Regulation of vesicular monoamine and glutamate transporters by vesicle-associated trimeric G proteins: New jobs for long-known signal transduction molecules

Handbook of Experimental Pharmacology

Volumn 175, Issue , 2006, Pages 305-325

  Brunk, I ^a   Holtje M ^a   Von Jagow, B ^a   Winter, S ^a   Sternberg, J ^a   Blex, C ^a   Pahner, I ^a   Ahnert Hilger, G ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

G protein; Neurotransmitter; Storage; Vesicular filling; Vesicular transmitter transporter

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CHLORIDE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; VESICULAR GLUTAMATE TRANSPORTER; VESICULAR MONOAMINE TRANSPORTER;

ANIMAL; BRAIN; HUMAN; METABOLISM; REVIEW; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; BRAIN; CHLORIDES; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; HETEROTRIMERIC GTP-BINDING PROTEINS; HUMANS; NEUROTRANSMITTER AGENTS; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; VESICULAR GLUTAMATE TRANSPORT PROTEINS; VESICULAR MONOAMINE TRANSPORT PROTEINS;

EID: 33845924925     PISSN: 01712004     EISSN: 18650325     Source Type: Book Series    
DOI: 10.1007/3-540-29784-7_15     Document Type: Article

References (78)

1. Ahnert-Hilger G, Nürnberg B, Exner T, Schäfer T, Jahn R (1998) The heterotrimeric G protein Go2 regulates catecholamine uptake by secretory vesicles. EMBO J 17:406-413
2. Ahnert-Hilger G, Höltje M, Pahner I, Winter S, Brunk I (2003) Regulation of vesicular transmitter transporter. Rev Physiol Biochem Pharmacol 150:140-160
3. Bai L, Xu H, Collins JF, Ghishan FK (2001) Molecular and functional analysis of a novel neuronal vesicular glutamate transporter. J Biol Chem 276:36764-36769
4. Bellocchio EE, Reimer RJ, Fremeau jr RT, Edwards RH (2000) Uptake of glutamate into synaptic vesicle by an inorganic phosphate transporter. Science 289:957-960
5. Blondeau F, Ritter B, Allaire PD, Wasiak S, Girard M, Hussain NK, Angers A, Legendre- Guillemin V, Roy L, Boismenu D, Kearney RE, Bell AW, Bergeron JJM, McPherson PS (2004) Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc Natl Acad Sci USA 101:3833-3838
6. BrunsD,RiedelD,Klingauf J, Jahn R(2000) Quantal release of serotonin.Neuron 28:205-220
7. Cases O, Seif I, Grimsby J, Gaspar P, Chen K, Pournin S,Muller U, Aguet M, Babinet C, Chen Shih J, DeMaeyer E (1995) Aggressive bahaviour and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 208:1763-1766
8. ChenC,Clarke IJ (1996)Go-2proteinmediates the reductioninCa2+ currentby somatostatin in cultured ovine somatotrophs. J Physiol 491:21-29
9. Colliver TL, Pyott SJ, Achalabun M, Ewing AG (2000) VMAT-mediated changes in quantal size and vesicular volume. J Neurosci 20:5276-5282
10. Croft BG, Fortin GD, Corera AT, Edwards RH, Beaudet A, Trudeau L-E, Fon EA (2005) Normal biogenesis and cycling of empty synaptic vesicles in dopamine neurons of vesicular monoamine transporter 2 knockout mice. Mol Biol Cell 16:306-315
11. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1-105
12. Daniels RW, Collins CA, Gelfand MV, Dant J, Brooks ES, Krantz DE, DiAntonio A (2004) Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content. J Neurosci 24:10466-10474
13. Dhingra A, Lyubarsky A, Jiang M, Pugh EN, Birnbaumer L, Sterling P, Vardi N (2001) The light responses of ON bipolar neurons require Gαo. J Neurosci 20:9053-9058
14. Dhingra A, Jiang M, Wang T-L, Lyubarsky A, Savchenko A, Bar-Yehuda T, Sterling P, Birnbaumer L, Vardi N (2002) Light response of retinal ON bipolar cells requires a specific splice variant of Gαo. J Neurosci 22:4878-4884
15. EngelD,Pahner I, Schulze K, FrahmC, JarryH, Ahnert-Hilger G, DraguhnA(2001) Plasticity of central inhibitory synapses through GABAmetabolism. J Physiol (Lond) 535:473-485
16. Erickson JD, Eiden LE, Hoffman BJ (1992) Expression cloning of a reserpine sensitive vesicular monoamine transporter. Proc Natl Acad Sci USA 89:10993-10997
17. Erickson JD, Schäfer MK, Bonner TI, Eiden LE, Weihe E (1996) Distinct pharmacological 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
18. Fon EA, Pothos EN, Sun B-C, 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
19. Fremeau jr RT, Matthew DT, 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
20. Fremeau RT, Burman J, Qureshi T, Tran CH, Proctor J, Johnson J, Zhang H, Sulzer D, Copenhagen DR, Storm-Mathisen J, Reimer RJ, Chaudhry FH, 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
21. Fremeau RT, KamK, Qureshi T, Johnson J, Copenhagen DR, Storm-Mathisen J, Chaudry FA, Nicoll RA, Edwards RH (2004) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304:1815-1819
22. Fujiyama F, Furuta T, Kaneko T (2001) Immunocytochemical localization of candidates for vesicular glutamate transporters the rat cerebral cortex. J Comp Neurol 435:379-387
23. Gong LW, Hafez I, Alvarez de Toledo G, LindauM(2003) Secretory vesicles membrane area is regulated in tandem with quantal size in chromaffin cells. J Neurosci 23:7017-7921
24. 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
25. Grishina G, Berlot CH (2000) A surface exposed region of Gs? in which substitutions decrease receptor mediated activation and increase receptor affinity. Mol Pharmacol 57:1081-1092
26. Hartinger J, Jahn R (1993) An anion binding site that regulates the glutamate transporter of synaptic vesicles. J Biol Chem 268:23122-23127
27. Hayashi M, Otsuka M, Morimoto R, Hitota S, Yatsushiro S, Takeda J, Yamamoto A, Moriyama Y (2001) Differentiation-associated Na+-dependent inorganic phosphate cotransporter (DNPI) is a vesicular glutamate transporter in endocrine glutamatergic systems. J Biol Chem 276:43400-43406
28. Hell JW,Maycox PR, Stadler H, Jahn R (1988) Uptake of GABA by rat brain synaptic vesicles isolated by a new procedure. EMBO J 7:3023-3029
29. Hell JW,Maycox PR, Jahn R (1990) Energy dependence and functional reconstitution of the γ-aminobutyric acid carrier from synaptic vesicles. J Biol Chem 265:2111-2117
30. Hisano S,HoshiK, IkedaY,MaruyamaD,KanemotoM,Ichijo J,Kojima I,Takeda J,NogamiH (2000) Regional expression of a gene encoding a neuron-specific Na+-dependent inorganic phosphate cotransporter (DNPI) in the rat forebrain. Mol Brain Res 83:34-43
31. Höltje M, von Jagow B, Pahner I, Lautenschlager M, Hörtnagl H, Nürnberg B, Jahn R, Ahnert-Hilger G (2000) The neuronal monoamine transporter VMAT2 is regulated by the trimeric GTPase Go2. J Neurosci 20:2131-2141
32. Höltje M, Winter S, Walther D, Pahner I, Hörtnagl H, Ottersen OP, Bader M, Ahnert- Hilger G (2003) The vesicular monoamine content regulates VMAT2 activity through G?q in mouse platelets. Evidence for autoregulation of vesicular transmitter uptake. J Biol Chem 278:15850-15858
33. Jiang M, Gold MS, Boulay G, Spicher K, Pexton M, Brabet P, Srinivasan Y, Rudolph U, Ellison G, Birnbaumer L (1998)Multiple neurological abnormalities in mice deficient in the G protein Go. Proc Natl Acad Sci USA 95:3269-3274
34. Johnson jr RG (1988) Accumulation of biological amines into chromaffin granules: amodel for hormone and neurotransmitter transport. Physiol Rev 68:232-307
35. KanekoT,FujiyamaF(2002)Complementary distributionof vesicular glutamate transporter in the central nervous system. Neurosci Res 42:243-250
36. Kleuss C, Hescheler J, Ewel C, Rosenthal W, Schultz G, Wittig B (1991) Assignment of Gprotein subtypes to specific receptors inducing inhibition of calcium currents. Nature 353:43-48
37. Lesch KP,Gross J,Wolozin BL,Murphy DL, Riederer P (1993) Extensive sequence divergence between the human and rat brain vesicular monoamine transporter: possible molecular basis for species differences in the susceptibility to MPP+. J Neural Transm 93:75-82
38. Liu Y, Peter A, 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
39. Liu Y, Schweitzer E, Nirenberg MJ, Pickel VM, Evans CJ, Edwards RH (1994) Preferential localization of a vesicular monoamine transporter to dense core vesicles in PC 12 cells. J Cell Biol 127:1419-1433
40. Ludwig M-G, Vanek M, Guerini D, Gasser JA, Jones CE, Junker U, Hofstetter H, Wolf RM, Seuwen K (2003) Proton-sensing G-protein-coupled receptors. Nature 425:93-98
41. Maycox PR, Hell JW, Jahn R (1990) Amino acid neurotransmission: spotlight on synaptic vesicles. Trends Neurosci 13:83-87
42. Miyazaki T, Fukaya M, Shimizu H, Watanabe M (2003) Subtype switching of vesicular glutamate transporters at parallel fibre-Purkinje cell synapses in developing mouse cerebellum. Eur J Neurosci 17:2563-2572
43. Naito S, Ueda T (1985) Characterization of glutamate uptake into synaptic vesicles. J Neurochem 44:99-109
44. Ni B, Rostock jr PR, 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
45. Nürnberg B, Ahnert-Hilger G (1996) Potential roles of heterotrimeric G proteins of the endomembrane system. FEBS Lett 389:61-65
46. Offermanns S (1999) New insights into the in vivo function of the heterotrimeric G-protein through gene deletion studies. Naunyn Schmiedebergs Arch Pharmacol 360:5-13
47. Pahner I, Höltje M, Winter S, Nürnberg B, Ottersen OP, Ahnert-Hilger G (2002) Subunit composition and functional properties of G-protein heterotrimers on rat chromaffin granules. Eur J Cell Biol 81:449-456
48. Pahner I, Höltje M, Winter S, Takamori S, Bellocchio EE, Spicher K, Laake P, Nürnberg B, Ottersen OP, Ahnert-Hilger G (2003) Functional G-protein heterotrimers are associated with vesicles of putative glutamatergic terminals: implications for regulation of transmitter uptake. Mol Cell Neurosci 23:398-413
49. Palay LS, Chan-Palay VC (1974) Cerebellar cortex. Cytology and organization. Springer- Verlag, Berlin Heidelberg New York
50. Peter D, LiuY, Sternini C, de GiorgioR, Brecha N, EdwardsRH(1995) Differential expression of two vesicular monoamine transporters. J Neurosci 15:6179-6188
51. 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
52. Pothos EN, Przedborski S, Davila V, Schmitz Y, Sulzer D (1998a) D2-like dopamine receptor reduces quantal size in PC12 cells. J Neurosci 18:5575-5585
53. Pothos EN, Davila V, Sulzer D (1998b) Presynaptic recording of quanta from midbrain dopamine neurons and modulation of quantal size. J Neurosci 18:4106-4118
54. Pothos EN, Larsen KE, Krantz DE, Liu Y-j,Haycock JW, SetlikW, GershonMD, Edwards RH, Sulzer D (2000) Synaptic vesicle transporter expression regulates vesicle phenotype and quantal size. J Neurosci 20:7297-7306
55. Reimer RJ, Fon EA, Edwards RH (1998) Vesicular neurotransmitter transport and the presynaptic regulation of quantal size. Curr Opin Neurobiol 8:405-412
56. Reimer RJ, Fremeau jr RT, Bellocchio EE, Edwards RH (2001) The essence of excitation. Curr Opin Cell Biol 13:417-421
57. Sakata-Haga H, Kanemoto M, Maruyama D, Hoshi K, Mogi K, Narita M, Okada N, Ikeda Y, Nogami H, Fukui Y, Kojima I, Takeda J, Hisano S (2001) Differential localization and colocalization of two neuron-types of sodium-dependent inorganic phosphate cotransporters in rat forebrain. Brain Res 902:142-155
58. Schäfer MKH, 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
59. Schuldiner S, Shirvan A, Linial M (1995) Vesicular neurotransmitter transporters: from bacteria to humans. Physiol Rev 75:369-392
60. Schütz B, Schäfer MK, Eiden LE, Weihe E (1998) Vesicular amine transporter expression and isoforms selection in developing brain, peripheral nervous system and gut. Brain Res Dev Brain Res 106:181-204
61. Song H-j, Ming G-l, Fon E, Bellocchio E, Edwards E, Poo M-m (1997) Expression of a putative vesicular acetylcholine transporter facilitates quantal transmitter release. Neuron 18:815-826
62. Sternweis PC, Robishaw JD (1984) Isolation of two proteins with high affinity for guanine nucleotides from membranes of bovine brain. J Biol Chem 259:13806-13813
63. Stobrawa SM, Breiderhoff T, Takamori S, Engel D, Schweizer M, Zdebik AA, Bösl 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
64. Tabb JS, KishPE, vanDykeR,UedaT(1992) Glutamate transport into synaptic vesicles.Roles ofmembrane potential, pH gradient, and intravesicular pH. J Biol Chem 22:15412-15418
65. Takahashi N, Miner LI, Sora I, Ujike H, revay RS, Kostic V, Jackson-lewis V, Przedborski S, Uhl GR (1997) VMAT2 knockout mice: heterozygotes display reduced amphetamineconditioned reward, enhanced amphetamine locomotion, and enhanced MPTP toxicity. Proc Natl Acad Sci USA 94:9938-9943
66. Takamori S, Rhee JS, Rosenmund C, Jahn R (2000) Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407:189-194
67. Takamori S, Rhee JS, Rosenmund C, Jahn R (2001) Identification of differentiation-associated brain-specific phosphate transporter as a second vesicular glutamate transporter (VGLUT2). J Neurosci 21:RC182
68. Takamori S, Malherbe P, Broger C, Jahn R (2002) Molecular cloning and functional characterization of human vesicular glutamate transporter 3. EMBO Rep 3:798-803
69. Travis ER, Wang Y-M, Michael DJ, Caron MG, Wightman RM (2000) Differential quantal release of histamine and 5-hydroxytryptamine from mast cells of vesicular monoamine transporter 2 knock out mice. Proc Natl Acad Sci USA 97:162-167
70. Van der KlootW(1991) The regulation of quantal size. Prog Neurobiol 36:93-103
71. Van der KlootW, Colasante C, Cameron R, Malgó J (2000) Recycling and refilling of transmitter quanta at the frog neuromuscular junction. J Physiol 523:247-258
72. Van derKloot W, Malgo J, Cameron R, Colasante C(2002) Vesicle size and transmitter release at the frog neuromuscular junction when quantal acetylcholine content is increased or decreased. J Physiol 541: 385-389
73. WaltherDJ, Peter JU, Bashammakh S,HörtnaglH,Voits M, Fink H, BaderM(2003) Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 299:76
74. WangY-M, GainetdinovPR, Fumagalli F,Xu F, Jones SR, BockCB,MillerGW, WightmanRM, 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
75. Williams J (1997) How does a vesicle know it is full? Neuron 18:683-686
76. Winter S, Brunk I, Walther DJ, Höltje M, Jiang M, Peter J-U, Takamori S, Jahn R, Birnbaumer L, Ahnert-Hilger G (2005) Gαo2 regulates VGLUT activity by changing its chloride dependence. J Neurosci 25:4672-4680
77. Wojcik SM, Rhee SE, Herzog E, Sigler A, Jahn R, Takamori S, Brose N, Rosenmund C (2004) An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc Natl Acad Sci USA 101:7158-7163
78. Wolosker H, de Souza DO, de Meis L (1996) Regulation of glutamate transport into vesicles by chloride and proton gradient. J Biol Chem 271:11726-11731