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Pharmacology of Neurotransmitter Transport into Secretory Vesicles

  • Farrukh A. Chaudhry
  • Jean-Luc Boulland
  • Monica Jenstad
  • May K. L. Bredahl
  • Robert H. Edwards
Part of the Handbook of Experimental Pharmacology book series (HEP, volume 184)

Many neuropsychiatric disorders appear to involve a disturbance of chemical neurotransmission, and the mechanism of available therapeutic agents supports this impression. Postsynaptic receptors have received considerable attention as drug targets, but some of the most successful agents influence presynaptic processes, in particular neurotransmitter reuptake. The pharmacological potential of many other presynaptic elements, and in particular the machinery responsible for loading transmitter into vesicles, has received only limited attention. The similarity of vesicular transporters to bacterial drug resistance proteins and the increasing evidence for regulation of vesicle filling and recycling suggest that the pharmacological potential of vesicular transporters has been underestimated. In this review, we discuss the pharmacological effects of psychostimulants and therapeutic agents on transmitter release.

Keywords

Synaptic Vesicle Secretory Vesicle Glutamate Uptake Evans Blue Vesicular Monoamine Transporter 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Accardi A, Kolmakova-Partensky L, Williams C, Miller C (2004) Ionic currents mediated by a prokaryotic homologue of CLC Cl-channels. J Gen Physiol 123:109-19.PubMedCrossRefGoogle Scholar
  2. Adamson CR, Emley TE, Herbig LJ, Near JA (1997) Effects of nerve growth factor on dihydrotetrabenazine binding to PC12 cells. Neurochem Int 30:411-15.PubMedCrossRefGoogle Scholar
  3. Alfonso A, Grundahl K, Duerr JS, Han HP, Rand JB (1993) The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter. Science 261:617-19.PubMedCrossRefGoogle Scholar
  4. Anderson DC, King SC, Parsons SM (1981) Uncoupling of acetylcholine uptake from the Torpedo cholinergic synaptic vesicle ATPase. Biochem Biophys Res Commun 103:422-8.PubMedCrossRefGoogle Scholar
  5. Anderson DC, King SC, Parsons SM (1983) Pharmacological characterization of the acetylcholine transport system in purified Torpedo electric organ synaptic vesicles. Mol Pharmacol 24:48-54.PubMedGoogle Scholar
  6. Anderson KJ, Monaghan DT, Cangro CB, Namboodiri MAA, Neale JH, Cotman CW (1986) Localization of N-acetylaspartylglutamate-like immunoreactivity in selected areas of the rat brain. Neurosci Lett 72:14-20.PubMedCrossRefGoogle Scholar
  7. Bahr BA, Clarkson ED, Rogers GA, Noremberg K, Parsons SM (1992) A kinetic and allosteric model for the acetylcholine transporter-vesamicol receptor in synaptic vesicles. Biochemistry 31:5752-5762.PubMedCrossRefGoogle Scholar
  8. Bahr BA, Parsons SM (1986) Demonstration of a receptor in Torpedo synaptic vesicles for the acetylcholine storage blocker L-trans-2-(4-phenyl[3,4-3H]-piperidino)cyclohexanol. Proc Natl Acad Sci USA 83:2267-2270.PubMedCrossRefGoogle Scholar
  9. Bajjalieh SM, Frantz GD, Weimann JM, McConnell SK, Scheller RH (1994) Differential expression of synaptic vesicle protein 2 (SV2) isoforms. J Neurosci 14:5223-5235.PubMedGoogle Scholar
  10. Bajjalieh SM, Peterson K, Linial M, Scheller RH (1993) Brain contains two forms of synaptic vesicle protein 2. Proc Natl Acad Sci USA 90:2150-2154.PubMedCrossRefGoogle Scholar
  11. Bajjalieh SM, Peterson K, Shinghal R, Scheller RH (1992) SV2, a brain synaptic vesicle protein homologous to bacterial transporters. Science 257:1271-1273.PubMedCrossRefGoogle Scholar
  12. Bak LK, Schousboe A, Waagepetersen HS (2006) The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer. J Neurochem 98:641-653.PubMedCrossRefGoogle Scholar
  13. Beers MH, Passman LJ (1990) Antihypertensive medications and depression. Drugs 40:792-799.PubMedCrossRefGoogle Scholar
  14. Bellocchio EE, Reimer RJ, Fremeau RT, Jr., Edwards RH (2000) Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter [see comments]. Science 289:957-960.PubMedCrossRefGoogle Scholar
  15. Beyenbach KW, Wieczorek H (2006) The V-type H+ ATPase: molecular structure and function, physiological roles and regulation. J Exp Biol 209:577-589.PubMedCrossRefGoogle Scholar
  16. Bezzi P, Gundersen V, Galbete JL, Seifert G, Steinhauser C, Pilati E, Volterra A (2004) Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat Neurosci 7:613-620.PubMedCrossRefGoogle Scholar
  17. Bole DG, Ueda T (2005) Inhibition of vesicular glutamate uptake by Rose Bengal-related compounds: structure-activity relationship. Neurochem Res 30:363-369.PubMedCrossRefGoogle Scholar
  18. Boulland JL, Qureshi T, Seal RP, Rafiki A, Gundersen V, Bergersen LH, Fremeau RT, Jr., Edwards RH, Storm-Mathisen J, Chaudhry FA (2004) Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. J Comp Neurol 480:264-280.PubMedCrossRefGoogle Scholar
  19. Bowman EJ, Graham LA, Stevens TH, Bowman BJ (2004) The bafilomycin/concanamycin binding site in subunit c of the V-ATPases from Neurospora crassa and Saccharomyces cerevisiae. J Biol Chem 279:33131-33138.PubMedCrossRefGoogle Scholar
  20. Bravo DT, Kolmakova NG, Parsons SM (2005) New transport assay demonstrates vesicular acetylcholine transporter has many alternative substrates. Neurochem Int 47:243-247.PubMedCrossRefGoogle Scholar
  21. Bravo DT, Kolmakova NG, Parsons SM (2004) Transmembrane reorientation of the substratebinding site in vesicular acetylcholine transporter. Biochemistry 43:8787-8793.PubMedCrossRefGoogle Scholar
  22. Bridges RJ, Kavanaugh MP, Chamberlin AR (1999) A pharmacologicalal review of competitive inhibitors and substrates of high-affinity, sodium-dependent glutamate transport in the central nervous system. Curr Pharm Des 5:363-379.PubMedGoogle Scholar
  23. Broer S, Schuster A, Wagner CA, Broer A, Forster I, Biber J, Murer H, Werner A, Lang F, Busch AE (1998) Chloride conductance and Pi transport are separate functions induced by the expression of NaPi-1 in Xenopus oocytes. J Membr Biol 164:71-77.PubMedCrossRefGoogle Scholar
  24. Brown JM, Hanson GR, Fleckenstein AE (2001) Regulation of the vesicular monoamine transporter-2: a novel mechanism for cocaine and other psychostimulants. J Pharmacol Exp Ther 296:762-767.PubMedGoogle Scholar
  25. Buchanan RW, Breier A, Kirkpatrick B, Ball P, Carpenter WT, Jr. (1998) Positive and negative symptom response to clozapine in schizophrenic patients with and without the deficit syndrome. Am J Psychiatry 155:751-760.PubMedGoogle Scholar
  26. Buckley K, Kelly RB (1985) Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J Cell Biol 100:1284-1294.PubMedCrossRefGoogle Scholar
  27. Buckley PF (1999) New antipsychotic agents: emerging clinical profiles. J Clin Psychiatry 60 Suppl 1:12-17.Google Scholar
  28. Burger PM, Hell J, Mehl E, Krasel C, Lottspeich F, Jahn R (1991) GABA and glycine in synaptic vesicles: storage and transport characteristics. Neuron 7:287-293.PubMedCrossRefGoogle Scholar
  29. Busch AE, Schuster A, Waldegger S, Wagner CA, Zempel G, Broer S, Biber J, Murer H, Lang F (1996) Expression of a renal type I sodium/phosphate transporter (NaPi-1) induces a conductance in Xenopus oocytes permeable for organic and inorganic anions. Proc Natl Acad Sci USA 93:5347-5351.PubMedCrossRefGoogle Scholar
  30. Carlson MD, Kish PE, Ueda T (1989) Characterization of the solubilized and reconstituted ATPdependent vesicular glutamate uptake system. J Biol Chem 264:7369-7376.PubMedGoogle Scholar
  31. Carlson MD, Ueda T (1990) Accumulated glutamate levels in the synaptic vesicle are not maintained in the absence of active transport. Neurosci Lett 110:325-330.PubMedCrossRefGoogle Scholar
  32. Carlsson A, Dahlstroem A, Fuxe K, Hillarp NA (1965) Failure of reserpine to deplete noradrenaline neurons of alpha-methylnoradrenaline formed from alpha-methyl dopa. Acta Pharmacol Toxicol (Copenh) 22:270-276.Google Scholar
  33. Carrigan CN, Bartlett RD, Esslinger CS, Cybulski KA, Tongcharoensirikul P, Bridges RJ, Thompson CM (2002) Synthesis and in vitro pharmacology of substituted quinoline-2,4-dicarboxylic acids as inhibitors of vesicular glutamate transport. J Med Chem 45:2260-2276.PubMedCrossRefGoogle Scholar
  34. Carrigan CN, Esslinger CS, Bartlett RD, Bridges RJ, Thompson CM (1999) Quinoline-2,4-dicarboxylic acids: synthesis and evaluation as inhibitors of the glutamate vesicular transport system. Bioorg Med Chem Lett 9:2607-2612.PubMedCrossRefGoogle Scholar
  35. Chaplin L, Cohen AH, Huettl P, Kennedy M, Njus D, Temperley SJ (1985) Reserpic acid as an inhibitor of norepinephrine transport into chromaffin vesicle ghosts. J Biol Chem 260:10981-10985.PubMedGoogle Scholar
  36. Chaudhry FA, Reimer RJ, Bellocchio EE, Danbolt NC, Osen KK, Edwards RH, Storm-Mathisen J (1998) The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycingergic as well as GABAergic neurons. J Neurosci 18:9733-9750.PubMedGoogle Scholar
  37. Chaudhry FA, Reimer RJ, Edwards RH (2002) The glutamine commute: take the N line and transfer to the A. J Cell Biol 157:349-355.PubMedCrossRefGoogle Scholar
  38. Chaudhry FA, Edwards RH, Fonnum F (2008) Vesicular neurotransmitter transporters as targets for endogenous and exogenous toxic substances. Annu Rev Pharmacol Toxicol, 48 [sep 20 Epub ahead of print]Google Scholar
  39. Christensen H, Fonnum F (1991) Uptake of glycine, GABA and glutamate by synaptic vesicles isolated from different regions of rat CNS. Neurosci Lett.Google Scholar
  40. Christensen H, Fykse EM, Fonnum F (1990) Uptake of glycine into synaptic vesicles isolated from rat spinal cord. J Neurochem 54:1142-1147.PubMedCrossRefGoogle Scholar
  41. Clarkson ED, Rogers GA, Parsons SM (1992) Binding and active transport of large analogues of acetylcholine by cholinergic synaptic vesicles in vitro. J Neurochem 59:695-700.PubMedCrossRefGoogle Scholar
  42. Crosby MJ, Hanson JE, Fleckenstein AE, Hanson GR (2002) Phencyclidine increases vesicular dopamine uptake. Eur J Pharmacol 438:75-78.PubMedCrossRefGoogle Scholar
  43. Crowder KM, Gunther JM, Jones TA, Hale BD, Zhang HZ, Peterson MR, Scheller RH, Chavkin C, Bajjalieh SM (1999) Abnormal neurotransmission in mice lacking synaptic vesicle protein 2A (SV2A). Proc Natl Acad Sci USA 96:15268-15273.PubMedCrossRefGoogle Scholar
  44. Crump FT, Fremeau RT, Craig AM (1999) Localization of the brain-specific high-affinity l-proline transporter in cultured hippocampal neurons: molecular heterogeneity of synaptic terminals. Mol Cell Neurosci 13:25-39.PubMedCrossRefGoogle Scholar
  45. Custer KL, Austin NS, Sullivan JM, Bajjalieh SM (2006) Synaptic vesicle protein 2 enhances release probability at quiescent synapses. J Neurosci 26:1303-1313.PubMedCrossRefGoogle Scholar
  46. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1-105.PubMedCrossRefGoogle Scholar
  47. Darchen F, Scherman D, Henry JP (1989) Reserpine binding to chromaffin granules suggests the existence of two conformations of the monoamine transporter. Biochemistry 28:1692-1697.PubMedCrossRefGoogle Scholar
  48. Dong M, Yeh F, Tepp WH, Dean C, Johnson EA, Janz R, Chapman ER (2006) SV2 is the protein receptor for botulinum neurotoxin A. Science 312:592-596.PubMedCrossRefGoogle Scholar
  49. Dwoskin LP, Crooks PA (2002) A novel mechanism of action and potential use for lobeline as a treatment for psychostimulant abuse. Biochem Pharmacol 63:89-98.PubMedCrossRefGoogle Scholar
  50. Erickson JD, De GS, Varoqui H, Schafer MK, Weihe E (2006) Activity-dependent regulation of vesicular glutamate and GABA transporters: a means to scale quantal size. Neurochem Int 48:643-649.PubMedGoogle Scholar
  51. Erickson JD, Eiden LE, Hoffman BJ (1992) Expression cloning of a reserpine-sensitive vesicular monoamine transporter. Proc Natl Acad Sci USA 89:10993-10997.PubMedCrossRefGoogle Scholar
  52. Erickson JD, Schafer MK, Bonner TI, Eiden LE, Weihe E (1996) Distinct pharmacologicalal properties and distribution in neurons and endocrine cells of two isoforms of the human vesicular monoamine transporter. Proc Natl Acad Sci USA 93:5166-5171.PubMedCrossRefGoogle Scholar
  53. Erickson JD, Varoqui H, Schafer MK, Modi W, Diebler MF, Weihe E, Rand J, Eiden LE, Bonner TI, Usdin TB (1994) Functional identification of a vesicular acetylcholine transporter and its expression from a “cholinergic” gene locus. J Biol Chem 269:21929-21932.PubMedGoogle Scholar
  54. Feany MB, Lee S, Edwards RH, Buckley KM (1992) The synaptic vesicle protein SV2 is a novel type of transmembrane transporter. Cell 70:861-867.PubMedCrossRefGoogle Scholar
  55. Ferguson SM, Blakely RD (2004) The choline transporter resurfaces: new roles for synaptic vesicles? Mol Interv 4:22-37.PubMedCrossRefGoogle Scholar
  56. Ferguson SM, Savchenko V, Apparsundaram S, Zwick M, Wright J, Heilman CJ, Yi H, Levey AI, Blakely RD (2003) Vesicular localization and activity-dependent trafficking of presynaptic choline transporters. J Neurosci 23:9697-9709.PubMedGoogle Scholar
  57. Fischer JF, Cho AK (1979) Chemical release of dopamine from striatal homogenates: evidence for an exchange diffusion model. J Pharmacol Exp Ther 208:203-209.PubMedGoogle Scholar
  58. Fog JU, Khoshbouei H, Holy M, Owens WA, Vaegter CB, Sen N, Nikandrova Y, Bowton E, McMahon DG, Colbran RJ, Daws LC, Sitte HH, Javitch JA, Galli A, Gether U (2006) Calmodulin kinase II interacts with the dopamine transporter C terminus to regulate amphetamineinduced reverse transport. Neuron 51:417-429.PubMedCrossRefGoogle Scholar
  59. Fon EA, Pothos EN, Sun BC, Killeen N, Sulzer D, Edwards RH (1997) Vesicular transport regulates monoamine storage and release but is not essential for amphetamine action. Neuron 19:1271-1283.PubMedCrossRefGoogle Scholar
  60. Forgac M (1989) Structure and function of vacuolar class of ATP-driven proton pumps. Physiol Rev 69:765-796.PubMedGoogle Scholar
  61. Fremeau RT, Jr., Burman J, Qureshi T, Tran CH, Proctor J, Johnson J, Zhang H, Sulzer D, Copenhagen DR, Storm-Mathisen J, Reimer RJ, Chaudhry FA, Edwards RH (2002) The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc Natl Acad Sci USA 99:14488-14493.PubMedCrossRefGoogle Scholar
  62. Fremeau RT, Jr., Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247-260.PubMedCrossRefGoogle Scholar
  63. Fykse EM, Iversen EG, Fonnum F (1992) Inhibition of L-glutamate uptake into synaptic vesicles. Neurosci Lett 135:125-128.PubMedCrossRefGoogle Scholar
  64. Gomeza J, Ohno K, Hulsmann S, Armsen W, Eulenburg V, Richter DW, Laube B, Betz H (2003) Deletion of the mouse glycine transporter 2 results in a hyperekplexia phenotype and postnatal lethality. Neuron 40:797-806.PubMedCrossRefGoogle Scholar
  65. Gonzalez AM, Walther D, Pazos A, Uhl GR (1994) Synaptic vesicular monoamine transporter expression: distribution and pharmacological profile. Brain Res Mol Brain Res 22:219-226.PubMedCrossRefGoogle Scholar
  66. Gottschalk KE, Soskine M, Schuldiner S, Kessler H (2004) A structural model of EmrE, a multi-drug transporter from Escherichia coli. Biophys J 86:3335-3348.PubMedCrossRefGoogle Scholar
  67. Gras C, Herzog E, Bellenchi GC, Bernard V, Ravassard P, Pohl M, Gasnier B, Giros B, El Mestikawy S (2002) A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J Neurosci 22:5442-5451.PubMedGoogle Scholar
  68. Haikerwal D, Dart AM, Little PJ, Kaye DM (1999) Identification of a novel, inhibitory action of amiodarone on vesicular monoamine transport. J Pharmacol Exp Ther 288:834-837.PubMedGoogle Scholar
  69. Harkany T, Holmgren C, Hartig W, Qureshi T, Chaudhry FA, Storm-Mathisen J, Dobszay MB, Berghuis P, Schulte G, Sousa KM, Fremeau RT, Jr., Edwards RH, Mackie K, Ernfors P, Zilberter Y (2004) Endocannabinoid-Independent Retrograde Signaling at Inhibitory Synapses in Layer 2/3 of Neocortex: Involvement of Vesicular Glutamate Transporter 3. J Neurosci 24:4978-4988.PubMedCrossRefGoogle Scholar
  70. Hartinger J, Jahn R (1993) An anion binding site that regulates the glutamate transporter of synaptic vesicles. J Biol Chem 268:23122-23127.PubMedGoogle Scholar
  71. Haydon PG, Carmignoto G (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86:1009-1031.PubMedCrossRefGoogle Scholar
  72. Heikkila RE, Manzino L, Cabbat FS, Duvoisin RC (1984) Protection against the dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine by monoamine oxidase inhibitors. Nature 311:467-469.PubMedCrossRefGoogle Scholar
  73. Hell JW, Maycox PR, Jahn R (1990) Energy dependence and functional reconstitution of the gamma-aminobutyric acid carrier from synaptic vesicles. J Biol Chem 265:2111-2117.PubMedGoogle Scholar
  74. Israel M, Manaranche R, Morot Gaudry-Talarmain Y, Lesbats B, Gulik-Krzywicki T, Dedieu JC (1987) Effect of cetiedil on acetylcholine release and intramembrane particles in cholinergic synaptosomes. Biol Cell 61:59-63.PubMedGoogle Scholar
  75. Janz R, Goda Y, Geppert M, Missler M, Sudhof TC (1999) SV2A and SV2B function as redundant Ca2+ regulators in neurotransmitter release. Neuron 24:1003-1016.PubMedCrossRefGoogle Scholar
  76. Janz R, Hofmann K, Sudhof TC (1998) SVOP, an evolutionarily conserved synaptic vesicle protein, suggests novel transport functions of synaptic vesicles. J Neurosci 18:9269-9281.PubMedGoogle Scholar
  77. Javitch JA, D’Amato RJ, Strittmatter SM, Snyder SH (1985) Parkinsonism-inducing neurotoxin, N-methyl-4-phenyl-1,2,3,6 - tetrahydropyridine: uptake of the metabolite N-methyl4-phenylpyridine by dopamine neurons explains selective toxicity. Proc Natl Acad Sci USA 82:2173-2177.PubMedCrossRefGoogle Scholar
  78. Jentsch TJ (2006) Chloride and the endosomal/lysosomal pathway-emerging roles of CLC chloride transporters. J Physiol.Google Scholar
  79. Jentsch TJ, Friedrich T, Schriever A, Yamada H (1999) The CLC chloride channel family. Pflugers Arch 437:783-795.PubMedCrossRefGoogle Scholar
  80. Jin H, Wu H, Osterhaus G, Wei J, Davis K, Sha D, Floor E, Hsu CC, Kopke RD, Wu JY (2003) Demonstration of functional coupling between gamma -aminobutyric acid (GABA) synthesis and vesicular GABA transport into synaptic vesicles. Proc Natl Acad Sci USA 100:4293-4298.PubMedCrossRefGoogle Scholar
  81. Johnson RG, Jr. (1988b) Accumulation of biological amines into chromaffin granules: a model for hormone and neurotransmitter transport. Physiol Rev 68:232-307.Google Scholar
  82. Johnson RG, Jr. (1988a) Accumulation of biological amines into chromaffin granules: a model for hormone and neurotransmitter transport. Physiol Rev 68:232-307.Google Scholar
  83. Jonas P, Bischofberger J, Sandkuhler J (1998) Corelease of two fast neurotransmitters at a central synapse [see comments]. Science 281:419-424.PubMedCrossRefGoogle Scholar
  84. Juge N, Yoshida Y, Yatsushiro S, Omote H, Moriyama Y (2006) Vesicular glutamate transporter contains two independent transport machineries. J Biol Chem.Google Scholar
  85. Kaufman R, Rogers GA, Fehlmann C, Parsons SM (1989) Fractional vesamicol receptor occupancy and acetylcholine active transport inhibition in synaptic vesicles. Mol Pharmacol 36:452-458.PubMedGoogle Scholar
  86. Keller BU, Blaschke M, Rivosecchi R, Hollmann M, Heinemann SF, Konnerth A (1993) Identification of a subunit-specific antagonist of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate/kainate receptor channels. Proc Natl Acad Sci USA 90:605-609.PubMedCrossRefGoogle Scholar
  87. Khoshbouei H, Sen N, Guptaroy B, Johnson L, Lund D, Gnegy ME, Galli A, Javitch JA (2004) N-terminal phosphorylation of the dopamine transporter is required for amphetamine-induced efflux. PLoS Biol 2:E78.PubMedCrossRefGoogle Scholar
  88. Kish PE, Fischer-Bovenkerk C, Ueda T (1989) Active transport of gamma-aminobutyric acid and glycine into synaptic vesicles. Proc Natl Acad Sci USA 86:3877-3881.PubMedCrossRefGoogle Scholar
  89. Knoth J, Zallakian M, Njus D (1981) Stoichiometry of H+-linked dopamine transport in chromaffin granule ghosts. Biochemistry 20:6625-6629.PubMedCrossRefGoogle Scholar
  90. Kolby L, Bernhardt P, Levin-Jakobsen AM, Johanson V, Wangberg B, Ahlman H, ForssellAronsson E, Nilsson O (2003) Uptake of meta-iodobenzylguanidine in neuroendocrine tumours is mediated by vesicular monoamine transporters. Br J Cancer 89:1383-1388.PubMedCrossRefGoogle Scholar
  91. Langston JW, Ballard P, Tetrud JW, Irwin I (1983) Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 219:979-980.PubMedCrossRefGoogle Scholar
  92. Langston JW, Forno LS, Rebert CS, Irwin I (1984) Selective nigral toxicity after systemic administration of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyrine (MPTP) in the squirrel monkey. Brain Res 292:390-394.PubMedCrossRefGoogle Scholar
  93. Liu Y, Edwards RH (1997) The role of vesicular transport proteins in synaptic transmission and neural degeneration. Annu Rev Neurosci 20:125-156.PubMedCrossRefGoogle Scholar
  94. Liu Y, Peter D, Roghani A, Schuldiner S, Prive GG, Eisenberg D, Brecha N, Edwards RH (1992) A cDNA that suppresses MPP+ toxicity encodes a vesicular amine transporter. Cell 70:539-551.PubMedCrossRefGoogle Scholar
  95. Lynch BA, Lambeng N, Nocka K, Kensel-Hammes P, Bajjalieh SM, Matagne A, Fuks B (2004) The synaptic vesicle protein SV2A is the binding site for the antiepileptic drug levetiracetam. Proc Natl Acad Sci USA 101:9861-9866.PubMedCrossRefGoogle Scholar
  96. Mahata M, Mahata SK, Parmer RJ, O’Connor DT (1996) Vesicular monoamine transport inhibitors. Novel action at calcium channels to prevent catecholamine secretion. Hypertension 28:414-420.PubMedGoogle Scholar
  97. Mariussen E, Fonnum F (2003) The effect of brominated flame retardants on neurotransmitter uptake into rat brain synaptosomes and vesicles. Neurochem Int 43:533-542.PubMedCrossRefGoogle Scholar
  98. Matthies DS, Fleming PA, Wilkes DM, Blakely RD (2006) The Caenorhabditis elegans choline transporter CHO-1 sustains acetylcholine synthesis and motor function in an activity-dependent manner. J Neurosci 26:6200-6212.PubMedCrossRefGoogle Scholar
  99. Maycox PR, Deckwerth T, Hell JW, Jahn R (1988) Glutamate uptake by brain synaptic vesicles. J Biol Chem 263:15423-15428.PubMedGoogle Scholar
  100. McIntire SL, Jorgensen E, Horvitz HR (1993) Genes required for GABA function in Caenorhabditis elegans. Nature 364:334-337.PubMedCrossRefGoogle Scholar
  101. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM (1997) Identification and chacterization of the vesicular GABA transporter. Nature 389:870-876.PubMedCrossRefGoogle Scholar
  102. Merickel A, Rosandich P, Peter D, Edwards RH (1995) Identification of residues involved in substrate recognition by a vesicular monoamine transporter. J Biol Chem 270:25798-25804.PubMedCrossRefGoogle Scholar
  103. Metzger RR, Brown JM, Sandoval V, Rau KS, Elwan MA, Miller GW, Hanson GR, Fleckenstein AE (2002) Inhibitory effect of reserpine on dopamine transporter function. Eur J Pharmacol 456:39-43.PubMedCrossRefGoogle Scholar
  104. Michel PP, Hefti F (1990) Toxicity of 6-hydroxydopamine and dopamine for dopaminergic neurons in culture. J Neurosci Res 26:428-435.PubMedCrossRefGoogle Scholar
  105. Montana V, Ni Y, Sunjara V, Hua X, Parpura V (2004) Vesicular glutamate transporter-dependent glutamate release from astrocytes. J Neurosci 24:2633-2642.PubMedCrossRefGoogle Scholar
  106. Moutsimilli L, Farley S, Dumas S, El MS, Giros B, Tzavara ET (2005) Selective cortical VGLUT1 increase as a marker for antidepressant activity. Neuropharmacology 49:890-900.PubMedCrossRefGoogle Scholar
  107. Naito S, Ueda T (1985) Characterization of glutamate uptake into synaptic vesicles. J Neurochem 44:99-109.PubMedCrossRefGoogle Scholar
  108. Naito S, Ueda T (1983) Adenosine triphosphate-dependent uptake of glutamate into protein I-associated synaptic vesicles. J Biol Chem 258:696-699.PubMedGoogle Scholar
  109. Naudon L, Raisman-Vozari R, Edwards RH, Leroux-Nicollet I, Peter D, Liu Y, Costentin J (1996) Reserpine affects differentially the density of the vesicular monoamine transporter and dihydrotetrabenazine binding sites. Eur J Neurosci 8:842-846.PubMedCrossRefGoogle Scholar
  110. Neal RJ, Chater KF (1987) Nucleotide sequence analysis reveals similarities between proteins determining methylenomycin A resistance in Streptomyces and tetracycline resistance in eubacteria. Gene 58:229-241.PubMedCrossRefGoogle Scholar
  111. Nelson N (1992) The vacuolar H(+)-ATPase-one of the most fundamental ion pumps in nature. J Exp Biol 172:19-27.PubMedGoogle Scholar
  112. Neyfakh AA, Bidnenko VE, Chen LB (1991) Efflux-mediated multidrug resistance in Bacillus subtilis: similarities and dissimilarities with the mammalian system. Proc Natl Acad Sci USA 88:4781-4785.PubMedCrossRefGoogle Scholar
  113. Nguyen TT, Postle K, Bertrand KP (1983) Sequence homology between the tetracycline-resistance determinants of Tn10 and pBR322. Gene 25:83-92.PubMedCrossRefGoogle Scholar
  114. Ni B, Rosteck PR, Jr., Nadi NS, Paul SM (1994) Cloning and expression of a cDNA encoding a brain-specific Na(+)-dependent inorganic phosphate cotransporter. Proc Natl Acad Sci USA 91:5607-5611.PubMedCrossRefGoogle Scholar
  115. Nicklas WJ, Vyas I, Heikkila RE (1985) Inhibition of NADH-linked oxidation in brain mitochondria by 1-methyl-4-phenyl-pyridine, a metabolite of the neurotoxin, 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine. Life Sci 36:2503-2508.PubMedCrossRefGoogle Scholar
  116. Nirenberg MJ, Chan J, Liu Y, Edwards RH, Pickel VM (1996) Ultrastructural localization of the vesicular monoamine transporter-2 in midbrain dopaminergic neurons: potential sites for somatodendritic storage and release of dopamine. J Neurosci 16:4135-4145.PubMedGoogle Scholar
  117. Ogita K, Hirata K, Bole DG, Yoshida S, Tamura Y, Leckenby AM, Ueda T (2001) Inhibition of vesicular glutamate storage and exocytotic release by Rose Bengal. J Neurochem 77:34-42.PubMedCrossRefGoogle Scholar
  118. Ortwine DF, Malone TC, Bigge CF, Drummond JT, Humblet C, Johnson G, Pinter GW (1992) Generation of N-methyl-D-aspartate agonist and competitive antagonist pharmacophore models. Design and synthesis of phosphonoalkyl-substituted tetrahydroisoquinolines as novel antagonists. J Med Chem 35:1345-1370.PubMedCrossRefGoogle Scholar
  119. Ozkan ED, Lee FS, Ueda T (1997) A protein factor that inhibits ATP-dependent glutamate and gamma-aminobutyric acid accumulation into synaptic vesicles: purification and initial characterization. Proc Natl Acad Sci USA 94:4137-4142.PubMedCrossRefGoogle Scholar
  120. Parsons SM, Prior C, Marshall IG (1993) Acetylcholine transport, storage, and release. Int Rev Neurobiol 35:279-390.PubMedCrossRefGoogle Scholar
  121. Peter D, Jimenez J, Liu Y, Kim J, Edwards RH (1994) The chromaffin granule and synaptic vesicle amine transporters differ in substrate recognition and sensitivity to inhibitors. J Biol Chem 269:7231-7237.PubMedGoogle Scholar
  122. Peter D, Liu Y, Sternini C, de Giorgio R, Brecha N, Edwards RH (1995) Differential expression of two vesicular monoamine transporters. J Neurosci 15:6179-6188.PubMedGoogle Scholar
  123. Picollo A, Pusch M (2005) Chloride/proton antiporter activity of mammalian CLC proteins ClC-4 and ClC-5. Nature 436:420-423.PubMedCrossRefGoogle Scholar
  124. Pothos EN, Larsen KE, Krantz DE, Liu Y, Haycock JW, Setlik W, Gershon MD, Edwards RH, Sulzer D (2000) Synaptic vesicle transporter expression regulates vesicle phenotype and quantal size. J Neurosci 20:7297-7306.PubMedGoogle Scholar
  125. Pyle RA, Schivell AE, Hidaka H, Bajjalieh SM (2000) Phosphorylation of synaptic vesicle protein 2 modulates binding to synaptotagmin. J Biol Chem 275:17195-17200.PubMedCrossRefGoogle Scholar
  126. Raiteri L, Raiteri M, Bonanno G (2002) Coexistence and function of different neurotransmitter transporters in the plasma membrane of CNS neurons. Prog Neurobiol 68:287-309.PubMedCrossRefGoogle Scholar
  127. Ramsay RR, Salach JI, Singer TP (1986) Uptake of the neurotoxin 1-methyl-4-phenylpyridine (MPP+) by mitochondria and its relation to the inhibition of the mitochondrial oxidation of NAD+-linked substrates by MPP+. Biochem Biophys Res Commun 134:743-748.PubMedCrossRefGoogle Scholar
  128. Rehavi M, Roz N, Weizman A (2002) Chronic clozapine, but not haloperidol, treatment affects rat brain vesicular monoamine transporter 2. Eur Neuropsychopharmacol 12:261-268.PubMedCrossRefGoogle Scholar
  129. Reimer RJ, Edwards RH (2004) Organic anion transport is the primary function of the SLC17/type I phosphate transporter family. Pflugers Arch 447:629-635.PubMedCrossRefGoogle Scholar
  130. Renick SE, Kleven DT, Chan J, Stenius K, Milner TA, Pickel VM, Fremeau RT, Jr. (1999) The mammalian brain high-affinity L-proline transporter is enriched preferentially in synaptic vesicles in a subpopulation of excitatory nerve terminals in rat forebrain. J Neurosci 19:21-33.PubMedGoogle Scholar
  131. Riddle EL, Fleckenstein AE, Hanson GR (2005) Role of monoamine transporters in mediating psychostimulant effects. AAPS J 7:E847-E851.PubMedCrossRefGoogle Scholar
  132. Rizzoli SO, Richards DA, Betz WJ (2003) Monitoring synaptic vesicle recycling in frog motor nerve terminals with FM dyes. J Neurocytol 32:539-549.PubMedCrossRefGoogle Scholar
  133. Rogers GA, Kornreich WD, Hand K, Parsons SM (1993) Kinetic and equilibrium characterization of vesamicol receptor-ligand complexes with picomolar dissociation constants. Mol Pharmacol 44:633-641.PubMedGoogle Scholar
  134. Rogers GA, Parsons SM (1989) Inhibition of acetylcholine storage by acetylcholine analogs in vitro. Mol Pharmacol 36:333-341.PubMedGoogle Scholar
  135. Roghani A, Feldman J, Kohan SA, Shirzadi A, Gundersen CB, Brecha N, Edwards RH (1994) Molecular cloning of a putative vesicular transporter for acetylcholine. Proc Natl Acad Sci USA 91:10620-10624.PubMedCrossRefGoogle Scholar
  136. Roghani A, Shirzadi A, Kohan SA, Edwards RH, Butcher LL (1996) Differential distribution of the putative vesicular transporter for acetylcholine in the rat central nervous system. Brain Res Mol Brain Res 43:65-76.PubMedCrossRefGoogle Scholar
  137. Roseth S, Fonnum F (1995) A study of the uptake of glutamate, gamma-aminobutyric acid (GABA), glycine and beta-alanine in synaptic brain vesicles from fish and avians. Neurosci Lett 183:62-66.PubMedCrossRefGoogle Scholar
  138. Roseth S, Fykse EM, Fonnum F (1995) Uptake of L-glutamate into rat brain synaptic vesicles: effect of inhibitors that bind specifically to the glutamate transporter. J Neurochem 65:96-103.PubMedGoogle Scholar
  139. Roseth S, Fykse EM, Fonnum F (1998) The effect of arachidonic acid and free fatty acids on vesicular uptake of glutamate and gamma-aminobutyric acid. Eur J Pharmacol 341:281-288.PubMedCrossRefGoogle Scholar
  140. Rudnick G, Steiner-Mordoch SS, Fishkes H, Stern-Bach Y, Schuldiner S (1990) Energetics of reserpine binding and occlusion by the chromaffin granule biogenic amine transporter. Biochemistry 29:603-608.PubMedCrossRefGoogle Scholar
  141. Rudnick G, Wall SC (1992) The molecular mechanism of “ecstasy” [3,4-methylenedioxymethamphetamine (MDMA)]: serotonin transporters are targets for MDMA-induced serotonin release. Proc Natl Acad Sci USA 89:1817-1821.PubMedCrossRefGoogle Scholar
  142. Ruiz J, Ribera A, Jurado A, Marco F, Vila J (2005) Evidence for a reserpine-affected mechanism of resistance to tetracycline in Neisseria gonorrhoeae. APMIS 113:670-674.PubMedCrossRefGoogle Scholar
  143. Ryan TA, Smith SJ (1995) Vesicle pool mobilization during action potential firing at hippocampal synapses. Neuron 14:983-989.PubMedCrossRefGoogle Scholar
  144. Sagne C, El Mestikawy S., Isambert MF, Hamon M, Henry JP, Giros B, Gasnier B (1997) Cloning of a functional vesicular GABA and glycine transporter by screening of genome databases. FEBS Lett 417:177-183.PubMedCrossRefGoogle Scholar
  145. Sagne C, Isambert MF, Vandekerckhove J, Henry JP, Gasnier B (1997) The photoactivatable inhibitor 7-azido-8-iodoketanserin labels the N terminus of the vesicular monoamine transporter from bovine chromaffin granules. Biochemistry 36:3345-3352.PubMedCrossRefGoogle Scholar
  146. Sandoval V, Riddle EL, Hanson GR, Fleckenstein AE (2002) Methylphenidate redistributes vesicular monoamine transporter-2: role of dopamine receptors. J Neurosci 22:8705-8710.PubMedGoogle Scholar
  147. Schafer MK, Varoqui H, Defamie N, Weihe E, Erickson JD (2002) Molecular cloning and functional identification of mouse vesicular glutamate transporter 3 and its expression in subsets of novel excitatory neurons. J Biol Chem 277:50734-50748.PubMedCrossRefGoogle Scholar
  148. Schafer MK, Weihe E, Varoqui H, Eiden LE, Erickson JD (1994) Distribution of the vesicular acetylcholine transporter (VAChT) in the central and peripheral nervous systems of the rat. J Mol Neurosci 5:1-26.PubMedCrossRefGoogle Scholar
  149. Scheel O, Zdebik AA, Lourdel S, Jentsch TJ (2005) Voltage-dependent electrogenic chloride/proton exchange by endosomal CLC proteins. Nature 436:424-427.PubMedCrossRefGoogle Scholar
  150. Scheunemann M, Sorger D, Wenzel B, Heinitz K, Schliebs R, Klingner M, Sabri O, Steinbach J (2004) Synthesis of novel 4- and 5-substituted benzyl ether derivatives of vesamicol and in vitro evaluation of their binding properties to the vesicular acetylcholine transporter site. Bioorg Med Chem 12:1459-1465.PubMedCrossRefGoogle Scholar
  151. Schivell AE, Batchelor RH, Bajjalieh SM (1996) Isoform-specific, calcium-regulated interaction of the synaptic vesicle proteins SV2 and synaptotagmin. J Biol Chem 271:27770-27775.PubMedCrossRefGoogle Scholar
  152. Schuldiner S, Granot D, Mordoch SS, Ninio S, Rotem D, Soskin M, Tate CG, Yerushalmi H (2001) Small is mighty: EmrE, a multidrug transporter as an experimental paradigm. News Physiol Sci 16:130-134.PubMedGoogle Scholar
  153. Schuldiner S, Liu Y, Edwards RH (1993a) Reserpine binding to a vesicular amine transporter expressed in Chinese hamster ovary fibroblasts. J Biol Chem 268:29-34.Google Scholar
  154. Schuldiner S, Shirvan A, Linial M (1995) Vesicular neurotransmitter transporters: from bacteria to humans. Physiol Rev 75:369-392.PubMedGoogle Scholar
  155. Schuldiner S, Steiner-Mordoch S, Yelin R (1998) Molecular and biochemical studies of rat vesicular monoamine transporter. Adv Pharmacol 42:223-227.PubMedCrossRefGoogle Scholar
  156. Schuldiner S, Steiner-Mordoch S, Yelin R, Wall SC, Rudnick G (1993b) Amphetamine derivatives interact with both plasma membrane and secretory vesicle biogenic amine transporters. Mol Pharmacol 44:1227-1231.Google Scholar
  157. Sievert MK, Ruoho AE (1997) Peptide mapping of the [125I]Iodoazidoketanserin and [125I]2-N-[(3 -iodo-4 -azidophenyl)propionyl]tetrabenazine binding sites for the synaptic vesicle monoamine transporter. J Biol Chem 272:26049-26055.PubMedCrossRefGoogle Scholar
  158. Song H, Ming G, Fon E, Bellocchio E, Edwards RH, Poo M (1997) Expression of a putative vesicular acetylcholine transporter facilitates quantal transmitter packaging. Neuron 18:815-826.PubMedCrossRefGoogle Scholar
  159. Stobrawa SM, Breiderhoff T, Takamori S, Engel D, Schweizer M, Zdebik AA, Bosl MR, Ruether K, Jahn H, Draguhn A, Jahn R, Jentsch TJ (2001) Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron 29:185-196.PubMedCrossRefGoogle Scholar
  160. Sulzer D, Chen TK, Lau YY, Kristensen H, Rayport S, Ewing A (1995) Amphetamine redistributes dopamine from synaptic vesicles to the cytosol and promotes reverse transport. J Neurosci 15:4102-4108.PubMedGoogle Scholar
  161. Sulzer D, Galli A (2003) Dopamine transport currents are promoted from curiosity to physiology. Trends Neurosci 26:173-176.PubMedCrossRefGoogle Scholar
  162. Sulzer D, Maidment NT, Rayport S (1993) Amphetamine and other weak bases act to promote reverse transport of dopamine in ventral midbrain neurons. J Neurochem 60:527-535.PubMedCrossRefGoogle Scholar
  163. Sulzer D, Rayport S (1990) Amphetamine and other psychostimulants reduce pH gradients in midbrain dopaminergic neurons and chromaffin granules: a mechanism of action. Neuron 5:797-808.PubMedCrossRefGoogle Scholar
  164. Tabb JS, Ueda T (1991) Phylogenetic studies of the synaptic vesicle glutamate transport system. J Neurosci 11:1822-1828.PubMedGoogle Scholar
  165. Takamori S (2006) VGLUTs: ‘exciting’ times for glutamatergic research? Neurosci Res 55:343-351.PubMedCrossRefGoogle Scholar
  166. Takamori S, et al. (2006) Molecular anatomy of a trafficking organelle. Cell 127:831-846.PubMedCrossRefGoogle Scholar
  167. Takamori S, Rhee JS, Rosenmund C, Jahn R (2000) Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons [see comments]. Nature 407:189-194.PubMedCrossRefGoogle Scholar
  168. Tayebati SK, Di Tullio MA, Amenta F (2004) Effect of treatment with the cholinesterase inhibitor rivastigmine on vesicular acetylcholine transporter and choline acetyltransferase in rat brain. Clin Exp Hypertens 26:363-373.PubMedCrossRefGoogle Scholar
  169. Teng L, Crooks PA, Dwoskin LP (1998) Lobeline displaces [3H]dihydrotetrabenazine binding and releases [3H]dopamine from rat striatal synaptic vesicles: comparison with d-amphetamine. J Neurochem 71:258-265.PubMedCrossRefGoogle Scholar
  170. Thompson CM, Davis E, Carrigan CN, Cox HD, Bridges RJ, Gerdes JM (2005) Inhibitor of the glutamate vesicular transporter (VGLUT). Curr Med Chem 12:2041-2056.PubMedCrossRefGoogle Scholar
  171. Tordera RM, Pei Q, Sharp T (2005) Evidence for increased expression of the vesicular glutamate transporter, VGLUT1, by a course of antidepressant treatment. J Neurochem 94:875-883.PubMedCrossRefGoogle Scholar
  172. Torres GE, Gainetdinov RR, Caron MG (2003) Plasma membrane monoamine transporters: structure, regulation and function. Nat Rev Neurosci 4:13-25.PubMedCrossRefGoogle Scholar
  173. Van der Kloot W (2003) Loading and recycling of synaptic vesicles in the Torpedo electric organ and the vertebrate neuromuscular junction. Prog Neurobiol 71:269-303.PubMedCrossRefGoogle Scholar
  174. Varoqui H, Erickson JD (1996) Active transport of acetylcholine by the human vesicular acetylcholine transporter. J Biol Chem 271:27229-27232.PubMedCrossRefGoogle Scholar
  175. Venton BJ, Seipel AT, Phillips PE, Wetsel WC, Gitler D, Greengard P, Augustine GJ, Wightman RM (2006) Cocaine increases dopamine release by mobilization of a synapsin-dependent reserve pool. J Neurosci 26:3206-3209.PubMedCrossRefGoogle Scholar
  176. Wall SC, Gu H, Rudnick G (1995) Biogenic amine flux mediated by cloned transporters stably expressed in cultured cell lines: amphetamine specificity for inhibition and efflux. Mol Pharmacol 47:544-550.PubMedGoogle Scholar
  177. Wang XQ, Deriy LV, Foss S, Huang P, Lamb FS, Kaetzel MA, Bindokas V, Marks JD, Nelson DJ (2006) CLC-3 channels modulate excitatory synaptic transmission in hippocampal neurons. Neuron 52:321-333.PubMedCrossRefGoogle Scholar
  178. Wang YM, Gainetdinov RR, Fumagalli F, Xu F, Jones SR, Bock CB, Miller GW, Wightman RM, Caron MG (1997) Knockout of the vesicular monoamine transporter 2 gene results in neonatal death and supersensitivity to cocaine and amphetamine. Neuron 19:1285-1296.PubMedCrossRefGoogle Scholar
  179. Weaver JA, Deupree JD (1982) Conditions required for reserpine binding to the catecholamine transporter on chromaffin granule ghosts. Eur J Pharmacol 80:437-438.PubMedCrossRefGoogle Scholar
  180. Weihe E, Schafer MK, Erickson JD, Eiden LE (1994) Localization of vesicular monoamine transporter isoforms (VMAT1 and VMAT2) to endocrine cells and neurons in rat. J Mol Neurosci 5:149-164.PubMedCrossRefGoogle Scholar
  181. Whittaker VP (1987) Cholinergic synaptic vesicles from the electromotor nerve terminals of Torpedo. Composition and life cycle. Ann N Y Acad Sci 493:77-91.PubMedCrossRefGoogle Scholar
  182. Wilkens S (2005) Rotary molecular motors. Adv Protein Chem 71:345-382.PubMedCrossRefGoogle Scholar
  183. Winter S, Brunk I, Walther DJ, Holtje M, Jiang M, Peter JU, Takamori S, Jahn R, Birnbaumer L, hnert-Hilger G (2005) Galphao2 regulates vesicular glutamate transporter activity by changing its chloride dependence. J Neurosci 25:4672-4680.PubMedCrossRefGoogle Scholar
  184. Wojcik SM, Katsurabayashi S, Guillemin I, Friauf E, Rosenmund C, Brose N, Rhee JS (2006) A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron 50:575-587.PubMedCrossRefGoogle Scholar
  185. Wolosker H, de Souza DO, de ML (1996) Regulation of glutamate transport into synaptic vesicles by chloride and proton gradient. J Biol Chem 271:11726-11731.PubMedCrossRefGoogle Scholar
  186. Xu T, Bajjalieh SM (2001) SV2 modulates the size of the readily releasable pool of secretory vesicles. Nat Cell Biol 3:691-698.PubMedCrossRefGoogle Scholar
  187. Yang L, Matthews RT, Schulz JB, Klockgether T, Liao AW, Martinou JC, Penney JB, Jr., Hyman BT, Beal MF (1998) 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyride neurotoxicity is attenuated in mice overexpressing Bcl-2. J Neurosci 18:8145-8152.PubMedGoogle Scholar
  188. Yelin R, Schuldiner S (1995) The pharmacologicalal profile of the vesicular monoamine transporter resembles that of multidrug transporters. FEBS Lett 377:201-207.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • Farrukh A. Chaudhry
    • 1
  • Jean-Luc Boulland
    • 2
  • Monica Jenstad
    • 3
  • May K. L. Bredahl
    • 4
  • Robert H. Edwards
    • 5
  1. 1.The Biotechnology Centre of Oslo, Centre for Molecular Biology and NeuroscienceUniversity of OsloBlindern, OsloNorway
  2. 2.The Biotechnology Centre of Oslo, Centre for Molecular Biology and NeuroscienceUniversity of OsloOsloNorway
  3. 3.The Biotechnology Centre of Oslo, Centre for Molecular Biology and NeuroscienceUniversity of OsloOsloNorway
  4. 4.The Biotechnology Centre of OsloUniversity of OsloOsloNorway
  5. 5.Departments of Neurology and PhysiologyUniversity of California, San Francisco School of MedicineCaliforniaUSA

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