Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles to the synapse

J.T. Littleton; H.J. Bellen; M.S. Perin

Summary

Synaptotagmin is a synaptic vesicle-specific integral membrane protein that has been suggested to play a key role in synaptic vesicle docking and fusion. By monitoring Synaptotagmin's cellular and subcellular distribution during development, it is possible to study synaptic vesicle localization and transport, and synapse formation. We have initiated the study of Synaptotagmin's expression during Drosophila neurogenesis in order to follow synaptic vesicle movement prior to and during synapse formation, as well as to localize synaptic sites in Drosophila. In situ hybridizations to whole-mount embryos show that synaptotagmin (syt) message is present in the cell bodies of all peripheral nervous system neurons and many, if not all, central nervous system neurons during neurite outgrowth and synapse formation, and in mature neurons. Immunocytochemical staining with antisera specific to Synaptotagmin indicates that the protein is present at all stages of the Drosophila life cycle following germ band retraction. In embryos, Synaptotagmin is only transiently localized to the cell body of neurons and is transported rapidly along axons during axonogenesis. After synapse formation, Synaptotagmin accumulates in a punctate pattern at all identifiable synaptic contact sites, suggesting a general role for Synaptotagmin in synapse function. In embryos and larvae, the most intense staining is found along two broad longitudinal tracts on the dorsal side of the ventral nerve cord and the brain, and at neuromuscular junctions in the periphery. In the adult head, Synaptotagmin localizes the discrete regions of the neurophil where synapses are predicted to occur. These data indicate that synaptic vesicles are present in axons before synapse formation, and become restricted to synaptic contact sites after synapses are formed. Since a similar expression pattern of Synaptotagmin has been reported in mammals, we propose that the function of Synaptotagmin and the mechanisms governing localization of the synaptic vesicle before and after synapse formation are conserved in invertebrate and vertebrate species. The ability to mark synapses in Drosophila should facilitate the study of synapse formation and function, providing a new tool to dissect the molecular mechanisms underlying these processes.

Reference

1. Bellen H.,
2. Kooyer S.,
3. D'Evelyn D.,
4. Pearlman J.
(1992) The Drosophila Couch potato protein is expressed in neural precursors and encodes nuclear proteins that contain RNA binding domains. Genes Dev 6, 2125–2136
OpenUrl Abstract/FREE Full Text
1. Bennett M. K.,
2. Calakos N.,
3. Scheller R. H.
(1992) Syntaxin- A synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257, 255–259
OpenUrl Abstract/FREE Full Text
1. Bodmer R.,
2. Carretto R.,
3. Jan Y. N.
(1989) Neurogenesis of the peripheral nervous system in Drosophila embryos: DNA replication patterns and cell lineages. Neuron 3, 21–32
OpenUrl CrossRef PubMed Web of Science
1. Broadie K. E.,
2. Bates M.
(1993) Development of the embryonic neuromuscular synapse of Drosophila melanogaster. J. Neurosci 13, 144–166
OpenUrl Abstract
1. Brose N.,
2. Petrenko A. G.,
3. Sudhof T. C.,
4. Jahn R.
(1992) Synaptotagmin- a calcium sensor on the synaptic vesicle surface. Science 256, 1021–1025
OpenUrl Abstract/FREE Full Text
1. Budnick V.,
2. Wu C.-F.,
3. White K.
(1989) Altered branching of serotonin-containing neurons in Drosophila mutants unable to synthesize serotonin and dopamine. J. Neurosci 9, 2866–2877
OpenUrl Abstract
1. Budnik V.,
2. Zhong Y.,
3. Wu C.-F.
(1990) Morphological plasticity of motor axons in Drosophila mutants with altered excitability. J. Neurosci 10, 3754–3768
OpenUrl Abstract
1. Costello W. J.,
2. Wyman R. J.
(1986) Development of an indirect flight muscle in a muscle-specific mutnat of Drosophila melanogaster. Dev. Biol 118, 247–258
OpenUrl CrossRef PubMed
1. Geppert M.,
2. Archer III B. T.,
3. Sudhof T. C.
(1991) Synaptotagmin II: A novel differentially distributed form of synaptotagmin. J. Biol. Chem 266, 13548–13552
OpenUrl Abstract/FREE Full Text
1. Han P.-L.,
2. Levin L. R.,
3. Reed R. R.,
4. Davis R. L.
(1992) Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron 9, 619–627
OpenUrl CrossRef PubMed Web of Science
1. Hortsch M.,
2. Bieber A. J.,
3. Patel N. H.,
4. Goodman C. S.
(1990) Differential splicing generates a nervous system-specific form of Drosophila neuroglian. Neuron 4, 697–709
OpenUrl CrossRef PubMed Web of Science
1. Hunter D. D.,
2. Shah V.,
3. Merlie J. P.,
4. Sanes J. R.
(1989) A laminin-like adhesive protein concentrated in the synaptic cleft of the neuromuscular junction. Nature 338, 229–234
OpenUrl CrossRef PubMed
1. Jan L. Y.,
2. Jan Y. N.
(1976) Properties of the larval neuromuscular junction in Drosophila melanogaster. J. Physiol 262, 189–214
OpenUrl PubMed Web of Science
1. Johansen J.,
2. Halpern M. E.,
3. Johansen K. M.,
4. Keshishian H.
(1989) Stereotypic morphology of glutamatergic synapses on identified muscle cells of Drosophila larvae. J. Neurosci 9, 710–25
OpenUrl Abstract
1. Johansen J.,
2. Halpern M. E.,
3. Keshishian H.
(1989) Axonal guidance and the development of muscle fiber-specific innervation in Drosophila embryos. J. Neurosci 9, 4318–32
OpenUrl Abstract
1. Koenig J. H.,
2. Kosaka T.,
3. Ikeda K.
(1989) The relationship between the number of synaptic vesicles and the amount of transmitter released. J. Neurosci 9, 1937–1942
OpenUrl Abstract
1. Leveque C.,
2. Hoshino T.,
3. David P.,
4. Shoji-Kasai Y.,
5. Leys K.,
6. Omori A.,
7. Lang B.,
8. El Far O.,
9. Sato K.,
10. Martin-Moutot N.,
11. Newsom-Davis J.,
12. Takahashi M.,
13. Seagar M. J.
(1992) The synaptic vesicle protein synaptotagmin associates with calcium channels and is a putative Lambert-Eaton myasthenic syndrome antigen. Proc. Natl. Acad. Sci. USA 89, 3625–3629
OpenUrl Abstract/FREE Full Text
1. Matteoli M.,
2. Takei K.,
3. Perin M. S.,
4. Sudhof T. C.,
5. DeCamilli P.
(1992) Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J. Cell Biol 117, 849–861
OpenUrl Abstract/FREE Full Text
1. Nose A.,
2. Mahajan B. B.,
3. Goodman C. S.
(1992) Connectin: a homophilic cell adhesion molecule expressed on a subset of muscles and the motoneurons that innervate them in Drosophila. Cell 70, 553–567
OpenUrl CrossRef PubMed Web of Science
1. Perin M. S.,
2. Fried V. A.,
3. Slaughter C. A.,
4. Sudhof T. C.
(1988) The structure of cytochrome b561, a secretory vesicle-specific electron transport protein. EMBO J 7, 2697–2703
OpenUrl PubMed Web of Science
1. Perin M. S.,
2. Fried V. A.,
3. Mignery G. A.,
4. Sudhof T. C.,
5. Jahn R.
(1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory domain of protein kinase C. Nature 345, 260–263
OpenUrl CrossRef PubMed Web of Science
1. Perin M. S.,
2. Archer B. T.,
3. Ozcelik T.,
4. Francke U.,
5. Jahn R.,
6. Sudhof T. C.
(1991) Structural and functional conservation of synaptotagmin (p65) in Drosophila and humans. J. Biol. Chem 266, 615–622
OpenUrl Abstract/FREE Full Text
1. Perin M. S.,
2. Brose N.,
3. Jahn R.,
4. Sudhof T. C.
(1991) Domain Structure of synaptotagmin (p65). J. Biol. Chem 266, 623–629
OpenUrl Abstract/FREE Full Text
1. Petrenko A. G.,
2. Perin M. S.,
3. Davletov B. A.,
4. Ushkaryov Y. A.,
5. Geppert M.,
6. Sudhof T. C.
(1991) Binding of synaptotagmin to the-latrotoxin receptor implicates both in synaptic vesicle exocytosis. Nature 353, 65–68
OpenUrl CrossRef PubMed Web of Science
1. Reichardt L. F.,
2. Tomaselli K. J.
(1991) Extracellular matrix molecules and their receptors: Functions in neural development. Annu. Rev. Neurosci 14, 531–570
OpenUrl CrossRef PubMed Web of Science
1. Reist N. E.,
2. Werle M. J.,
3. McMahan U. J.
(1992) Agrin released by motor neurons induces the aggregation of acetylcholine receptors at neuromuscular junctions. Neuron 8, 865–868
OpenUrl CrossRef PubMed Web of Science
1. Sink H.,
2. Whittington P. M.
(1991) Pathfinding in the central nervous system and periphery by identified embryonic Drosophila motor axons. Development 112, 307–316
OpenUrl Abstract
1. Sudhof T. C.,
2. Jahn F.
(1991) Proteins of synaptic vesicles involved in exocytosis and membrane recycling. Neuron 6, 665–677
OpenUrl CrossRef PubMed Web of Science
1. Tautz D.,
2. Pfeifle C.
(1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81–85
OpenUrl CrossRef PubMed Web of Science
1. Ushkaryov Y. A.,
2. Petrenko A. G.,
3. Geppert M.,
4. Sudhof T. C.
(1992) Neurexins: Synaptic cell surface proteins related to the-latrotoxin receptor and laminin. Science 257, 50–56
OpenUrl Abstract/FREE Full Text
1. Wendland B.,
2. Miller K. G.,
3. Schilling J.,
4. Scheller R. H.
(1991) Differential expression of the p65 gene family. Neuron 6, 993–1007
OpenUrl CrossRef PubMed Web of Science
1. Zinn K.,
2. McAllister L.,
3. Goodman C. S.
(1988) Sequence analysis and neuronal expression of Fasciclin I in grasshopper and Drosophila. Cell 53, 577–87
OpenUrl CrossRef PubMed Web of Science
1. Zipursky S. L.,
2. Venkatesh T. R.,
3. Benzer S.
(1985) From monoclonal antibody to gene for a neuron-specific glycoprotein in Drosophila. Proc. Natl. Acad. Sci. USA 82, 1855–1859
OpenUrl Abstract/FREE Full Text

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[1] Bellen H.,
Kooyer S.,
D'Evelyn D.,
Pearlman J.
(1992) The Drosophila Couch potato protein is expressed in neural precursors and encodes nuclear proteins that contain RNA binding domains. Genes Dev 6, 2125–2136
OpenUrl Abstract/FREE Full Text

[2] Bellen H.,

[3] Kooyer S.,

[4] D'Evelyn D.,

[5] Pearlman J.

[6] Bennett M. K.,
Calakos N.,
Scheller R. H.
(1992) Syntaxin- A synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257, 255–259
OpenUrl Abstract/FREE Full Text

[7] Bennett M. K.,

[8] Calakos N.,

[9] Scheller R. H.

[10] Bodmer R.,
Carretto R.,
Jan Y. N.
(1989) Neurogenesis of the peripheral nervous system in Drosophila embryos: DNA replication patterns and cell lineages. Neuron 3, 21–32
OpenUrl CrossRef PubMed Web of Science

[11] Bodmer R.,

[12] Carretto R.,

[13] Jan Y. N.

[14] Broadie K. E.,
Bates M.
(1993) Development of the embryonic neuromuscular synapse of Drosophila melanogaster. J. Neurosci 13, 144–166
OpenUrl Abstract

[15] Broadie K. E.,

[16] Bates M.

[17] Brose N.,
Petrenko A. G.,
Sudhof T. C.,
Jahn R.
(1992) Synaptotagmin- a calcium sensor on the synaptic vesicle surface. Science 256, 1021–1025
OpenUrl Abstract/FREE Full Text

[18] Brose N.,

[19] Petrenko A. G.,

[20] Sudhof T. C.,

[21] Jahn R.

[22] Budnick V.,
Wu C.-F.,
White K.
(1989) Altered branching of serotonin-containing neurons in Drosophila mutants unable to synthesize serotonin and dopamine. J. Neurosci 9, 2866–2877
OpenUrl Abstract

[23] Budnick V.,

[24] Wu C.-F.,

[25] White K.

[26] Budnik V.,
Zhong Y.,
Wu C.-F.
(1990) Morphological plasticity of motor axons in Drosophila mutants with altered excitability. J. Neurosci 10, 3754–3768
OpenUrl Abstract

[27] Budnik V.,

[28] Zhong Y.,

[29] Wu C.-F.

[30] Costello W. J.,
Wyman R. J.
(1986) Development of an indirect flight muscle in a muscle-specific mutnat of Drosophila melanogaster. Dev. Biol 118, 247–258
OpenUrl CrossRef PubMed

[31] Costello W. J.,

[32] Wyman R. J.

[33] Geppert M.,
Archer III B. T.,
Sudhof T. C.
(1991) Synaptotagmin II: A novel differentially distributed form of synaptotagmin. J. Biol. Chem 266, 13548–13552
OpenUrl Abstract/FREE Full Text

[34] Geppert M.,

[35] Archer III B. T.,

[36] Sudhof T. C.

[37] Han P.-L.,
Levin L. R.,
Reed R. R.,
Davis R. L.
(1992) Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron 9, 619–627
OpenUrl CrossRef PubMed Web of Science

[38] Han P.-L.,

[39] Levin L. R.,

[40] Reed R. R.,

[41] Davis R. L.

[42] Hortsch M.,
Bieber A. J.,
Patel N. H.,
Goodman C. S.
(1990) Differential splicing generates a nervous system-specific form of Drosophila neuroglian. Neuron 4, 697–709
OpenUrl CrossRef PubMed Web of Science

[43] Hortsch M.,

[44] Bieber A. J.,

[45] Patel N. H.,

[46] Goodman C. S.

[47] Hunter D. D.,
Shah V.,
Merlie J. P.,
Sanes J. R.
(1989) A laminin-like adhesive protein concentrated in the synaptic cleft of the neuromuscular junction. Nature 338, 229–234
OpenUrl CrossRef PubMed

[48] Hunter D. D.,

[49] Shah V.,

[50] Merlie J. P.,

[51] Sanes J. R.

[52] Jan L. Y.,
Jan Y. N.
(1976) Properties of the larval neuromuscular junction in Drosophila melanogaster. J. Physiol 262, 189–214
OpenUrl PubMed Web of Science

[53] Jan L. Y.,

[54] Jan Y. N.

[55] Johansen J.,
Halpern M. E.,
Johansen K. M.,
Keshishian H.
(1989) Stereotypic morphology of glutamatergic synapses on identified muscle cells of Drosophila larvae. J. Neurosci 9, 710–25
OpenUrl Abstract

[56] Johansen J.,

[57] Halpern M. E.,

[58] Johansen K. M.,

[59] Keshishian H.

[60] Johansen J.,
Halpern M. E.,
Keshishian H.
(1989) Axonal guidance and the development of muscle fiber-specific innervation in Drosophila embryos. J. Neurosci 9, 4318–32
OpenUrl Abstract

[61] Johansen J.,

[62] Halpern M. E.,

[63] Keshishian H.

[64] Koenig J. H.,
Kosaka T.,
Ikeda K.
(1989) The relationship between the number of synaptic vesicles and the amount of transmitter released. J. Neurosci 9, 1937–1942
OpenUrl Abstract

[65] Koenig J. H.,

[66] Kosaka T.,

[67] Ikeda K.

[68] Leveque C.,
Hoshino T.,
David P.,
Shoji-Kasai Y.,
Leys K.,
Omori A.,
Lang B.,
El Far O.,
Sato K.,
Martin-Moutot N.,
Newsom-Davis J.,
Takahashi M.,
Seagar M. J.
(1992) The synaptic vesicle protein synaptotagmin associates with calcium channels and is a putative Lambert-Eaton myasthenic syndrome antigen. Proc. Natl. Acad. Sci. USA 89, 3625–3629
OpenUrl Abstract/FREE Full Text

[69] Leveque C.,

[70] Hoshino T.,

[71] David P.,

[72] Shoji-Kasai Y.,

[73] Leys K.,

[74] Omori A.,

[75] Lang B.,

[76] El Far O.,

[77] Sato K.,

[78] Martin-Moutot N.,

[79] Newsom-Davis J.,

[80] Takahashi M.,

[81] Seagar M. J.

[82] Matteoli M.,
Takei K.,
Perin M. S.,
Sudhof T. C.,
DeCamilli P.
(1992) Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J. Cell Biol 117, 849–861
OpenUrl Abstract/FREE Full Text

[83] Matteoli M.,

[84] Takei K.,

[85] Perin M. S.,

[86] Sudhof T. C.,

[87] DeCamilli P.

[88] Nose A.,
Mahajan B. B.,
Goodman C. S.
(1992) Connectin: a homophilic cell adhesion molecule expressed on a subset of muscles and the motoneurons that innervate them in Drosophila. Cell 70, 553–567
OpenUrl CrossRef PubMed Web of Science

[89] Nose A.,

[90] Mahajan B. B.,

[91] Goodman C. S.

[92] Perin M. S.,
Fried V. A.,
Slaughter C. A.,
Sudhof T. C.
(1988) The structure of cytochrome b561, a secretory vesicle-specific electron transport protein. EMBO J 7, 2697–2703
OpenUrl PubMed Web of Science

[93] Perin M. S.,

[94] Fried V. A.,

[95] Slaughter C. A.,

[96] Sudhof T. C.

[97] Perin M. S.,
Fried V. A.,
Mignery G. A.,
Sudhof T. C.,
Jahn R.
(1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory domain of protein kinase C. Nature 345, 260–263
OpenUrl CrossRef PubMed Web of Science

[98] Perin M. S.,

[99] Fried V. A.,

[100] Mignery G. A.,

[101] Sudhof T. C.,

[102] Jahn R.

[103] Perin M. S.,
Archer B. T.,
Ozcelik T.,
Francke U.,
Jahn R.,
Sudhof T. C.
(1991) Structural and functional conservation of synaptotagmin (p65) in Drosophila and humans. J. Biol. Chem 266, 615–622
OpenUrl Abstract/FREE Full Text

[104] Perin M. S.,

[105] Archer B. T.,

[106] Ozcelik T.,

[107] Francke U.,

[108] Jahn R.,

[109] Sudhof T. C.

[110] Perin M. S.,
Brose N.,
Jahn R.,
Sudhof T. C.
(1991) Domain Structure of synaptotagmin (p65). J. Biol. Chem 266, 623–629
OpenUrl Abstract/FREE Full Text

[111] Perin M. S.,

[112] Brose N.,

[113] Jahn R.,

[114] Sudhof T. C.

[115] Petrenko A. G.,
Perin M. S.,
Davletov B. A.,
Ushkaryov Y. A.,
Geppert M.,
Sudhof T. C.
(1991) Binding of synaptotagmin to the-latrotoxin receptor implicates both in synaptic vesicle exocytosis. Nature 353, 65–68
OpenUrl CrossRef PubMed Web of Science

[116] Petrenko A. G.,

[117] Perin M. S.,

[118] Davletov B. A.,

[119] Ushkaryov Y. A.,

[120] Geppert M.,

[121] Sudhof T. C.

[122] Reichardt L. F.,
Tomaselli K. J.
(1991) Extracellular matrix molecules and their receptors: Functions in neural development. Annu. Rev. Neurosci 14, 531–570
OpenUrl CrossRef PubMed Web of Science

[123] Reichardt L. F.,

[124] Tomaselli K. J.

[125] Reist N. E.,
Werle M. J.,
McMahan U. J.
(1992) Agrin released by motor neurons induces the aggregation of acetylcholine receptors at neuromuscular junctions. Neuron 8, 865–868
OpenUrl CrossRef PubMed Web of Science

[126] Reist N. E.,

[127] Werle M. J.,

[128] McMahan U. J.

[129] Sink H.,
Whittington P. M.
(1991) Pathfinding in the central nervous system and periphery by identified embryonic Drosophila motor axons. Development 112, 307–316
OpenUrl Abstract

[130] Sink H.,

[131] Whittington P. M.

[132] Sudhof T. C.,
Jahn F.
(1991) Proteins of synaptic vesicles involved in exocytosis and membrane recycling. Neuron 6, 665–677
OpenUrl CrossRef PubMed Web of Science

[133] Sudhof T. C.,

[134] Jahn F.

[135] Tautz D.,
Pfeifle C.
(1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81–85
OpenUrl CrossRef PubMed Web of Science

[136] Tautz D.,

[137] Pfeifle C.

[138] Ushkaryov Y. A.,
Petrenko A. G.,
Geppert M.,
Sudhof T. C.
(1992) Neurexins: Synaptic cell surface proteins related to the-latrotoxin receptor and laminin. Science 257, 50–56
OpenUrl Abstract/FREE Full Text

[139] Ushkaryov Y. A.,

[140] Petrenko A. G.,

[141] Geppert M.,

[142] Sudhof T. C.

[143] Wendland B.,
Miller K. G.,
Schilling J.,
Scheller R. H.
(1991) Differential expression of the p65 gene family. Neuron 6, 993–1007
OpenUrl CrossRef PubMed Web of Science

[144] Wendland B.,

[145] Miller K. G.,

[146] Schilling J.,

[147] Scheller R. H.

[148] Zinn K.,
McAllister L.,
Goodman C. S.
(1988) Sequence analysis and neuronal expression of Fasciclin I in grasshopper and Drosophila. Cell 53, 577–87
OpenUrl CrossRef PubMed Web of Science

[149] Zinn K.,

[150] McAllister L.,

[151] Goodman C. S.

[152] Zipursky S. L.,
Venkatesh T. R.,
Benzer S.
(1985) From monoclonal antibody to gene for a neuron-specific glycoprotein in Drosophila. Proc. Natl. Acad. Sci. USA 82, 1855–1859
OpenUrl Abstract/FREE Full Text

[153] Zipursky S. L.,

[154] Venkatesh T. R.,

[155] Benzer S.

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The people behind the papers – George Britton and Aryeh Warmflash

Travelling Fellowship – New imaging approach unveils a bigger picture

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preLights – Self-organised symmetry breaking in zebrafish reveals feedback from morphogenesis to pattern formation

Spotlight – Can laboratory model systems instruct human limb regeneration?

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