Na+/H+ exchanger inhibition modifies dopamine neurotransmission during normal and metabolic stress conditions

Journal of Neurochemistry

Volumn 106, Issue 1, 2008, Pages 231-243

  Rocha, Marcelo A ^a   Crockett, David P ^a   Wong, Lai Yoong ^a   Richardson, Jason R ^a   Sonsalla, Patricia K ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Cariporide; Dopamine; Microdialysis; Na+ H+ exchanger; Neurotransmission; Striatum

Indexed keywords

CARIPORIDE; DOPAMINE; MALONIC ACID; SODIUM PROTON EXCHANGE PROTEIN; SODIUM PROTON EXCHANGE PROTEIN 1; SODIUM PROTON EXCHANGE PROTEIN 2; SODIUM PROTON EXCHANGE PROTEIN 3; SODIUM PROTON EXCHANGE PROTEIN 4; SODIUM PROTON EXCHANGE PROTEIN 5;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; DOPAMINERGIC TRANSMISSION; IN VIVO STUDY; INHIBITION KINETICS; MALE; MESENCEPHALON; METABOLIC STRESS; MICRODIALYSIS; MOUSE; NERVE FIBER; NEUROTRANSMISSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUBSTANTIA NIGRA;

ANIMALS; ANTI-ARRHYTHMIA AGENTS; BRAIN DISEASES, METABOLIC; CATION TRANSPORT PROTEINS; CORPUS STRIATUM; DOPAMINE; ENERGY METABOLISM; GUANIDINES; MALE; MALONATES; MICE; MITOCHONDRIA; MITOCHONDRIAL DISEASES; OXIDATIVE STRESS; PRESYNAPTIC TERMINALS; PROTEIN ISOFORMS; SODIUM-HYDROGEN ANTIPORTER; SUBSTANTIA NIGRA; SULFONES; SYNAPTIC TRANSMISSION; WALLERIAN DEGENERATION;

MUS;

EID: 45249111182     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05355.x     Document Type: Article

References (79)

1. Albers D. S., Zeevalk G. D. Sonsalla P. K. (1996) Damage to dopaminergic nerve terminals in mice by combined treatment of intrastriatal malonate with systemic methamphetamine or MPTP. Brain Res. 718, 217 220.
2. Alfinito P. D., Wang S. P., Manzino L., Rijhsinghani S., Zeevalk G. D. Sonsalla P. K. (2003) Adenosinergic protection of dopaminergic and GABAergic neurons against mitochondrial inhibition through receptors located in the substantia nigra and striatum, respectively. J. Neurosci. 23, 10982 10987.
3. + antiporter in insulin-induced endogenous dopamine release from tuberoinfundibular neurons. Life Sci. 46, 885 894.
4. Andersson D. R., Nissbrandt H. Bergquist F. (2006) Partial depletion of dopamine in substantia nigra impairs motor performance without altering striatal dopamine neurotransmission. Eur. J. Neurosci. 24, 617 624.
5. + exchanger (NHE5) highly expressed in brain. J. Biol. Chem. 274, 4383 4388 ().
6. + exchanger isoform 5 (NHE5) from human brain. J. Biol. Chem. 274, 4377 4382.
7. Burrows K. B., Nixdorf W. L. Yamamoto B. K. (2000) Central administration of methamphetamine synergizes with metabolic inhibition to deplete striatal monoamines. J. Pharmacol. Exp. Ther. 292, 853 860.
8. Buyukuysal R. L. Mete B. (1999) Anoxia-induced dopamine release from rat striatal slices: involvement of reverse transport mechanism. J. Neurochem. 72, 1507 1515.
9. Callahan B. T., Cord B. J., Yuan J., McCann U. D. Ricaurte G. A. (2001) Inhibitors of Na(+)/H(+) and Na(+)/Ca(2+) exchange potentiate methamphetamine-induced dopamine neurotoxicity: possible role of ionic dysregulation in methamphetamine neurotoxicity. J. Neurochem. 77, 1348 1362.
10. Camacho M., Machado J. D., Montesinos M. S., Criado M. Borges R. (2006) Intragranular pH rapidly modulates exocytosis in adrenal chromaffin cells. J. Neurochem. 96, 324 334.
11. + accumulation in rat hypothalamic synaptosomes: involvement of calcium ions. Neurochem. Int. 43, 9 17.
12. + exchange inhibition prior to 90 minutes of hypothermic circulatory arrest. Ann. Thorac. Surg. 79, 646 654.
13. Chesler M. (2003) Regulation and modulation of pH in the brain. Physiol. Rev. 83, 1183 1221.
14. Chesler M. Kraig R. P. (1989) Intracellular pH transients of mammalian astrocytes. J. Neurosci. 9, 2011 2019.
15. Colzi A., D'Agostini F., Cesura A., Borroni E. Da Prada M. (1993) Monoamine oxidase-A inhibitors and dopamine metabolism in rat caudatus: evidence that an increased cytosolic level of dopamine displaces reversible monoamine oxidase-A inhibitors in vivo. J. Pharmacol. Exp. Ther. 265, 103 111.
16. + exchanger NHE-1 possesses N- and O-linked glycosylation restricted to the first N-terminal extracellular domain. Biochemistry 33, 10463 10469.
17. + exchanger in A6 cells. Am. J. Physiol. 271, C1639 C1645.
18. Douglas R. M., Schmitt B. M., Xia Y., Bevensee M. O., Biemesderfer D., Boron W. F. Haddad G. G. (2001) Sodium-hydrogen exchangers and sodium-bicarbonate co-transporters: ontogeny of protein expression in the rat brain. Neuroscience 102, 217 228.
19. Drapeau P. Nachshen D. A. (1988) Effects of lowering extracellular and cytosolic pH on calcium fluxes, cytosolic calcium levels, and transmitter release in presynaptic nerve terminals isolated from rat brain. J. Gen. Physiol. 91, 305 315.
20. Ferger B., Eberhardt O., Teismann P., de Groote C. Schulz J. B. (1999) Malonate-induced generation of reactive oxygen species in rat striatum depends on dopamine release but not on NMDA receptor activation. J. Neurochem. 73, 1329 1332.
21. Globus M. Y., Ginsberg M. D., Dietrich W. D., Busto R. Scheinberg P. (1987) Substantia nigra lesion protects against ischemic damage in the striatum. Neurosci. Lett. 80, 251 256.
22. Grichtchenko I. I. Chesler M. (1994) Depolarization-induced acid secretion in gliotic hippocampal slices. Neuroscience 62, 1057 1070.
23. Haas R. H., Nasirian F., Nakano K., Ward D., Pay M., Hill R. Shults C. W. (1995) Low platelet mitochondrial complex I and complex II/III activity in early untreated Parkinson's disease. Ann. Neurol. 37, 714 722.
24. Hastings T. G., Lewis D. A. Zigmond M. J. (1996) Role of oxidation in the neurotoxic effects of intrastriatal dopamine injections. Proc. Natl Acad. Sci. USA 93, 1956 1961.
25. Hogan K. A., Staal R. G. Sonsalla P. K. (2000) Analysis of VMAT2 binding after methamphetamine or MPTP treatment: disparity between homogenates and vesicle preparations. J. Neurochem. 74, 2217 2220.
26. + exchanger is a major pH regulator in GABAergic presynaptic nerve terminals synapsing onto rat CA3 pyramidal neurons. J. Neurochem. 99, 1224 1236.
27. + exchange system in rat brain synaptosomes. Interdependence of internal and external pH control of the exchange activity. J. Biol. Chem. 260, 9678 9684.
28. Johnson R. G., Carty S. Scarpa A. (1982) A model of biogenic amine accumulation into chromaffin granules and ghosts based on coupling to the electrochemical proton gradient. Fed. Proc. 41, 2746 2754.
29. Kang J., Jiang L., Goldman S. A. Nedergaard M. (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat. Neurosci. 1, 683 692.
30. Kilty J. E., Lorang D. Amara S. G. (1991) Cloning and expression of a cocaine-sensitive rat dopamine transporter. Science 254, 578 579.
31. + production in primary astroglial cultures. Brain Res. 173, 111 124.
32. Kumar A. P., Chang M. K., Fliegel L., Pervaiz S. Clement M. V. (2007) Oxidative repression of NHE1 gene expression involves iron-mediated caspase activity. Cell Death Differ. 14, 1733 1746.
33. + exchanger family, regulates osteoclast differentiation and survival. Biochem. Biophys. Res. Commun. 369, 320 326.
34. Lindefors N., Amberg G. Ungerstedt U. (1989) Intracerebral microdialysis: I. Experimental studies of diffusion kinetics. J. Pharmacol. Methods 22, 141 156.
35. + exchanger isoform 1-null mice after in vitro and in vivo ischemia. J. Neurosci. 25, 11256 11268.
36. + exchangers in rat central nervous system. Neuroscience 79, 591 603.
37. Makani S. Chesler M. (2007) Endogenous alkaline transients boost postsynaptic NMDA receptor responses in hippocampal CA1 pyramidal neurons. J. Neurosci. 27, 7438 7446.
38. McSwine R. L., Babnigg G., Musch M. W., Chang E. B. Villereal M. L. (1994) Expression and phosphorylation of NHE1 in wild-type and transformed human and rodent fibroblasts. J. Cell. Physiol. 161, 351 357.
39. Moy L. Y., Zeevalk G. D. Sonsalla P. K. (2000) Role for dopamine in malonate-induced damage in vivo in striatum and in vitro in mesencephalic cultures. J. Neurochem. 74, 1656 1665.
40. Moy L. Y., Wang S. P. Sonsalla P. K. (2007) Mitochondrial stress-induced dopamine efflux and neuronal damage by malonate involves the dopamine transporter. J. Pharmacol. Exp. Ther. 320, 747 756.
41. + exchange and increases excitability of solitary complex neurons from rat brain slices. Am. J. Physiol. Cell Physiol. 286, C940 C951.
42. Nachshen D. A. Drapeau P. (1988) The regulation of cytosolic pH in isolated presynaptic nerve terminals from rat brain. J. Gen. Physiol. 91, 289 303.
43. + exchanger isoforms are distributed to Golgi and post-Golgi compartments and are involved in organelle pH regulation. J. Biol. Chem. 280, 1561 1572.
44. Newman E. (1996) Acid efflux from retinal glial cells generated by sodium bicarbonate cotransport. J. Neurosci. 16, 159 168.
45. Nicholson C. Rice M. E. (1986) The migration of substances in the neuronal microenvironment. Ann. NY Acad. Sci. 481, 55 71.
46. Nicklas W. J. Browning E. T. (1978) Amino acid metabolism in glial cells: homeostatic regulation of intra- and extracellular milieu by C-6 glioma cells. J. Neurochem. 30, 955 963.
47. Nixdorf W. L., Burrows K. B., Gudelsky G. A. Yamamoto B. K. (2001) Enhancement of 3,4-methylenedioxymethamphetamine neurotoxicity by the energy inhibitor malonate. J. Neurochem. 77, 647 654.
48. Orlowski J. Grinstein S. (2004) Diversity of the mammalian sodium/proton exchanger SLC9 gene family. Pflugers Arch. 447, 549 565.
49. Parker W. D. Jr, Boyson S. J. Parks J. K. (1989) Abnormalities of the electron transport chain in idiopathic Parkinson's disease. Ann. Neurol. 26, 719 723.
50. Pasternack M., Smirnov S. Kaila K. (1996) Proton modulation of functionally distinct GABAA receptors in acutely isolated pyramidal neurons of rat hippocampus. Neuropharmacology 35, 1279 1288.
51. Pedersen S. F., King S. A., Rigor R. R., Zhuang Z., Warren J. M. Cala P. M. (2003) Molecular cloning of NHE1 from winter flounder RBCs: activation by osmotic shrinkage, cAMP, and calyculin A. Am. J. Physiol. Cell Physiol. 284, C1561 C1576.
52. - cotransport in the heart, brain, and blood. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291, R1 R25.
53. Phillis J. W., Estevez A. Y., Guyot L. L. O'Regan M. H. (1999) 5-(N-Ethyl-N-isopropyl)-amiloride, an Na(+)-H(+) exchange inhibitor, protects gerbil hippocampal neurons from ischemic injury. Brain Res. 839, 199 202.
54. + exchange activity in cultured rat hippocampal astrocytes. J. Neurosci. Res. 44, 191 198.
55. Pothos E. N. (2002) Regulation of dopamine quantal size in midbrain and hippocampal neurons. Behav. Brain Res. 130, 203 207.
56. Pothos E. N., Larsen K. E., Krantz D. E., Liu Y., Haycock J. W., Setlik W., Gershon M. D., Edwards R. H. Sulzer D. (2000) Synaptic vesicle transporter expression regulates vesicle phenotype and quantal size. J. Neurosci. 20, 7297 7306.
57. Praetorius J. Nielsen S. (2006) Distribution of sodium transporters and aquaporin-1 in the human choroid plexus. Am. J. Physiol. Cell Physiol. 291, 59 67.
58. Prod'hom B., Pietrobon D. Hess P. (1989) Interactions of protons with single open L-type calcium channels. Location of protonation site and dependence of proton-induced current fluctuations on concentration and species of permeant ion. J. Gen. Physiol. 94, 23 42.
59. +-induced efflux of dopamine and lactate from rat striatum have similar time courses as shown by in vivo brain dialysis. J. Pharmacol. Exp. Ther. 245, 858 866.
60. Rothstein J. D., Dykes-Hoberg M., Pardo C. A. et al. (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16, 675 686.
61. Sandoval V., Riddle E. L., Hanson G. R. Fleckenstein A. E. (2002) Methylphenidate redistributes vesicular monoamine transporter-2: role of dopamine receptors. J. Neurosci. 22, 8705 8710.
62. Santos M. S., Moreno A. J. Carvalho A. P. (1996) Relationships between ATP depletion, membrane potential, and the release of neurotransmitters in rat nerve terminals. An in vitro study under conditions that mimic anoxia, hypoglycemia, and ischemia. Stroke 27, 941 950.
63. + exchange system in brain synaptosomes. Brain Res. 301, 371 374.
64. Scholz W., Albus U., Counillon L., Gogelein H., Lang H. J., Linz W., Weichert A. Scholkens B. A. (1995) Protective effects of HOE642, a selective sodium-hydrogen exchange subtype 1 inhibitor, on cardiac ischaemia and reperfusion. Cardiovasc. Res. 29, 260 268.
65. Shrode L. D. Putnam R. W. (1994) Intracellular pH regulation in primary rat astrocytes and C6 glioma cells. Glia 12, 196 210.
66. Staal R. G. Sonsalla P. K. (2000) Inhibition of brain vesicular monoamine transporter (VMAT2) enhances 1-methyl-4-phenylpyridinium neurotoxicity in vivo in rat striata. J. Pharmacol. Exp. Ther. 293, 336 342.
67. + exchanger isoform 5 stably expressed in Chinese hamster ovary cells. J. Biol. Chem. 275, 6302 6307.
68. + exchanger NHE5 isoform: regulation by phosphatidylinositol 3′-kinase and the actin cytoskeleton. J. Biol. Chem. 277, 42623 42632.
69. Takahashi K., Dixon D. B. Copenhagen D. R. (1993) Modulation of a sustained calcium current by intracellular pH in horizontal cells of fish retina. J. Gen. Physiol. 101, 695 714.
70. +. Proc. Natl Acad. Sci. USA 87, 6445 6449.
71. Tolliver B. K., Newman A. H., Katz J. L., Ho L. B., Fox L. M., Hsu K. Jr Berger S. P. (1999) Behavioral and neurochemical effects of the dopamine transporter ligand 4-chlorobenztropine alone and in combination with cocaine in vivo. J. Pharmacol. Exp. Ther. 289, 110 122.
72. Trudeau L.-E., Parpura V. Haydon P. G. (1999) Activation of neurotransmitter release in hippocampal nerve terminals during recovery from intracellular acidification. J. Neurophysiol. 81, 2627 2635.
73. Vornov J. J., Thomas A. G. Jo D. (1996) Protective effects of extracellular acidosis and blockade of sodium/hydrogen ion exchange during recovery from metabolic inhibition in neuronal tissue culture. J. Neurochem. 67, 2379 2389.
74. Westerink B. H. De Vries J. B. (2001) A method to evaluate the diffusion rate of drugs from a microdialysis probe through brain tissue. J. Neurosci. Methods 109, 53 58.
75. Xia X. G., Schmidt N., Teismann P., Ferger B. Schulz J. B. (2001) Dopamine mediates striatal malonate toxicity via dopamine transporter-dependent generation of reactive oxygen species and D2 but not D1 receptor activation. J. Neurochem. 79, 63 70.
76. +/H+ exchanger isoform 1 null mutant mouse brain. Neuroscience 122, 37 46.
77. Yao H., Ma E., Gu X. Q. Haddad G. G. (1999) Intracellular pH regulation of CA1 neurons in Na(+)/H(+) isoform 1 mutant mice. J. Clin. Invest. 104, 637 645.
78. Zeevalk G. D., Manzino L., Hoppe J. Sonsalla P. (1997) In vivo vulnerability of dopamine neurons to inhibition of energy metabolism. Eur. J. Pharmacol. 320, 111 119.
79. Zubieta J. K., Cragoe E. J. Jr Cubeddu L. X. (1988) Effects of amiloride and 5-(N,N-hexamethylene)amiloride on dopaminergic and cholinergic neurotransmission. J. Pharmacol. Exp. Ther. 247, 88 95.