Synaptotagmin I, synaptobrevin II, and syntaxin I are coexpressed in rat and gerbil pinealocytes

Cell and Tissue Research

Volumn 283, Issue 3, 1996, Pages 443-454

  Redecker, P ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Immunohistochemistry; Meriones unguiculatus (Rodentia); Pineal gland; Rat (Wistar, Lewis); S antigen; Synaptic like microvesicles; Synaptophysin; Synaptoporin

Indexed keywords

SYNAPTOBREVIN; SYNAPTOTAGMIN; SYNTAXIN;

ANIMAL TISSUE; ARTICLE; CELL VACUOLE; GERBIL; IMMUNOBLOTTING; IMMUNOGOLD STAINING; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NERVE ENDING; NONHUMAN; PINEALOCYTE; PRIORITY JOURNAL; RAT;

ANIMALS; ANTIGENS, SURFACE; CALCIUM-BINDING PROTEINS; GERBILLINAE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; NERVE TISSUE PROTEINS; PINEAL GLAND; R-SNARE PROTEINS; RATS; RATS, INBRED LEW; RATS, WISTAR; SYNAPTOTAGMIN I; SYNAPTOTAGMINS; SYNTAXIN 1;

EID: 0030030910     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004410050555     Document Type: Article

References (73)

1. Ahnert-Hilger G, Wiedenmann B (1992) The amphicrine pancreatic cell line, AR42J, secretes GABA and amylase by separate regulated pathways. FEBS Lett 314:41-44
2. Akagawa K, Barnstable CJ (1986) Identification and characterization of cell types in monolayer cultures of rat retina using monoclonal antibodies. Brain Res 383:110-120
3. Araki M, Nonaka T, Akagawa K, Kimura H, Mashiko T (1994) Developing rat pineal cells manifest potential of neuronal differentiation in vitro. Neurosci Res 20:57-69
4. Bauerfeind R, Régnier-Vigouroux A, Flatmark T, Huttner WB (1993) Selective storage of acetylcholine, but not catecholamines, in neuroendocrine synaptic-like microvesicles of early endosomal origin. Neuron 11:105-121
5. Baumert M, Maycox PR, Navone F, De Camilli P, Jahn R (1989) Synaptobrevin: an integral membrane protein of 18 000 daltons present in small synaptic vesicles of rat brain. EMBO J 8:379-384
6. Bennet MK, Calakos N, Scheller RH (1992) Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257:255-259
7. Braun JEA, Fritz BA, Wong SME, Lowe AW (1994) Identification of a vesicle-associated membrane protein (VAMP)-like membrane protein in zymogen granules of the rat exocrine pancreas. J Biol Chem 269:5328-5335
8. Broadie K, Bellen HJ, Di Antonio A, Littleton JT, Schwarz TL (1994) Absence of synaptotagmin disrupts excitation-secretion coupling during synaptic transmission. Proc Natl Acad Sci USA 91:10727-10731
9. Brose N, Petrenko AG, Südhof TC, Jahn R (1992) Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science 256:1021-1025
10. Buckley KM (1994) Molecular analysis of a secretory organelle: structure and function of synaptic vesicle-specific proteins. J Membrane Biol 139:75-80
11. Craxton M, Goedert M (1995) Synaptotagmin V: a novel synaptotagmin isoform expressed in rat brain. FEBS Lett 361: 196-200
12. De Camilli P (1994) Co-secretion of multiple signal molecules from endocrine cells via distinct exocytotic pathways. Trends Pharmacol Sci 12:446-448
13. Edelmann L, Hanson PI, Chapman ER, Jahn R (1995) Synaptobrevin binding to synaptophysin: a potential mechanism for controlling the exocytotic fusion machine. EMBO J 14: 224-231
14. Elferink LA, Trimble WS, Scheller RH (1989) Two vesicle-associated membrane protein genes are differentially expressed in the rat central nervous system. J Biol Chem 264:11061-11064
15. Ferro-Novick S, Jahn R (1994) Vesicle fusion from yeast to man. Nature 370:191-193
16. Fykse EM, Takei K, Walch-Solimena C, Geppert M, Jahn R, De Camilli P, Südhof TC (1993) Relative properties and localizations of synaptic vesicle protein isoforms: the case of the synaptophysins. J Neurosci 13:4997-5007
17. Geppert M, Archer BTI, Südhof TC (1991) Synaptotagmin II. A novel differentially distributed form of synaptotagmin. J Biol Chem 266:13548-13552
18. 2+ sensor for transmitter release at a central synapse. Cell 79:717-727
19. Gilerovitch HG, Bishop GA, King JS, Burry RW (1995) The use of electron microscopic immunocytochemistry with silver-enhanced 1.4-nm gold particles to localize GAD in the cerebellar nuclei. J Histochem Cytochem 43:337-343
20. Grube D, Kusumoto Y (1986) Serial semithin sections in immunohistochemistry: techniques and applications. Arch Histol Jpn 49:391-410
21. Honer WG, Hu L, Davies P ( 1993) Human synaptic proteins with a heterogeneous distribution in cerebellum and visual cortex. Brain Res 609:9-20
22. Hsu S-M, Raine L, Fanger H (1981) Use of avidin-biotin peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabelled antibody PAP procedures. J Histochem Cytochem 27:577-580
23. Huang S-K, Klein DC, Korf H-W (1992) Immunocytochemical demonstration of rod-opsin, S-antigen, and neuron-specific proteins in the human pineal gland. Cell Tissue Res 267: 493-498
24. Inoue A, Akagawa K (1992) Neuron-specific antigen HPC-1 from bovine brain reveals strong homology to epimorphin, an essential factor involved in epithelial morphogenesis: identification of a novel protein family. Biochem Biophys Res Commun 187:1144-1150
25. Inoue A, Obata K, Akagawa K (1992) Cloning and sequence analysis of cDNA for a neuronal cell membrane antigen, HPC-1. J Biol Chem 267:10613-10619
26. Jacobsson G, Bean AJ, Scheller RH, Juntti-Berggren L, Deeney JT, Berggren P-O, Meister B (1994) Identification of synaptic proteins and their isoform mRNAs in compartments of pancreatic endocrine cells. Proc Natl Acad Sci USA 91: 12487-12491
27. Jahn R, Südhof TC (1994) Synaptic vesicles and exocytosis. Annu Rev Neurosci 17:219-246
28. Jahn R, Schiebler W, Ouimet C, Greengard P (1985) A 38 000-dalton membrane protein (p38) present in synaptic vesicles. Proc Natl Acad Sci USA 82:4137-4141
29. Kalsow CM, Wacker WB (1977) Pineal reactivity of anti-retina sera. Invest Ophthalmol Visual Sci 16:181-184
30. Knaus P, Marquèze-Pouey B, Scherer H, Betz H (1990) Synaptoporin, a novel putative channel protein of synaptic vesicles. Neuron 5:453-462
31. Koh S, Yamamoto A, Inoue A, Inoue Y, Akagawa K, Kawamura Y, Kawamoto K, Tashiro Y (1993) Immunoelectron microscopic localization of the HPC-1 antigen in rat cerebellum. J Neurocytol 22:995-1005
32. Korf H-W, Møller M, Gery I, Zigler JS, Klein DC (1985) Immunocytochemical demonstration of retinal S-antigen in the pineal organ of four mammalian species. Cell Tissue Res 239:81-85
33. Korf H-W, Oksche A, Ekström P, Gery I, Zigler JS Jr, Klein DC (1986) Pinealocyte projections into the mammalian brain revealed with S-antigen antiserum. Science 231:735-737
34. Korf H-W, Sato T, Oksche A (1990) Complex relationships between the pineal organ and the medial habenular nucleus-pretectal region of the mouse as revealed by S-antigen immunocytochemistry. Cell Tissue Res 261:493-500
35. Lah JL, Burry RW (1993) Neuronotypic differentiation results in reduced levels and altered distribution of synaptophysin in PC 12 cells. J Neurochem 60:503-512
36. Marquèze-Pouey B, Wisden W, Malosio ML, Betz H (1991) Differential expression of synaptophysin and synaptoporin mRNAs in the postnatal rat central nervous system. J Neurosci 11:3388-3397
37. Mc Mahon HT, Ushkaryov YA, Edelmann L, Link E, Binz T, Niemann H, Jahn R, Südhof TC (1993) Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein. Nature 364:346-349
38. Mizuta M, Inagaki N, Nemoto Y, Matsukura S, Takahashi M, Seino S (1994) Synaptotagmin III is a novel isoform of rat synaptotagmin expressed in endocrine and neuronal cells. J Biol Chem 269:11675-11678
39. Moriyama Y, Yamamoto A (1995) Microvesicles isolated from bovine pineal gland specifically accumulate L-glutamate. FEBS Lett 367:233-236
40. Mundigl O, Matteoli M, Daniell L, Thomas-Reetz A, Metcalf A, Jahn R, De Camilli P (1994) Synaptic vesicle proteins and early endosomes in cultured hippocampal neurons: differential effects of Brefeldin A in axon and dendrites. J Cell Biol 122:1207-1221
41. Navone F, Jahn R, Di Gioia G, Stukenbrok H, Greengard P, De Camilli P (1986) Protein p38: an integral membrane protein specific for small vesicles of neurons and neuroendocrine cells. J Cell Biol 103:2511-2527
42. O'Connor V, Augustine GJ, Betz H (1994) Synaptic vesicle exocytosis: molecules and models. Cell 76:785-787
43. Oho C, Seino S, Takahashi M (1995) Expression and complex formation of soluble N-ethyl-maleimide-sensitive factor attachment protein (SNAP) receptors in clonal rat endocrine cells. Neurosci Lett 186:208-210
44. Perin MS, Fried VA, Mignery GA, Jahn R, Südhof TC (1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory domain of protein kinase C. Nature 345:260-263
45. Pevsner J, Scheller RH (1994) Mechanisms of vesicle docking and fusion: insights from the nervous system. Curr Opin Cell Biol 6:555-560
46. Phend KD, Rustioni A, Weinberg RJ (1995) An osmium-free method of Epon embedment that preserves both ultrastructure and antigenicity for post-embedding immunocytochemistry. J Histochem Cytochem 43:283-292
47. Ralston E, Beushausen S, Ploug T (1994) Expression of the synaptic vesicle proteins VAMPs/synaptobrevins 1 and 2 in non-neural tissues. J Biol Chem 269:15403-15406
48. Redecker P (1993) Dense accumulations of synaptic-like microvesicles in 'dark' pinealocytes of the gerbil pineal gland. J Neurocytol 22:572-581
49. Redecker P (1995) The ras-like rab3A protein is present in pinealocytes of the gerbil pineal gland. Neurosci Lett 184:117-120
50. Redecker P, Bargsten G (1993) Synaptophysin - a common constituent of presumptive secretory microvesicles in the mammalian pinealocyte: a study of rat and gerbil pineal glands. J Neurosci Res 34:79-96
51. Redecker P, Veh RW (1994) Glutamate immunoreactivity is enriched over pinealocytes of the gerbil pineal gland. Cell Tissue Res 278:579-588
52. Redecker P, Grube D, Jahn R (1990) Immunohistochemical localization of synaptophysin (p38) in the pineal gland of the Mongolian gerbil (Meriones unguiculatus). Anat Embryol 181: 433-440
53. Reetz A, Solimena M, Matteoli M, Folli F, Takei K, De Camilli P (1991) GABA and pancreatic β-cells: colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion. EMBO J 10:1275-1284
54. Schägger H, Jagow G von (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166: 368-379
55. Schomerus C, Ruth P, Korf H-W (1994) Photoreceptor-specific proteins in the mammalian pineal organ: immunocytochemical data and functional considerations. Acta Neurobiol Exp 54[Suppl]:9-17
56. Söllner T, Rothman JE (1994) Neurotransmission: harnessing fusion machinery at the synapse. Trends Neurosci 17:344-348
57. Söllner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362: 318-324
58. Sternberger LA (1986) Immunocytochemistry, 3rd edn. Wiley, New York
59. Südhof TC, Baumert M, Perin MS, Jahn R (1989) A synaptic vesicle membrane protein is conserved from mammals to Drosophila. Neuron 2:1475-1481
60. Tagaya M, Toyonaga S, Takahashi M, Yamamoto A, Fujiwara T, Akagawa K, Moriyama Y, Mizushima S (1995) Syntaxin I (HPC-1) is associated with chromaffin granules. J Biol Chem 270:15930-15933
61. Thomas-Reetz AC, De Camilli P (1994) A role for synaptic vesicles in non-neuronal cells: clues from pancreatic β cells and from chromaffin cells. FASEB J 8:209-216
62. Thomas-Reetz A, Hell JW, During MJ, Walch-Solimena C, Jahn R, De Camilli P (1994) A γ-aminobutyric acid transporter driven by a proton pump is present in synaptic-like microvesicles of pancreatic β-cells. Proc Natl Acad Sci USA 90:5317-5321
63. Trimble WS, Cowan DM, Scheller RH (1988) VAMP-1: a synaptic vesicle-associated integral membrane protein. Proc Natl Acad Sci USA 85:4538-4542
64. Trimble WS, Gray TS, Elferink LA, Wilson MC, Scheller RH (1990) Distinct patterns of expression of two VAMP genes within the rat brain. J Neurosci 10:1380-1387
65. Ullrich B, Südhof TC (1994) Distribution of synaptic markers in the retina: implications for synaptic vesicle traffic in ribbon synapses. J Physiol (Lond) 88:249-257
66. Van Veen T, Elofsson R, Hartwig HG, Gery I, Mochizuki M, Cena V, Klein DC (1986) Retinal S-antigen: immunocytochemical and immunochemical studies on distribution in animal photoreceptors and pineal organs. Exp Biol 45:15-25
67. Vollrath L (1981) The pineal organ. In: Oksche A, Vollrath L (eds) Handbuch der mikroskopischen Anatomie des Menschen, vol VI/7. Springer, Berlin Heidelberg New York
68. Vollrath L, Schröder H (1987) Neuronal properties of mammalian pinealocytes? In: Trentini GP, Gaetani C de, Pévet P (eds) Fundamentals and clinics in pineal research, vol 44. Raven, New York, pp 13-23
69. Walch-Solimena C, Blasi J, Edelmann L, Chapman ER, Fischer von Mollard G, Jahn R (1995) The t-SNAREs syntaxin 1 and SNAP-25 are present on organelles that participate in synaptic vesicle recycling. J Cell Biol 128:637-645
70. Welsh MG, Reiter RJ (1978) The pineal gland of the gerbil, Meriones unguiculatus. I. An ultrastructural study. Cell Tissue Res 193:323-336
71. Wendland B, Miller KG, Schilling J, Scheller RH (1991) Differential expression of the p65 gene family. Neuron 6:993-1007
72. Wessel D, Flügge UI (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138:141-142
73. Yoshida A, Oho C, Omori A, Kuwahara R, Ito T, Takahashi M (1992) HPC-1 is associated with synaptotagmin and ω-conotoxin receptor. J Biol Chem 267:24925-24928