Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters

Journal of Comparative Neurology

Volumn 480, Issue 3, 2004, Pages 264-280

  Boulland, Jean Luc ^a   Qureshi, Tayyaba ^a   Seal, Rebecca P ^b   Rafiki, Amina ^a   Gundersen, Vidar ^a   Bergersen, Linda H ^a   Fremeau Jr , Robert T ^b   Edwards, Robert H ^b   Storm Mathisen, Jon ^a   Chaudhry, Farrukh A ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Coexpression; Recycling; Synapse; Transmitter; Vesicle; VGLUT

Indexed keywords

CARRIER PROTEIN; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 2; GLUCOSE TRANSPORTER 3; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; ISOPROTEIN; NEUROTRANSMITTER; UNCLASSIFIED DRUG; VESICULAR 4 AMINOBUTYRIC ACID TRANSPORTER; VESICULAR ACETYLCHOLINE TRANSPORTER; VESICULAR MONOAMINE TRANSPORTER 2; VESICULAR TRANSPORT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; BRAIN REGION; CELL ORGANELLE; CELL POPULATION; CELL SPECIFICITY; CELL TYPE; CEREBELLUM; CEREBELLUM NUCLEUS; DEVELOPMENTAL STAGE; ELECTRON MICROSCOPY; EXOCYTOSIS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MORPHOGENESIS; MOUSE; NERVE CELL CULTURE; NERVE ENDING; NEUROTRANSMITTER RELEASE; NEWBORN; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SARCOPLASM; SKELETAL MUSCLE; STEM CELL; SYNAPSE VESICLE; TELENCEPHALON;

AMINO ACID TRANSPORT SYSTEM X-AG; AMINO ACID TRANSPORT SYSTEMS, ACIDIC; ANIMALS; ASTROCYTES; CELLS, CULTURED; EXOCYTOSIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAMIC ACID; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MORPHOGENESIS; NEURONS; NEUROTRANSMITTER AGENTS; PROSENCEPHALON; PROTEIN ISOFORMS; RATS; STEM CELLS; SYNAPTIC VESICLES; TISSUE DISTRIBUTION; UP-REGULATION; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2; VESICULAR GLUTAMATE TRANSPORT PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 9644287855     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20354     Document Type: Article

References (83)

1. Aghajanian GK, Bloom FE. 1967. The formation of synaptic junctions in developing rat brain: a quantitative electron microscopic study. Brain Res 6:716-727.
2. Ahnert-Hilger G, Kutay U, Chahoud I, Rapoport T, Wiedenmann B. 1996. Synaptobrevin is essential for secretion but not for the development of synaptic processes. Eur J Cell Biol 70:1-11.
3. +-dependent inorganic phosphate cotransporter. J Neurochem 74:2622-2625.
4. Araque A, Carmignoto G, Haydon PG. 2001. Dynamic signaling between astrocytes and neurons. Annu Rev Physiol 63:795-813.
5. Battaglia FC. 2000. Glutamine and glutamate exchange between the fetal liver and the placenta. J Nutr 130:974S-977S.
6. Behar TN, Scott CA, Greene CL, Wen X, Smith SV, Maric D, Liu QY, Colton CA, Barker JL. 1999. Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J Neurosci 19:4449-4461.
7. Bellocchio EE, Hu H, Pohorille A, Chan J, Pickel VM, Edwards RH. 1998. The localization of the brain-specific inorganic phosphate transporter suggests a specific presynaptic role in glutamatergic transmission. J Neurosci 18:8648-8659.
8. 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.
9. Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini BL, Pozzan T, Volterra A. 1998. Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391:281-285.
10. Bolshakov VY, Siegelbaum SA. 1995. Regulation of hippocampal transmitter release during development and long-term potentiation. Science 269:1730-1734.
11. Boulland J-L, Osen KK, Levy LM, Danbolt NC, Edwards RH, Storm-Mathisen J, Chaudhry FA. 2002. Cell-specific expression of the glutamine transporter SN1 suggests differences in dependence on the glutamine cycle. Eur J Neurosci 15:1615-1631.
12. Boulland J-L, Rafiki A, Levy LM, Storm-Mathisen J, Chaudhry FA. 2003. Highly differential expression of SN1, a bidirectional glutamine transporter, in astroglia and endothelium in the developing rat brain. Glia 41:260-275.
13. Cameron HA, McEwen BS, Gould E. 1995. Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 15:4687-4692.
14. Chaudhry FA, Lehre KP, Van Lockeren Campagne M, Ottersen OP, Danbolt NC, Storm-Mathisen J. 1995. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 14:711-720.
15. 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.
16. Chaudhry FA, Reimer RJ, Krizaj D, Barber R, Storm-Mathisen J, Copenhagen DR, Edwards RH. 1999. Molecular analysis of System N suggests novel physiological roles in nitrogen metabolism and synaptic transmission. Cell 99:769-780.
17. Coco S, Verderio C, De Camilli P, Matteoli M. 1998. Calcium dependence of synaptic vesicle recycling before and after synaptogenesis. J Neurochem 71:1987-1992.
18. Colman H, Nabekura J, Lichtman JW. 1997. Alterations in synaptic strength preceding axon withdrawal. Science 275:356-361.
19. Copani A, Casabona G, Bruno V, Caruso A, Condorelli DF, Messina A, Di GG, V, Pin JP, Kuhn R, Knopfel T, Nicoletti F. 1998. The metabotropic glutamate receptor mGlu5 controls the onset of developmental apoptosis in cultured cerebellar neurons. Eur J Neurosci 10:2173-2184.
20. Court JA, Perry EK, Johnson M, Piggott MA, Kerwin JA, Perry RH, Ince PG. 1993. Regional patterns of cholinergic and glutamate activity in the developing and aging human brain. Brain Res Dev Brain Res 74:73-82.
21. Dan Y, Poo MM. 1992. Quantal transmitter secretion from myocytes loaded with acetylcholine. Nature 359:733-736.
22. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol 65:1-105.
23. Dehnes Y, Chaudhry FA, Ullensvang K, Lehre KP, Storm-Mathisen J, Danbolt NC. 1998. The glutamate transporter EAAT4 in rat cerebellar Purkinje cells: a glutamate-gated chloride channel concentrated near the synapse in parts of the dendritic membrane facing astroglia. J Neurosci 18:3606-3619.
24. Dingledine R, Borges K, Bowie D, Traynelis SF. 1999. The glutamate receptor ion channels. Pharmacol Rev 51:7-61.
25. Dudek SM, Bear MF. 1993. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci 13:2910-2918.
26. Forrest D, Yuzaki M, Soares HD, Ng L, Luk DC, Sheng M, Stewart CL, Morgan JI, Connor JA, Curran T. 1994. Targeted disruption of NMDA receptor 1 gene abolishes NMDA response and results in neonatal death. Neuron 13:325-338.
27. 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.
28. 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 U S A 99:14488-14493.
29. Fremeau RT Jr, Voglmaier S, Seal RP, Edwards RH. 2004a. VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci 27:98-103.
30. Fremeau RT Jr, Kam K, Qureshi T, Johnson J, Copenhagen DR, Storm-Mathisen J, Chaudhry FA, Nicoll RA, Edwards RH. 2004b. Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 309:1815-1819.
31. Freund TF. 2003. Interneuron Diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489-495.
32. Freund TF, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus 6: 347-470.
33. Gerfen CR. 1992. The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci 15:133-139.
34. 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.
35. 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.
36. Herkenham M, Pert CB. 1981. Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum. Nature 291:415-418.
37. Herzog E, Bellenchi GC, Gras C, Bernard V, Ravassard P, Bedet C, Gasnier B, Giros B, El Mestikawy S. 2001. The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J Neurosci 21:RC181.
38. Hilfiker S, Pieribone VA, Czernik AJ, Kao HT, Augustine GJ, Greengard P. 1999. Synapsins as regulators of neurotransmitter release. Philos Trans R Soc Lond B Biol Sci 354:269-279.
39. Kitayama T, Yoneyama M, Yoneda Y. 2003. Possible regulation by N-methyl-D-aspartate receptors of proliferative progenitor cells expressed in adult mouse hippocampal dentate gyrus. J Neurochem 84: 767-780.
40. Komuro H, Rakic P. 1993. Modulation of neuronal migration by NMDA receptors. Science 260:95-97.
41. Kopp DM, Ferkel DJ, Balice-Gordon RJ. 2000. Disparity in neurotransmitter release probability among competing inputs during neuromuscular synapse elimination. J Neurosci 20:8771-8779.
42. Kotak VC, Korada S, Schwartz IR, Sanes DH. 1998. A developmental shift from GABAergic to glycinergic transmission in the central auditory system. J Neurosci 18:4646-4655.
43. Kraszewski K, Mundigl O, Daniell L, Verderio C, Matteoli M, De Camilli P. 1995. Synaptic vesicle dynamics in living cultured hippocampal neurons visualized with Cy3-conjugated antibodies directed against the lumenal domain of synaptotagmin. J Neurosci 15:4328-4342.
44. Kwong WH, Chan WY, Lee KK, Fan M, Yew DT. 2000. Neurotransmitters, neuropeptides and calcium binding proteins in developing human cerebellum: a review. Histochem J 32:521-534.
45. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
46. LaMantia AS. 1995. The usual suspects: GABA and glutamate may regulate proliferation in the neocortex. Neuron 15:1223-1225.
47. Lauder JM. 1993. Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci 16:233-240.
48. Liu Y, Edwards RH. 1997. The role of vesicular transport proteins in synaptic transmission and neural degeneration. Annu Rev Neurosci 20:125-156.
49. Liu Y, Schweitzer ES, Nirenberg MJ, Pickel VM, Evans CJ, Edwards RH. 1994. Preferential localization of a vesicular monoamine transporter to dense core vesicles in PC12 cells. J Cell Biol 127:1419-1433.
50. LoTurco JJ, Owens DF, Heath MJ, Davis MB, Kriegstein AR. 1995. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15:1287-1298.
51. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein mesurement with the folin phenol reagent. J Biol Chem 193:265-275.
52. Lubbers K, Wolff JR, Frotscher M. 1985. Neurogenesis of GABAergic neurons in the rat dentate gyrus: a combined autoradiographic and immunocytochemical study. Neurosci Lett 62:317-322.
53. Luk KC, Kennedy TE, Sadikot AF. 2003. Glutamate promotes proliferation of striatal neuronal progenitors by an NMDA receptor-mediated mechanism. J Neurosci 23:2239-2250.
54. Machon O, van den Bout CJ, Backman M, Rosok O, Caubit X, Fromm SH, Geronimo B, Krauss S. 2002. Forebrain-specific promoter/enhancer D6 derived from the mouse Dach1 gene controls expression in neural stem cells. Neuroscience 112:951-966.
55. Marini AM, Rabin SJ, Lipsky RH, Mocchetti I. 1998. Activity-dependent release of brain-derived neurotrophic factor underlies the neuroprotective effect of N-methyl-D-aspartate. J Biol Chem 273:29394-29399.
56. Matsui K, Jahr CE. 2003. Ectopic release of synaptic vesicles. Neuron 40:1173-1183.
57. McDonald JW, Johnston MV. 1990. Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Res 15:41-70.
58. Monti B, Contestabile A. 2000. Blockade of the NMDA receptor increases developmental apoptotic elimination of granule neurons and activates caspases in the rat cerebellum. Eur J Neurosci 12:3117-3123.
59. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH. 1994. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
60. Mount HT, Dreyfus CF, Black IB. 1993. Purkinje cell survival is differentially regulated by metabotropic and ionotropic excitatory amino acid receptors. J Neurosci 13:3173-3179.
61. Nakanishi S, Nakajima Y, Masu M, Ueda Y, Nakahara K, Watanabe D, Yamaguchi S, Kawabata S, Okada M. 1998. Glutamate receptors: brain function and signal transduction. Brain Res Brain Res Rev 26:230-235.
62. Oertel WH, Schmechel DE, Mugnaini E, Tappaz ML, Kopin IJ. 1981. Immunocytochemical localization of glutamate decarboxylase in rat cerebellum with a new antiserum. Neuroscience 6:2715-2735.
63. Ottersen OP, Storm-Mathisen J. 1984. Glutamate- and GABA-containing neurons in the mouse and rat brain as demonstrated with a new immunocytochemical technique. J Comp Neurol 229:374-392.
64. Pahner I, Holtje M, Winter S, Takamori S, Bellocchio EE, Spicher K, Laake P, Numberg 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.
65. Pearce IA, Cambray-Deakin MA, Burgoyne RD. 1987. Glutamate acting on NMDA receptors stimulates neurite outgrowth from cerebellar granule cells. FEBS Lett 223:143-147.
66. Pencea V, Luskin MB. 2003. Prenatal development of the rodent rostral migratory stream. J Comp Neurol 463:402-418.
67. Rabacchi S, Bailly Y, Delhaye-Bouchaud N, Mariani J. 1992. Involvement of the N-methyl D-aspartate (NMDA) receptor in synapse elimination during cerebellar development. Science 256:1823-1825.
68. Reimer RJ, Fremeau RT Jr, Bellocchio EE, Edwards RH. 2001. The essence of excitation. Curr Opin Cell Biol 13:417-421.
69. Roberts PJ, Storm-Mathisen J, Johnston GAR. 1981. Glutamate: transmitter in the central nervous system. New York: John Wiley & Sons.
70. 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 U S A 91:10620-10624.
71. 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.
72. Soriano E, Cobas A, Fairén A. 1986. Asynchronism in the neurogenesis of GABAergic and non-GABAergic neurons in the mouse hippocampus. Brain Res Dev Brain Res 30:88-92.
73. Spencer GE, Klumperman J, Syed NI. 1998. Neurotransmitters and neurodevelopment. Role of dopamine in neurite outgrowth, target selection and specific synapse formation. Perspect Dev Neurobiol 5:451-467.
74. Sprengel R, Suchanek B, Amico C, Brusa R, Burnashev N, Rozov A, Hvalby O, Jensen V, Paulsen O, Andersen P, Kim JJ, Thompson RF, Sun W, Webster LC, Grant SG, Eilers J, Konnerth A, Li J, McNamara JO, Seeburg PH. 1998. Importance of the intracellular domain of NR2 subunits for NMDA receptor function in vivo. Cell 92:279-289.
75. Sulzer D, Joyce MP, Lin L, Geldwert D, Haber SN, Hattori T, Rayport S. 1998. Dopamine neurons make glutamatergic synapses in vitro. J Neurosci 18:4588-4602.
76. 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.
77. 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.
78. +TPI transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. J Neurosci 22:142-155.
79. Verderio C, Coco S, Bacci A, Rossetto O, De Camilli P, Montecucco C, Matteoli M. 1999. Tetanus toxin blocks the exocytosis of synaptic vesicles clustered at synapses but not of synaptic vesicles in isolated axons. J Neurosci 19:6723-6732.
80. Verhage M, Maia AS, Plomp JJ, Brussaard AB, Heeroma JH, Vermeer H, Toonen RF, Hammer RE, van den Berg TK, Missler M, Geuze HJ, Sudhof TC. 2000. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287:864-869.
81. Wærhaug O, Ottersen OP. 1993. Demonstration of glutamate-like immunoreactivity at rat neuromuscular junctions by quantitative electron microscopic immunocytochemistry. Anat Embryol 188:501-513.
82. Wang XH, Poo MM. 1997. Potentiation of developing synapses by postsynaptic release of neurotrophin-4. Neuron 19:825-835.
83. Yu MC, Cho E, Luo CB, Li WW, Shen WZ, Yew DT. 1996. Immunohistochemical studies of GABA and parvalbumin in the developing human cerebellum. Neuroscience 70:267-276.