Abstract
In this brief review we have attempted to highlight the core principles and mechanism of regulated exocytosis and highlight some of the key questions and opportunities for analysis of the vesicle lifecycle in dendrites. Many questions remain: how are secretory vesicles targeted to dendrites? Does local vesicle biogenesis or recycling occur in dendrites? Do functionally distinct vesicle pools reside in the dendrite? Are secretory vesicles docked at active zones with distinct Ca2+ channels in dendrites? Are SVs and LDCVs differentially targeted and regulated in dendrites? How is vesicle priming and recycling controlled? We are entering a fascinating period in which many key molecular, biochemical, imaging, biophysical and bioinformatics tools can be assembled to allow functional analysis of dendritic release and forge the framework to understand the integrative function of dendritic retrograde signalling in health & disease.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
Similar content being viewed by others
7. References
Alés, E., Tabares, L., Poyato, J. M., Valero, V., Lindau, M., and Alvarez de Toledo, G., 1999, High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism, Nat. Cell. Biol. 1: 40.
Araneda, R., and Bustos, G., 1989, Modulation of dendritic release of dopamine by N-Methyl-D-Aspartate receptors in rat substantia nigra, J. Neurochem. 52: 962.
Archer, D. A., Graham, M. E., and Burgoyne, R. D., 2002, Complexin regulates the closure of the fusion pore during regulated vesicle exocytosis, J. Biol. Chem. 277: 18249.
Aridor, M., Guzik, A. K., Bielli, A., and Fish, K. N., 2004, Endoplasmic reticulum export site formation and function in dendrites, J. Neurosci. 24:3770.
Attwell, D., Barbour, B., and Szatkowski, M., 1993, Nonvesicular release of transmitter, Neuron. 11: 401.
Bains, J. S., and Ferguson, A. V., 1999, Activation of N-methyl-D-aspartate receptors evokes calcium spikes in the dendrites of rat hypothalamic paraventricular nucleus neurons, Neuroscience 90: 885.
Barg, S., 2003, Mechanisms of exocytosis in insulin-secreting β-cells and glucagon-secreting α-cells, Pharm. Toxicol. 92: 3.
Bayer, M. J., Reese, C., Bühler, S., Peters, C., and Mayer, A., 2003, Vacuole membrane fusion: Vo functions after trans-SNARE pairing and is coupled to the Ca2+-releasing channel, J. Cell Biol. 162: 211.
Bergquist, F., Niazi, H. S., and Nissbrandt, H., 2002, Evidence for different exocytosis pathways in dendritic and terminal dopamine release in vivo, Brain Res. 950: 245.
Brose, N., Petrenko, A. G., Sudhof, T. C., and Jahn, R., 1992, Synaptotagmin: a calcium sensor on the synaptic vesicle surface, Science 256: 1021.
Brose, N., and Rosenmund, C., 2002, Move over, protein kinase C, you’ve got company: alternative cellular effectors of diacylglycerol and phorbol esters, J. Cell Sci. 115: 4399.
Burack, M. A., Silverman, M. A., and Banker, G., 2000, The role of selective transport in neuronal protein sorting, Neuron 26: 465.
Burgoyne, R. D., and Morgan, A., 2003, Secretory granule exocytosis, Phys. Rev. 83: 581
Chen, B. T., and Rice, M. E., 2001, Novel Ca2+ dependence and time course of somatodendritic dopamine release: Substantia nigra versus striatum, J. Neurosci. 21: 7841.
Chevaleyre, V., Dayanithi, G., Moos, F. C., and Desarmenien, M. G., 2000, Developmental regulation of a local positive autocontrol of supraoptic neurons, J. Neurosci. 20: 5813.
Cousin, M. A., and Robinson, P. J., 2001, The dephosphins: dephosphorylation by calcineurin triggers synaptic vesicle endocytosis, Trends Neurosci. 24: 659.
Duncan, R. R., Greaves, J., Wiegand, U. K., Matskevich, I., Bodammer, G., Apps, D. K., Shipston, M. J., and Chow, R. H., 2003, Functional and spatial segregration of secretory vesicle pools according to vesicle age, Nature 422: 176.
Falkenburger, B. H., Barstow, K. L., and Mintz, I. M., 2001, Dendrodendritic inhibition through reversal of dopamine transport, Science 293: 2465.
Fernández-Chacón, R., Königstorfer, A., Gerber, S. H., García, J., Matos, M. F., Stevens, C. F., Brose, N., Rizo, J., Rosenmund, C., and Südhof, T. C., 2001, Synaptotagmin I functions as a calcium regulator of release probability, Nature 410: 41.
Fesce, R., Grohovaz, F., Valtorta, F., and Meldolesi, J., 1994, Transmitter release: Fusion or “kiss-and-run”?, Trends Cell Biol. 4: 1.
Fisher, T. E., and Bourque, C. W., 1996, Calcium-channel subtypes in the somata and axon terminals of magnocellular neurosecretory cells, Trends Neurosci. 19: 440.
Fisher, T. E., and Bourque, C. W., 2001, The function of Ca2+ channel subtypes in exocytotic secretion: new perspectives from synaptic and non-synaptic release, Prog. Biophys. Mol. Biol. 77: 269.
Foehring, R. C., and Armstrong, W. E., 1996, Pharmacological dissection of high-voltage-activated Ca2+ current types in acutely dissociated rat supraoptic magnocellular neurons, J. Neurophysiol. 76: 977.
Ford, M. G., Mills, I. G., Peter, B. J., Vallis, Y., Praefcke, G. J., Evans, P. R., and McMahon, H. T., 2002, Curvature of clathrin-coated pits driven by epsin, Nature 419: 361.
Gallwitz, D., and Jahn, R., 2003, The riddle of the Sec1/Munc-18 proteins-new twists added to their interactions with SNAREs, Trends Biochem. Sci. 28: 113.
Gandhi, S. P., and Stevens, C. F., 2003, Three modes of synaptic vesicular recycling revealed by single-vesicle imaging, Nature 423: 607.
Grishanin, R. N., Klenchin, V. A., Loyet, K. M., Kowalchyk, J. A., Ann, K., and Martin, T. F., 2002, Membrane association domains in Ca2+-dependent activator protein for secretion mediate plasma membrane and dense-core vesicle binding required for Ca2+-dependent exocytosis, J. Biol. Chem. 277: 22025.
Han, X., Wang, C-T., Bai, J., Chapman, E. R., and Jackson, M. B., 2004, Transmembrane segments of syntaxin line the fusion pore of Ca2+-triggered exocytosis, Science 304: 289.
Harata, N., Pyle, J. L., Aravanis, A. M., Mozhayeva, M., Kavalali, E. T., and Tsien, R. W., 2001, Limited numbers of recycling vesicles in small CNS nerve terminals: implications for neural signaling and vesicular cycling, Trends Neurosci. 24: 637.
Hatsuzawa, K., Lang, T., Fasshauer, D., Bruns, D., and Jahn, R., 2003, The R-SNARE motif of tomosyn forms SNARE complexes with syntaxin 1 and SNAP-25 and down-regulates exocytosis, J. Biol. Chem. 278:31159.
Hilfiker, S., Pieribone, V. A., Czemik, A. J., Kao, H. T., Augustine, G. J., and Greengard, P., 1999, Synapsins as regulators of transmitter release, Philos. Trans. Roy. Soc. Lond[B]. 354: 269.
Jaffe, E. H., Marty, A., Schulte, A., and Chow, R. H., 1998, Extrasynaptic vesicular transmitter release from the somata of substantia nigra neurons in rat midbrain slices, J. Neurosci. 18: 3548.
Jahn, R., Lang, T., and Südhof, T. C., 2003, Membrane fusion, Cell 112: 519.
Joux, N., Chevaleyre, V., Alonso, G., Boissin-Agasse, L., Moos, F. C., Desarmenien, M. G., and Hussy, N., 2001, High voltage-activated Ca2+ currents in rat supraoptic neurones: Biophysical properties and expression of the various channel alpha 1 subunits, J. Neuroendocrinol. 13: 638.
Koenig, J. H., and Ikeda, K., 1989, Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval, J. Neurosci. 9: 3844.
Lambert, R. C., Dayanithi, G., Moos, F. C., and Richard, P., 1994, A rise in the intracellular Ca2+ concentration of isolated rat supraoptic cells in response to oxytocin, J. Physiol. 478: 275.
Landry, M., Vila-Porcile, E., Hökfelt, T., and Calas, A., 2003, Differential routing of coexisting neuropeptides in vasopressin neurons, Eur. J. Neurosci. 17: 579.
Langley, K., and Grant, N. J., 1997, Are exocytosis mechanisms transmitter specific?, Neurochem. Int. 31: 739.
Ludwig, M., 1998, Dendritic release of vasopressin and oxytocin, J. Neuroendocrinol. 10: 881.
Ludwig, M., and Pittman, Q. J., 2003, Talking back: dendritic transmitter release, Trends Neurosci. 26: 255.
Ludwig, M., Sabatier, N., Bull, P. M., Landgraf, R., Dayanithi, G., and Leng, G., 2002, Intracellular calcium stores regulate activity-dependent neuropeptide release from dendrites, Nature 418: 85.
Ma, D., and Morris, J. F., 1998, Local protein synthesis in magnocellular dendrites. Basic elements and their response to hyperosmotic stimuli, Adv. Exp. Med. Biol. 449: 55.
Ma, D., and Morris, J. F., 2002, Protein synthetic machinery in the dendrites of the magnocellular neurosecretory neurons of wild-type Long-Evans and homozygous Brattleboro rats, J. Chem. Neuroanat. 23: 171.
Maletic-Savatic, M., and Malinow, R., 1998, Calcium-evoked dendritic exocytosis in cultured hippocampal neurons. Part I: Trans-Golgi network-derived organelles undergo regulated exocytosis, J. Neurosci. 18: 6803.
Marek, K. W., and Davis, G. W., 2002, Transgenically encoded protein photoinactivation (FlAsH-FALI): acute inactivation of synaptotagmin I, Neuron 36: 805.
Marks, B., Stowell, M. H., Vallis, Y., Mills, I. G., Gibson, A., Hopkins, C. R., and McMahon, H. T., 2001, GTPase activity of dynamin and resulting conformation change are essential for endocytosis, Nature 410: 231.
Martin, T. F., 2002, Prime movers of synaptic vesicle exocytosis, Neuron. 34: 9.
Moos, F., Freundmercier, M. J., Guerne, Y., Guerne, J. M., Stoeckel, M. E., and Richard, P., 1984, Release of oxytocin and vasopressin by magnocellular nuclei in vitro-specific facilitatory effect of oxytocin on its own release, J. Endocrinol. 102: 63.
Morris, J. F., Christian, H., Ma, D., and Wang, H., 2000, Dendritic secretion of peptides from hypothalamic magnocellular neurosecretory neurones: a local dynamic control system and its functions, Exp. Physiol. 85: 131S.
Murthy, V. N., and De Camilli, P., 2003, Cell biology of the presynaptic terminal, Ann. Rev. Neurosci. 26: 701.
Neher, E., 1998, Vesicle pools and Ca2+ microdomains: new tools for understanding their roles in transmitter release, Neuron 20: 389.
Neumann, I., Russell, J. A., and Landgraf, R., 1993, Oxytocin and vasopressin release within the supraoptic and paraventricular nuclei of pregnant, parturient and lactating rats-a microdialysis study, Neuroscience 53: 65.
Parsons, S. M., 2000, Transport mechanisms in acetylcholine and monoamine storage, FASEB J. 14: 2423.
Peters, C, Bayer, M. J., Bühler, S., Andersen, J. S., Mann, M., and Mayer, A., 2001, Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion, Nature 409: 581.
Pow, D. V., and Morris, J. F., 1989, Dendrites of hypothalamic magnocellular neurons release neurohypophyseal peptides by exocytosis, Neuroscience 32: 435.
Rizzoli, S. O., and Betz, W. J., 2003, Neurobiology: All change at the synapse, Nature 423: 591.
Rizzoli, S. O., and Betz, W. J., 2004, The structural organization of the readily releasable pool of synaptic vesicles, Science 303: 2037.
Schwab, Y., Mouton, J., Chasserot-Golaz, S., Marty, I., Maulet, Y., and Jover, E., 2001, Calcium-dependent translocation of synaptotagmin to the plasma membrane in the dendrites of developing neurones, Mol. Brain Res. 96: 1.
Shibuya, I., Noguchi, J., Tanaka, K., Harayama, N., Inoue, Y., Kabashima, N., Ueta, Y., Hattori, Y., and Yamashita, H., 1998, PACAP increases the cytosolic Ca2+ concentration and stimulates somatodendritic vasopressin release in rat supraoptic neurons, J. Neuroendocrinol. 10: 31.
Simmons, M. L., Terman, G. W., Gibbs, S. M., and Chavkin, C., 1995, L-Type calcium channels mediate dynorphin neuropeptide release from dendrites but not axons of hippocampal granule cells, Neuron 14: 1265.
Slepnev, V. I., and De Camilli, P., 2000, Accessory factors in clathrin-dependent synaptic vesicle endocytosis, Nat. Rev. Neurosci. 1: 161.
Sugita, S., Shin, O.-H., Han, W., Lao, Y., and Südhof, T. C., 2002, Synaptotagmins form a heirarchy of exocytic Ca2+ sensors with distinct Ca2+ affinities, EMBO J. 21: 270.
Sutton, R. B., Fasshauer, D., Jahn, R., and Brunger, A. T., 1998, Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4Å resolution, Nature 395: 347.
Taraska, J. W., Perrais, D., Ohara-Imaizumi, M., Nagamatsu, S., and Almers, W., 2003, Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells, PNAS USA 100: 2070.
Tobin, V. A., Moos, F. C., and Desarmenien, M. G., 2002, ICRAC in magnocellular neurones from adult male rats., The 5th International Congress of Neuroendocrinology, Bristol, UK P262.
Tobin, V. A., Hurst, G., Norrie, L., Dal Rio, F., Bull, P. M., and Ludwig, M., 2004, Thapsigargin-induced mobilisation of dendritic dense core vesicles in supraoptic neurones, Eur. J. Neurosci. 19: 2909.
Tooze, S. A., Martens, G. J. M., and Huttner, W. B., 2001, Secretory granule biogenesis: rafting to the SNARE, Trends Cell Biol. 11: 116.
Virmani, T., Han, W., Liu, X., Sudhof, T. C., and Kavalali, E. T., 2003, Synaptotagmin 7 splice variants differentially regulate synaptic vesicle recycling, EMBO J. 22: 5347.
Vitale, M. L., Seward, E. P., and Trifaró, J.-M., 1995, Chromaffin cell cortical actin network dynamics control the size of the release-ready vesicle pool and the initial rate of exocytosis, Neuron 14: 353.
Voets, T., 2000, Dissection of three Ca2+-dependent steps leading to secretion in chromaffin cells from mouse adrenal slices, Neuron 28: 537.
Wang, C. T., Lu, J. C., Bai, J., Chang, P. Y., Martin, T. F., Chapman, E. R., and Jackson, M. B., 2003, Different domains of synaptotagmin control the choice between kiss-and-run and full fusion, Nature 424: 943.
Waters, M. G., and Hughson, F. M., 2000, Membrane tethering and fusion in the secretory and endocytic pathways, Traffic 1: 588.
Weber, T., Zemelman, B. T., McNew, J. A., Westermann, B., Gmachl, M., Parlati, F., Söllner, T. H., and Rothman, J. E., 1998, SNAREpins: minimal machinery for membrane fusion, Cell 92: 759.
Wotjak, C. T., Ganster, J., Kohl, G., Holsboer, F., Landgraf, R., and Engelmann, M., 1998, Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: New insights into the secretory capacities of peptidergic neurons, Neuroscience 85: 1209.
Yizhar, O., Matti, U., Melamed, R., Hagalili, Y., Bruns, D., Rettig, J., and Ashery, U., 2004, Tomosyn inhibits priming of large dense-core vesicles in a calcium-dependent manner, PNAS USA 101: 2578.
Yoshihara, M., Adolfsen, B., and Littleton, J. T., 2003, Is synaptotagmin the calcium sensor? Curr. Opin. Neurobiol. 13: 315.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2005 Springer Science+Business Media Inc.
About this chapter
Cite this chapter
Apps, D.K., Cousin, M.A., Duncan, R.R., Wiegand, U.K., Shipston, M.J. (2005). The Lifecycle of Secretory Vesicles: Implications for Dendritic Transmitter Release. In: Ludwig, M. (eds) Dendritic Neurotransmitter Release. Springer, Boston, MA. https://doi.org/10.1007/0-387-23696-1_3
Download citation
DOI: https://doi.org/10.1007/0-387-23696-1_3
Publisher Name: Springer, Boston, MA
Print ISBN: 978-0-387-22933-1
Online ISBN: 978-0-387-23696-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)