Tetanus neurotoxin-insensitive vesicle-associated membrane protein localizes to a presynaptic membrane compartment in selected terminal subsets of the rat brain

Neuroscience

Volumn 122, Issue 1, 2003, Pages 59-75

  Muzerelle, A ^a   Alberts, P ^b   Martinez Arca, S ^b   Jeannequin, O ^c   Lafaye, P ^c   Mazie J C ^c   Galli, T ^b   Gaspar, P ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b INSERM   (France)

^c INSTITUT PASTEUR   (France)

Author keywords

Exocytosis; Membrane trafficking; Mossy fibre; Nerve terminal; SNARE; TI VAMP

Indexed keywords

BIOLOGICAL MARKER; METENKEPHALIN; NEUROPEPTIDE; NEUROTOXIN; NEUROTRANSMITTER; SYNAPTOBREVIN; SYNAPTOPHYSIN;

ADULTHOOD; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; FEMALE; GABAERGIC SYSTEM; GLOBUS PALLIDUS; HIPPOCAMPUS; IMMUNOREACTIVITY; MOSSY FIBER; NERVE ENDING; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; RAT; SPINAL CORD DORSAL HORN; SUBSTANTIA NIGRA; SYNAPSE VESICLE;

EID: 0037800946     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(03)00567-0     Document Type: Article

References (57)

1. Advani R.J., Yang B., Prekeris R., Lee K.C., Klumperman J., Scheller R.H. VAMP-7 mediates vesicular transport from endosomes to lysosomes. J Cell Biol. 146:1999;765-775.
2. Alberts P, Rudge RE, Hinners I, Muzerelle A, Martinez-Arca S, Irinopoulou T, Martiens V, Tooze S, Rathjen F, Gaspar P, Galli, T (2003) Cross-talk between tetanus neurotoxin-insensitive vesicle-associated membrane protein-mediated transport and L1-mediated adhesion. Mol Biol Cell, in press.
3. Alheid G., Do Olmos J.S., Beltramino C.A. Amygdala and extended amygdala. Paxinos G. The rat nervous system. 1995;495-578 Academic Press, New York.
4. Amaral D.G., Dent J.A. Development of the mossy fibers of the dentate gyrus I. A light and electron microscopic study of the mossy fibers and their expansions . J Comp Neurol. 195:1981;51-86.
5. Anglade P., Tsuji S., Javoy-Agid F., Agid Y., Hirsch E.C. Plasticity of nerve afferents to nigrostriatal neurons in Parkinson's disease. Ann Neurol. 37:1995;265-272.
6. Ben-Ari Y., Represa A. Brief seizure episodes induce long-term potentiation and mossy fibre sprouting in the hippocampus. Trends Neurosci. 13:1990;312-318.
7. Blasi J., Chapman E.R., Link E., Binz T., Yamasaki S., De Camilli P., Südhof T.C., Niemann H., Jahn R. Botulinum neurotoxin A selectively cleaves the synaptic protein SNAP-25. Nature. 365:1993;160-163.
8. Bogdanovic A, Bennett N, Kieffer S, Louwagie M, Morio T, Garin J, Satre M, Bruckert F (2002) Syntaxin 7, Syntaxin 8, Vti1 and VAMP7 form an active SNARE complex for early macropinocytic compartment fusion in Dictyostelium discoideum. Biochem J 368:29-39.
9. Broman J., Anderson S., Ottersen O.P. Enrichment of glutamate-like immunoreactivity in primary afferent terminals throughout the spinal cord dorsal horn. Eur J Neurosci. 5:1993;1050-1061.
10. Broutman G., Baudry M. Involvement of the secretory pathway for AMPA receptors in NMDA-induced potentiation in hippocampus. J Neurosci. 21:2001;27-34.
11. Cameron H.A., McKay R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol. 435:2001;406-417.
12. Castillo P.E., Salin P.A., Weisskopf M.G., Nicoll R.A. Characterizing the site and mode of action of dynorphin at hippocampal mossy fiber synapses in the guinea pig. J Neurosci. 16:1996;5942-5950.
13. Chicurel M.E., Harris K.M. Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. J Comp Neurol. 325:1992;169-182.
14. Coco S., Raposo G., Martinez S., Fontaine J.J., Takamori S., Zahraoui A., Jahn R., Matteoli M., Louvard D., Galli T. Subcellular localization of tetanus neurotoxin-insensitive vesicle-associated membrane protein (VAMP)/VAMP7 in neuronal cells evidence for a novel membrane compartment . J Neurosci. 19:1999;9803-9812.
15. Dumoulin A., Rostaing P., Bedet C., Levi S., Isambert M.F., Henry J.P., Triller A., Gasnier B. Presence of the vesicular inhibitory amino acid transporter in GABAergic and glycinergic synaptic terminal boutons. J Cell Sci. 112:(Pt 6):1999;811-823.
16. Edelmann L., Hanson P.I., Chapman E.R., Jahn R. Synaptobrevin binding to synaptophysin a potential mechanism for controlling the exocytotic fusion machine . EMBO J. 14:1995;224-231.
17. Fox C.A., Andrade A.N., Lu Qui I.J., Rafols J.A. The primate globus pallidus a Golgi and electron microscopic study . J Hirnforsch. 15:1974;75-93.
18. Gall C., Brecha N., Karten H.J., Chang K.J. Localization of enkephalin-like immunoreactivity to identified axonal and neuronal populations of the rat hippocampus. J Comp Neurol. 198:1981;335-350.
19. Gall C.M., Pico R.M., Lauterborn J.C. Focal hippocampal lesions induce seizures and long-lasting changes in mossy fiber enkephalin and CCK immunoreactivity. Peptides. 9:(Suppl 1):1988;179-184.
20. Galli T, Haucke V (2001) Cycling of synaptic vesicles: how far? How fast! Sci STKE. RE1.
21. Galli T., Zahraoui A., Vaidyanathan V.V., Raposo G., Tian J.M., Karin M., Niemann H., Louvard D. A novel tetanus neurotoxin-insensitive vesicle-associated membrane protein in SNARE complexes of the apical plasma membrane of epithelial cells. Mol Biol Cell. 9:1998;1437-1448.
22. Gaspar P., Berger B., Gay M., Hamon M., Cesselin F., Vigny A., Javoy-Agid F., Agid Y. Tyrosine hydroxylase and methionine-enkephalin in the human mesencephalon immunocytochemical localization and relationships . J Neurol Sci. 58:1983;247-267.
23. Gaspar P., Berger B., Lesur A., Borsotti J.P., Febvret A. Somatostatin 28 and neuropeptide Y innervation in the septal area and related cortical and subcortical structures of the human brain distribution, relationships and evidence for differential coexistence . Neuroscience. 22:1987;49-73.
24. Grofova I., Rinvik E. An experimental electron microscopic study on the striatonigral projection in the cat. Exp Brain Res. 11:1970;249-262.
25. Grosse G., Grosse J., Tapp R., Kuchinke J., Gorsleben M., Fetter I., HohneZell B., Gratzl M., Bergmann M. SNAP-25 requirement for dendritic growth of hippocampal neurons. J Neurosci Res. 56:1999;539-546.
26. Grosshans D.R., Clayton D.A., Coultrap S.J., Browning M.D. LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1. Nat Neurosci. 5:2002;27-33.
27. Haber S.N., Nauta W.J. Ramifications of the globus pallidus in the rat as indicated by patterns of immunohistochemistry. Neuroscience. 9:1983;245-260.
28. Harlow E, Lane D (1988) Antibodies: a laboratory manual. Cold Spring Harbor Laboratory.
29. Herzog E., Bellenchi G.C., Gras C., Bernard V., Ravassard P., Bedet C., Gasnier B., Giros B., El Mestikawy S. The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J Neurosci. 21:2001;RC181.
30. Hibi T., Hirashima N., Nakanishi M. Rat basophilic leukemia cells express syntaxin-3 and VAMP-7 in granule membranes. Biochem Biophys Res Commun. 271:2000;36-41.
31. Hunt S.P., Kelly J.S., Emson P.C., Kimmel J.R., Miller R.J., Wu J.Y. An immunohistochemical study of neuronal populations containing neuropeptides or gamma-aminobutyrate within the superficial layers of the rat dorsal horn. Neuroscience. 6:1981;1883-1898.
32. Ingham C.A., Hood S.H., van Maldegem B., Weenink A., Arbuthnott G.W. Morphological changes in the rat neostriatum after unilateral 6-hydroxydopamine injections into the nigrostriatal pathway. Exp Brain Res. 93:1993;17-27.
33. Kantheti P., Qiao X., Diaz M.E., Peden A.A., Meyer G.E., Carskadon S.L., Kapfhamer D., Sufalko D., Robinson M.S., Noebels J.L., Burmeister M. Mutation in AP-3 delta in the mocha mouse links endosomal transport to storage deficiency in platelets, melanosomes, and synaptic vesicles. Neuron. 21:1998;111-122.
34. Lafont F., Verkade P., Galli T., Wimmer C., Louvard D., Simons K. Raft association of SNAP receptors acting in apical trafficking in Madin-Darby canine kidney cells. Proc Natl Acad Sci USA. 96:1999;3734-3738.
35. Lan J.Y., Skeberdis V.A., Jover T., Grooms S.Y., Lin Y., Araneda R.C., Zheng X., Bennett M.V., Zukin R.S. Protein kinase C modulates NMDA receptor trafficking and gating. Nat Neurosci. 4:2001;382-390.
36. Laurberg S., Zimmer J. Lesion-induced sprouting of hippocampal mossy fiber collaterals to the fascia dentata in developing and adult rats. J Comp Neurol. 200:1981;433-459.
37. Li J.L., Fujiyama F., Kaneko T., Mizuno N. Expression of vesicular glutamate transporters, VGluT1 and VGluT2, in axon terminals of nociceptive primary afferent fibers in the superficial layers of the medullary and spinal dorsal horns of the rat. J Comp Neurol. 457:2003;236-249.
38. Martinez-Arca S., Alberts P., Zahraoui A., Louvard D., Galli T. Role of tetanus neurotoxin insensitive vesicle-associated membrane protein (TI-VAMP) in vesicular transport mediating neurite outgrowth. J Cell Biol. 149:2000;889-899.
39. Martinez-Arca S., Coco S., Mainguy G., Schenk U., Alberts P., Bouille P., Mezzina M., Prochiantz A., Matteoli M., Louvard D., Galli T. A common exocytotic mechanism mediates axonal and dendritic outgrowth. J Neurosci. 21:2001;3830-3838.
40. Martinez-Arca S, Rudge RE, Vacca M, Camonis J, Daviet L, Formstecher E, Hamburger A, Filippini F, D'Esposito M, Galli T (2003) A dual mechanism controlling the localization and function of exocytic v-SNAREs. Proc Natl Acad Sci USA 100:9011-9016.
41. Osen-Sand A., Staple J.K., Naldi E., Schiavo G., Rossetto O., Petitpierre S., Malgaroli A., Montecucco C., Catsicas S. Common and distinct fusion proteins in axonal growth and transmitter release. J Comp Neurol. 367:1996;222-234.
42. Pierce J.P., Kurucz O.S., Milner T.A. Morphometry of a peptidergic transmitter system dynorphin B-like immunoreactivity in the rat hippocampal mossy fiber pathway before and after seizures . Hippocampus. 9:1999;255-276.
43. Renger J.J., Egles C., Liu G. A developmental switch in neurotransmitter flux enhances synaptic efficacy by affecting AMPA receptor activation. Neuron. 29:2001;469-484.
44. Ribeiro-da-Silva A., Coimbra A. Two types of synaptic glomeruli and their distribution in laminae I-III of the rat spinal cord. J Comp Neurol. 209:1982;176-186.
45. Rothman J.E. The machinery and principles of vesicle transport in the cell. Nat Med. 8:2002;1059-1062.
46. Salem N., Faundez V., Horng J.T., Kelly R.B. A v-SNARE participates in synaptic vesicle formation mediated by the AP3 adaptor complex. Nat Neurosci. 1:1998;551-556.
47. Schagger H., von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem. 166:1987;368-379.
48. Schoch S., Deak F., Konigstorfer A., Mozhayeva M., Sara Y., Sudhof T.C., Kavalali E.T. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science. 294:2001;1117-1122.
49. Seaberg R.M., van der Kooy D. Adult rodent neurogenic regions the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors . J Neurosci. 22:2002;1784-1793.
50. Soares S., von Boxberg Y., Lombard M.C., Ravaille-Veron M., Fischer I., Eyer J., Nothias F. Phosphorylated MAP1B is induced in central sprouting of primary afferents in response to peripheral injury but not in response to rhizotomy. Eur J Neurosci. 16:2002;593-606.
51. Song H.J., Stevens C.F., Gage F.H. Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci. 5:2002;438-445.
52. Sutula T., Zhang P., Lynch M., Sayin U., Golarai G., Rod R. Synaptic and axonal remodeling of mossy fibers in the hilus and supragranular region of the dentate gyrus in kainate-treated rats. J Comp Neurol. 390:1998;578-594.
53. Verhage M., Maia A.S., Plomp J.J., Brussaard A.B., Heeroma J.H., Vermeer H., Toonen R.F., Hammer R.E., vandenBerg T.K., Missler M., Geuze H.J., Sudhof T.C. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science. 287:2000;864-869.
54. Ward D.M., Pevsner J., Scullion M.A., Vaughn M., Kaplan J. Syntaxin 7 and VAMP-7 are soluble N-ethylmaleimide-sensitive factor attachment protein receptors required for late endosome-lysosome and homotypic lysosome fusion in alveolar macrophages. Mol Biol Cell. 11:2000;2327-2333.
55. Washbourne P., Thompson P.M., Carta M., Costa E.T., Mathews J.R., Lopez-Bendito G., Molnar Z., Becher M.W., Valenzuela C.F., Partridge L.D., Wilson M.C. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat Neurosci. 5:2002;19-26.
56. Zalutsky R.A., Nicoll R.A. Comparison of two forms of long-term potentiation in single hippocampal neurons. Science. 248:1990;1619-1624.
57. Zhang L.X., Volknandt W., Gundelfinger E.D., Zimmermann H. A comparison of synaptic protein localization in hippocampal mossy fiber terminals and neurosecretory endings of the neurohypophysis using the cryo-immunogold technique. J Neurocytol. 29:2000;19-30.