Reversed electrogenic sodium bicarbonate cotransporter 1 is the major acid loader during recovery from cytosolic alkalosis in mouse cortical astrocytes

Journal of Physiology

Volumn 593, Issue 16, 2015, Pages 3533-3547

  Theparambil, Shefeeq M ^a   Naoshin, Zinnia ^a   Thyssen, Anne ^a   Deitmer, Joachim W ^a  

^a University of Koblenz Landau   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BICARBONATE; BICARBONATE SODIUM COTRANSPORTER; BUTYRIC ACID; CARBON DIOXIDE; CARBONATE DEHYDRATASE II; CHLORIDE; ELECTROGENIC SODIUM BICARBONATE COTRANSPORTER 1; HYDROGEN; SODIUM; UNCLASSIFIED DRUG; SLC4A4 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL PH; CONTROLLED STUDY; CYTOSOL; CYTOSOLIC ALKALOSIS; EXTRACELLULAR SPACE; HETEROLOGOUS EXPRESSION; MOUSE; NONHUMAN; OOCYTE; POTASSIUM CELL LEVEL; PRIORITY JOURNAL; XENOPUS LAEVIS; ALKALOSIS; ANIMAL; C57BL MOUSE; CELL CULTURE; FEMALE; KNOCKOUT MOUSE; METABOLISM; PH; PHYSIOLOGY;

ALKALOSIS; ANIMALS; ASTROCYTES; BICARBONATES; BUTYRIC ACID; CARBON DIOXIDE; CELLS, CULTURED; CYTOSOL; FEMALE; HYDROGEN-ION CONCENTRATION; MICE, INBRED C57BL; MICE, KNOCKOUT; OOCYTES; SODIUM; SODIUM-BICARBONATE SYMPORTERS; XENOPUS LAEVIS;

EID: 84938966562     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP270086     Document Type: Article

References (65)

1. Becker HM, Bröer S & Deitmer JW (2004). Facilitated lactate transport by MCT1 when coexpressed with the sodium bicarbonate cotransporter (NBC) in Xenopus oocytes. Biophys J 86, 235-247.
2. - cotransporter. J Biol Chem 282, 13508-13521.
3. Becker HM, Klier M & Deitmer JW (2014). Carbonic anhydrase and their interplay with acid/base-coupled membrane transporters. In Carbonic Anhydrase: Mechanism, Regulation, Links to Disease and Industrial Applications, eds. Frost S & Robert McKenna R, Subcell Biochem 75, 105-134.
4. 3 cotransport. J. Gen. Physiol 110, 467-483.
5. - transport. J Gen Physiol 81, 53-94.
6. - exchangers by cAMP-dependent protein kinase in adult rat hippocampal CA1 neurons. J Physiol 545, 837-853.
7. - cotransport. Am J Physiol Cell Physiol 267, C1633-C1640.
8. 3 cotransport in cultured rat cerebellar astrocytes. Pflügers Arch 429, 64-71.
9. Casey JR, Grinstein S & Orlowski J (2009). Sensors and regulators of intracellular pH. Nat Rev Mol Cell Biol 11, 50-61.
10. Ch'en FF, Villafuerte FC, Swietach P, Cobden PM, and Vaughan-Jones RD (2008). S0859, an N-cyanosulphonamide inhibitor of sodium-bicarbonate cotransport in the heart. Br J Pharmacol 153, 972-982.
11. Chesler M & Kraig RP (1987). Intracellular pH of astrocytes increases rapidly with cortical stimulation. Am J Physiol Regul Integr Comp Physiol 253, R666-R670.
12. Chesler M & Kraig RP (1989). Intracellular pH transients of mammalian astrocytes. J Neurosci 9, 2011-2019.
13. Chesler M (2003). Regulation and modulation of pH in the Brain. Physiol Rev 83, 1183-1221.
14. Deitmer JW (1991). Electrogenic sodium-dependent bicarbonate secretion by glial cells of the leech central nervous system. J Gen Physiol 98, 637-655.
15. Deitmer JW (1992). Evidence for glial control of extracellular pH in the leech central nervous system. Glia 5, 43-47.
16. Deitmer JW (2007). Acid-base transport and pH regulation. In Handbook of Neurochemistry and Molecular Neurobiology, Vol.5: Brain Energetics. Integration of Molecular and Cellular Processes, eds Gibson GE & Dienel GA, pp. 469-486. Springer-Verlag Berlin Heidelberg.
17. Deitmer JW & Rose CR (1996). pH regulation and proton signalling by glial cells. Progr Neurobiol 48, 73-103.
18. Deitmer JW & Chesler M (2009). Neuron-glia pH regulation. In New Encyclopedia of Neuroscience, Vol. 6, ed. Squire LR, pp. 739-747. Academic Press, Oxford.
19. Deitmer JW & Rose CR (1996). pH regulation and proton signalling by glial cells. Progr Neurobiol 48, 73-103.
20. Deitmer JW & Schneider H-P (1998). Acid-base transport across the leech giant glial cell membrane at low external bicarbonate concentrations. J Physiol 512.2, 459-469.
21. Deitmer JW & Szatkowski MS (1990). Membrane potential dependence of intracellular pH regulation by identified glial cells in the leech central nervous system. J Physiol 421, 617-631.
22. Deitmer JW & Schlue WR (1989). An inwardly directed, electrogenic sodium-bicarbonate co-transport in glial cells of the leech central nervous system. J Physiol 411, 179-194.
23. 2+ current in mammalina cone photoreceptors. Neuron 32, 1107-1117.
24. Du J, Reznikov LR, Price MP, Zha XM, Lu Y, Moninger TO, Wemmie JA & Welsh MJ (2014). Protons are a neurotransmitter that regulates synaptic plasticity in the lateral amygdala. Proc Natl Acad Sci U S A 111, 8961-8966.
25. Grosche J, Matyash V, Möller T, Verkhratsky A, Reichenbach A & Kettenmann H (1999). Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nat Neurosci 2, 139-143.
26. Halassa MM & Haydon PG (2010). Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu Rev Physiol 72, 335-355.
27. Hassan SF, Cornish JL & Goodchild AK (2013). Respiratory, metabolic and cardiac functions are altered by disinhibition of subregions of the medial prefrontal cortex. J Physiol 591, 6069-6088.
28. Havenga MJ, Bosman GJ, Appelhans H & DeGrip WJ (1994). Expression of the anion exchanger (AE) gene family in human brain. Identification of a new AE protein: AE0. Brain Res Mol Brain Res 25, 97-104.
29. Haydon PG & Carmignoto G (2006). Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86, 1009-1031.
30. - exchanger AE3 display a reduced seizure threshold. Mol Cell Biol 26, 182-191.
31. Heidtmann H, Ruminot I, Becker HM & Deitmer JW (2015). Inhibiton of monocarboxylate transporter by N-cyanosulphonamide S0859. Eur J Pharmacol, doi:10.1016/j.ejphar.2015.
32. Kimelberg HK, Bowman C, Biddlecome S & Bourke RS (1979). Cation transport and membrane potential properties of primary astroglial cultures from neonatal rat brains. Brain Res 177, 533-550.
33. Kobayashi S, Morgans CW, Casey JR & Kopito RR (1994). AE3 anion exchanger isoforms in the vertebrate retina: developmental regulation and differential expression in neurons and glia. J Neurosci. 14, 6266-79.
34. Kofuji P & Newman EA (2004). Potassium buffering in the central nervous system. Neuroscience 129, 1045-1056.
35. Kopito RR, Lee BS, Simmons DM, Lindsey AE, Morgans CW & Schneider K (1989). Regulation of intracellular pH by a neuronal homolog of the erythrocyte anion exchanger. Cell 59, 927-937.
36. Krishtal OA, Osipchuk YV, Shelest TN, Smirnoff SV (1987). Rapid extracellular pH transients related to synaptic transmission in rat hippocampal slices. Brain Res 436, 352-356
37. Leem CH & Vaughan-Jones RD (1997). Chloride-hydroxyl exchange in the guinea-pig ventricular myocyte: no role for bicarbonate. J Mol Cell Cardiol 29, 2483-2489.
38. Leem CH & Vaughan-Jones RD (1998). Sarcolemmal mechanisms for pHi recovery from alkalosis in the guinea-pig ventricular myocyte. J Physiol 509, 487-496.
39. Maren TH (1967). Carbonic anhydrase: chemistry, physiology, and inhibition. Physiol Rev 47, 595-781.
40. McAlear SD & Bevensee MO (2003). pH regulation in non-neuronal brain cells and interstitial fluid. Adv Mol Cell Biol 31, 707-745
41. -containing media. Exp Brain Res 95, 371-380.
42. Miesenbock G, DeAngelis DA & Rothman JE (1998). Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195
43. Munsch T & Deitmer JW (1994). Sodium-bicarbonate cotransport current identified leech glial cells. J Physiol 474, 43-55.
44. Newman EA (1991). Sodium-bicarbonate cotransport in retinal Müller (glial) cells of the salamander. J Neurosci 11, 3972-3983.
45. O'Connor ER, Sontheimer H & Ransom BR (1994). Rat hippocampal astrocytes exhibit electrogenic sodium-bicarbonate co-transport. J Neurophysiol 72, 2580-2589.
46. - exchange function differs in adult and fetal rat hippocampal neurons. Brain Res 614, 308-314.
47. Ransom BR (2000). Glial modulation of neural excitability mediated by extracellular pH: a hypothesis revisited. Prog Brain Res 125, 217-228.
48. -) transporters. Mol Aspects Med. 34, 159-182.
49. Rose CR & Deitmer JW (1994). Evidence that glial cells modulate extracellular pH transients induced by neuronal activity in the leech central nervous system. J Physiol 481.1, 1-5.
50. Rose CR & Deitmer JW (1995a). Stimulus-evoked changes of extra- and intracellular pH in the leech central nervous system. I. Bicarbonate dependence. J Neurophysiol 73, 125-131.
51. Rose CR & Deitmer JW (1995b). Stimulus-evoked changes of extra- and intracellular pH in the leech central nervous system. II. Mechanisms and maintenance of pH homeostasis. J Neurophysiol 73, 132-140.
52. Ruffin VA, Salameh AI, Boron WF & Parker MD (2014). Intracellular pH regulation by acid-base transporters in mammalian neurons. Front Physiol 5, 43.
53. +. J Neurosci 31, 14264-14271.
54. Schüler C, Becker HM, McKenna R & Deitmer JW (2011). Transport activity of the sodium bicarbonate cotransporter NBCe1 is enhanced by different isoforms of carbonic anhydrase. PLoS ONE 6, e27167.
55. - cotransporter, rkNBC, expressed in oocytes. Am J Physiol Renal Physiol 277, F611-F623.
56. Shrode LD & Putnam RW (1994). Intracellular pH regulation in primary rat astrocytes and C6 glioma cells. Glia 12, 196-210.
57. Srivastava J, Barber DL & Jacobson MP (2007). Intracellular pH sensors: design principles and functional significance. Physiology 22, 30-39
58. Stridh M, Alt M, Wittmann S, Heidtmann H, Aggarwal A, Riederer B, Seidler U, Wennemuth G, McKenna R, Deitmer JW & Becker HM (2012). Lactate fluxes in astrocytes enhanced by a non-catalytic action of carbonic anhydrase II. J Physiol 590.10, 2333-2351.
59. Sun B, Leem CH & Vaughan-Jones RD (1996). Novel chloride-dependent acid loader in the guinea-pig ventricular myocyte: part of a dual acid-loading mechanism. J Physiol 495, 65-82.
60. - exchange in hippocampal neurons. J Neurosci 29, 3252-3258.
61. Theodosis DT, Poulain DA & Oliet SH (2008). Activity-dependent structural and functional plasticity of astrocyte-neuron interactions. Physiol Rev 88, 983-1008.
62. + buffering in mouse cortical astrocytes attributable to fast bicarbonate transport. Glia, doi:10.1002/glia.22829 (in epub).
63. Theparambil SM, Ruminot I, Schneider HP, Shull GE & Deitmer JW (2014). The electrogenic sodium-bicarbonate cotransporter NBCe1 is a high-affinity bicarbonate carrier in mouse cortical astrocytes. J Neurosci 34, 1148-1157.
64. Traynelis SF & Cull-Candy SG (1990). Proton inhibition of N-methyl-D-aspartate receptors in cerebellar neurons. Nature 345, 347-350.
65. Walz W & Hertz L (1983). Functional interactions between neurons and astrocytes. II. Potassium homeostasis at the cellular level. Prog Neurobiol 20, 133-183.