pflugers Arch 413:553-558.
23. 2+ entry, and spontaneous transmitter release. Neuron 29:197-208.
24. Feng J, Chi P, Blanpied TA, Xu Y, Magarinos AM, Ferreira A, Takahashi RH, Kao HT, McEwen BS, Ryan TA, Augustine GJ, Greengard P (2002) Regulation of neurotransmitter release by synapsin III. J Neurosci 22:4372-4380.
25. Gaffield MA, Betz WJ (2006) Imaging synaptic vesicle exocytosis and endocytosis with FM dyes. Nat Protoc 1:2916-2921.
26. 3 exchanger. J Biol Chem 276:8358-8363.
27. 3 exchanger AE3 display a reduced seizure threshold. Mol Cell Biol 26:182-191.
28. Hertz L, Dienel GA (2005) Lactate transport and transporters: general principles and functional roles in brain cells. J Neurosci Res 79:11-18.
29. Jacobs S, Ruusuvuori E, Sipilä ST, Haapanen A, Damkier HH, Kurth I, Hentschke M, Schweizer M, Rudhard Y, Laatikainen LM, Tyynelä J, Praetorius J, Voipio J, Hübner CA (2008) Mice with targeted Slc4a10 gene disruption have small brain ventricles and show reduced neuronal excitability. Proc Natl Acad Sci U S A 105:311-316.
30. + exchanger is a major pH regulator in GAB Aergic presynaptic nerve terminals synapsing onto rat CA3 pyramidal neurons. J Neurochem 99:1224-1236.
31. Katz B, Miledi R (1968) The role of calcium in neuromuscular facilitation. J Physiol 195:481-492.
32. 2+-and pH-dependent mechanism in interneurons. J Neurosci 29:11495-11510.
33. Lee J, Taira T, Pihlaja P, Ransom BR, Kaila K (1996) Effects of CO2 on excitatory transmission apparently caused by changes in intracellular pH in the rat hippocampal slice. Brain Res 706:210-216.
34. + reabsorption process in the renal cortical collecting ducts of mice. J Clin Invest 120:1627-1635.
35. Liebmann L, Karst H, Joëls M (2009) Effects of corticosterone and the betaagonist isoproterenol on glutamate receptor-mediated synaptic currents in the rat basolateral amygdala. Eur J Neurosci 30:800-807.
36. +exchange isoform 1 in the central nervous system. Curr Neurovasc Res 4:205-215.
37. Ma J, Fill M, Knudson CM, Campbell KP, Coronado R (1988) Ryanodine receptor of skeletal muscle is a gap junction-type channel. Science 242:99-102.
38. Maycox PR, Deckwerth T, Hell JW, Jahn R (1988) Glutamate uptake by brain synaptic vesicles. Energy dependence of transport and functional reconstitution in proteoliposomes. J Biol Chem 263:15423-15428.
39. Mulkey RM, Zucker RS (1992) Posttetanic potentiation at the crayfish neuromuscular junction is dependent on both intracellular calcium and sodium ion accumulation. J Neurosci 12:4327-4336.
40. Okada Y, Yamazaki H, Sekine-Aizawa Y, Hirokawa N (1995) The neuronspecific kinesin superfamily protein KIF1A is a unique monomeric motor for anterograde axonal transport of synaptic vesicle precursors. Cell 81:769-780.
41. Park HJ, Rajbhandari I, Yang HS, Lee S, Cucoranu D, Cooper DS, Klein JD, Sands JM, Choi I (2010) Neuronal expression of sodium/bicarbonate cotransporter NBC n1 (SLC4A7) and its response to chronic metabolic acidosis. Am J Physiol Cell Physiol 298:C1018-C1028.
42. 2+ exchanger in presynaptic boutons of hippocampal cells in culture. Neuron 15:1077-1084.
43. 2+ in lymphocytes. J Cell Biol 95:189-196.
44. +-driven anion exchanger (NDAE1). A new bicarbonate transporter. J Biol Chem 275:24552-24559.
45. Russell JM, Boron WF (1976) Role of chloride transport in regulation of intracellular pH. Nature 264:73-74.
46. Saggau P, Gray R, Dani JA (1999) Optical measurements of calcium signals in mammalian presynaptic terminals. Methods Enzymol 294:3-19.
47. Schneggenburger R, Neher E (2000) Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406:889-893.
48. Schuchmann S, Schmitz D, Rivera C, Vanhatalo S, Salmen B, Mackie K, Sipilä ST, Voipio J, Kaila K (2006) Experimental febrile seizures are precipitated by a hyperthermia-induced respiratory alkalosis. Nat Med 12:817-823.
49. 3 exchange. J Physiol 475:59-67.
50. Schwiening CJ, Willoughby D (2002) Depolarization-induced pH microdomains and their relationship to calcium transients in isolated snail neurones. J Physiol 538:371-382.
51. Schwiening CJ, Kennedy HJ, Thomas RC (1993) Calcium-hydrogen exchange by the plasma membrane Ca-ATP ase of voltage-clamped snail neurons. Proc Biol Sci 253:285-289.
52. Stewart AK, Boyd CA, Vaughan-Jones RD (1999) A novel role for carbonic anhydrase: cytoplasmic pH gradient dissipation in mouse small intestinal enterocytes. J Physiol 516:209-217.
53. Supuran CT (2008) Carbonic anhydrases-an overview. Curr Pharm Des 14:603-614.
54. 2+ currents in isolated rat CA1 neurons. J Neurophysiol 77:639-653.
55. Tong CK, Chesler M (1999) Activity-evoked extracellular pH shifts in slices of rat dorsal lateral geniculate nucleus. Brain Res 815:373-381.
56. + pump. Neuroreport 7:2000-2004.
57. 2+ release in permeabilized smooth muscle cells of the guinea-pig. J Physiol 475:369-375.
58. Walker CR, Peacock JH (1981) Development of GABA ergic function of dissociated hippocampal cultures from fetal mice. Brain Res 254: 541-555.
59. 3 exchanger. Cloning, tissue distribution, and functional characterization. J Biol Chem 275:35486-35490.
60. Westermann M, Steiniger F, Richter W (2005) Belt-like localisation of caveolin in deep caveolae and its re-distribution after cholesterol depletion. Histochem Cell Biol 123:613-620.
61. Wu LG, Saggau P (1994) Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus. J Neurosci 14:645-654.
62. Xiong ZQ, Saggau P, Stringer JL (2000) Activity-dependent intracellular acidification correlates with the duration of seizure activity. J Neurosci 20:1290-1296.
63. 2+ and glycolysis. Brain Res 780:86-94.
64. Zhang Z, Nguyen KT, Barrett EF, David G (2010) Vesicular ATP ase inserted into the plasma membrane of motor terminals by exocytosis alkalinizes cytosolic pH and facilitates endocytosis. Neuron 68:1097-1108.