Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-23T03:25:03.090Z Has data issue: false hasContentIssue false
  • English
  • Français

Fusion Pore: An Evolutionary Invention of Nucleated Cells

Published online by Cambridge University Press:  01 July 2010

N. Vardjan ,
M. Stenovec ,
J. Jorgačevski ,
M. Kreft  and
R. Zorec
N. Vardjan
Affiliation:
Celica Biomedical Center, LCI, Tehnološki park 24, 1000 Ljubljana, Slovenia LN-MCP, Institute of Pathophysiology, Faculty of Medicine, University of Ljubljana, Zaloška 4, 1000 Ljubljana, Slovenia.
M. Stenovec
Affiliation:
Celica Biomedical Center, LCI, Tehnološki park 24, 1000 Ljubljana, Slovenia LN-MCP, Institute of Pathophysiology, Faculty of Medicine, University of Ljubljana, Zaloška 4, 1000 Ljubljana, Slovenia.
J. Jorgačevski
Affiliation:
LN-MCP, Institute of Pathophysiology, Faculty of Medicine, University of Ljubljana, Zaloška 4, 1000 Ljubljana, Slovenia.
M. Kreft
Affiliation:
Celica Biomedical Center, LCI, Tehnološki park 24, 1000 Ljubljana, Slovenia LN-MCP, Institute of Pathophysiology, Faculty of Medicine, University of Ljubljana, Zaloška 4, 1000 Ljubljana, Slovenia.
R. Zorec*
Affiliation:
Celica Biomedical Center, LCI, Tehnološki park 24, 1000 Ljubljana, Slovenia LN-MCP, Institute of Pathophysiology, Faculty of Medicine, University of Ljubljana, Zaloška 4, 1000 Ljubljana, Slovenia.
*
E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

This article outlines the lecture presented by Robert Zorec at the Academia Europea meeting in Liverpool on 19 September 2008, four decades after the Sherrington Lecture of Bernard Katz who, together with his colleagues, developed a number of paradigms addressing vesicles in chemical synapses. Vesicles are subcellular organelles that evolved in eukaryotic cells 1000 to 2000 million years ago. They store signalling molecules such as chemical messengers, which are essential for the function of neurons and endocrine cells in supporting the communication between tissues and organs in the human body. Upon a stimulus, the vesicle-stored signalling molecules (neurotransmitters or hormones) are released from cells. This event involves exocytosis, a fundamental biological process, consisting of the merger of the vesicle membrane with the plasma membrane. The two fusing membranes lead to the formation of an aqueous channel – the fusion pore – through which signalling molecules exit into the extracellular space or blood stream. The work of Bernard Katz and colleagues considered that vesicle cargo discharge initially requires the delivery of vesicles to the plasma membrane, where vesicles dock and get primed for fusion with the plasma membrane, and that stimulation initiates the formation of the transient fusion pore through which cargo molecules leave the vesicle lumen in an all-or-none-fashion. However, recent studies indicate that this may not be so simple. Here we highlight the novel findings which indicate that fusion pores are subject to regulations, which affect the release competence of a single vesicle. At least in pituitary lactotrophs, which are the subject of research in our laboratories, single vesicle release of peptide signalling molecules involves modulation of fusion pore diameter and fusion pore kinetics.

Type
Focus: Evolution
Information
European Review , Volume 18 , Issue 3 , July 2010 , pp. 347 - 364
Copyright
Copyright © Academia Europaea 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Cooper, G. M. (2000) The Origin and Evolution of Cells (Massachusetts: Sunderland) pp. 5–10.Google Scholar
2.Yoon, H. S., Hackett, J., Ciniglia, C., Pinto, G. and Bhattacharya, D. (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Molecular Biology and Evolution, 21, pp. 809–818.CrossRefGoogle ScholarPubMed
3.Katz, B. and Miledi, R. (1967) A study of synaptic transmission in the absence of nerve impulses. The Journal of Physiology, 192, pp. 407–436.CrossRefGoogle Scholar
4.Katz, B. (1969) The Release of Neural Transmitter Substances (Liverpool: Liverpool University Press).Google Scholar
5.Jones, S. (1998) Overview of voltage-dependent calcium channels. Journal of Bioenergetics and Biomembranes, 30, pp. 299–312.CrossRefGoogle Scholar
6.Takamori, S., Holt, M., Stenius, K., Lemke, E., Grønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., Müller, S., Rammner, B., Gräter, F., Hub, J., De Groot, B., Mieskes, G., Moriyama, Y., Klingauf, J., Grubmüller, H., Heuser, J., Wieland, F. and Jahn, R. (2006) Molecular anatomy of a trafficking organelle. Cell, 127, pp. 831–846.CrossRefGoogle ScholarPubMed
7.Neher, E. and Marty, A. (1982) Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proceedings of the National Academy of Sciences of the United States of America, 79, pp. 6712–6716.CrossRefGoogle ScholarPubMed
8.Ceccarelli, B., Hurlbut, W. and Mauro, A. (1973) Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. The Journal of Cell Biology, 57, pp. 499–524.CrossRefGoogle ScholarPubMed
9.Heuser, J. and Reese, T. (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. The Journal of Cell Biology, 57, pp. 315–344.CrossRefGoogle ScholarPubMed
10.Fernandez, J., Neher, E. and Gomperts, B. (1984) Capacitance measurements reveal stepwise fusion events in degranulating mast cells. Nature, 312, pp. 453–455.CrossRefGoogle ScholarPubMed
11.Stenovec, M., Kreft, M., Poberaj, I., Betz, W. and Zorec, R. (2004) Slow spontaneous secretion from single large dense-core vesicles monitored in neuroendocrine cells. The FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 18, pp. 1270–1272.CrossRefGoogle ScholarPubMed
12.Vardjan, N., Stenovec, M., Jorgacevski, J., Kreft, M. and Zorec, R. (2007) Subnanometer fusion pores in spontaneous exocytosis of peptidergic vesicles. The Journal of Neurosciences: The Official Journal of Society for Neurosciences, 27, pp. 4737–4746.CrossRefGoogle ScholarPubMed
13.Jorgacevski, J., Stenovec, M., Kreft, M., Bajić, A., Rituper, B., Vardjan, N., Stojilkovic, S. and Zorec, R. (2008) Hypotonicity and peptide discharge from a single vesicle. American Journal of Physiology. Cell Physiology, 295, pp. C624–C631.CrossRefGoogle Scholar
14.Henkel, A., Meiri, H., Horstmann, H., Lindau, M. and Almers, W. (2000) Rhythmic opening and closing of vesicles during constitutive exo- and endocytosis in chromaffin cells. The EMBO Journal, 19, pp. 84–93.CrossRefGoogle ScholarPubMed
15.Thiel, G., Kreft, M. and Zorec, R. (2009) Rhytmic kinetics of single fusion and fission in a plant cell protoplast. Annals of the New York Academy of Sciences, 1152, pp. 1–6.CrossRefGoogle Scholar
16.Debus, K. and Lindau, M. (2000) Resolution of patch capacitance recordings and of fusion pore conductances in small vesicles. Biophysical Journal, 78, pp. 2983–2997.CrossRefGoogle Scholar
17.Murthy, V. and Stevens, C. (1999) Reversal of synaptic vesicle docking at central synapses. Nature Neuroscience, 2, pp. 503–507.CrossRefGoogle ScholarPubMed
18.Jahn, R. and Scheller, R. (2006) SNAREs – engines for membrane fusion. Nature Reviews. Molecular Cell Biology, 7, pp. 631–643.CrossRefGoogle ScholarPubMed
19.Deitcher, D., Ueda, A., Stewart, B., Burgess, R., Kidokoro, Y. and Schwarz, T. (1998) Distinct requirements for evoked and spontaneous release of neurotransmitter are revealed by mutations in the Drosophila gene neuronal-synaptobrevin. The Journal of Neuroscience: The Official Journal of Society of Neurosciences, 18, pp. 2028–2039.CrossRefGoogle ScholarPubMed
20.Schoch, S., Deák, F., Königstorfer, A., Mozhayeva, M., Sara, Y., Südhof, T. and Kavalali, E. T. (2001) SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science, 294, pp. 1117–1122.CrossRefGoogle ScholarPubMed
21.Washbourne, P., Thompson, P., Carta, M., Costa, E., Mathews, J., Lopez-Benditó, G., Molnár, Z., Becher, M., Valenzuela, C., Partridge, L. and Wilson, M. (2002) Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nature Neuroscience, 5, pp. 19–26.CrossRefGoogle ScholarPubMed
22.Deák, F., Schoch, S., Liu, X., Südhof, T. and Kavalali, E. T. (2004) Synaptobrevin is essential for fast synaptic-vesicle endocytosis. Nature Cell Biology, 6, pp. 1102–1108.CrossRefGoogle Scholar
23.Hua, S., Raciborska, D., Trimble, W. and Charlton, M. (1998) Different VAMP/synaptobrevin complexes for spontaneous and evoked transmitter release at the crayfish neuromuscular junction. Journal of Neurophysiology, 80, pp. 3233–3246.CrossRefGoogle ScholarPubMed
24.Geppert, M., Goda, Y., Hammer, R., Li, C., Rosahl, T., Stevens, C. and Südhof, T. (1994) Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell, 79, pp. 717–727.CrossRefGoogle Scholar
25.Kreft, M., Kuster, V., Grilc, S., Rupnik, M., Milisav, I. and Zorec, R. (2003) Synaptotagmin I increases the probability of vesicle fusion at low [Ca2+] in pituitary cells. American Journal of Physiology. Cell Physiology, 284, pp. C547–C554.CrossRefGoogle ScholarPubMed
26.Pang, Z., Sun, J., Rizo, J., Maximov, A. and Südhof, T. (2006) Genetic analysis of synaptotagmin 2 in spontaneous and Ca2+-triggered neurotransmitter release. The EMBO Journal, 25, pp. 2039–2050.CrossRefGoogle Scholar
27.Maximov, A., Shin, O., Liu, X. and Südhof, T. (2007) Synaptotagmin-12, a synaptic vesicle phosphoprotein that modulates spontaneous neurotransmitter release. The Journal of Cell Biology, 176, pp. 113–124.CrossRefGoogle ScholarPubMed
28.Wucherpfennig, T., Wilsch-Bräuninger, M. and González-Gaitán, M. (2003) Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. The Journal of Cell Biology, 161, pp. 609–624.CrossRefGoogle Scholar
29.Virmani, T., Ertunc, M., Sara, Y., Mozhayeva, M. and Kavalali, E. T. (2005) Phorbol esters target the activity-dependent recycling pool and spare spontaneous vesicle recycling. The Journal of Neuroscience: The Official Journal of Society of Neuroscience, 25, pp. 10922–10929.CrossRefGoogle ScholarPubMed
30.Sara, Y., Virmani, T., Deák, F., Liu, X. and Kavalali, E. T. (2005) An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron, 45, pp. 563–573.CrossRefGoogle ScholarPubMed
31.Groemer, T. and Klingauf, J. (2007) Synaptic vesicles recycling spontaneously and during activity belong to the same vesicle pool. Nature Neuroscience, 10, pp. 145–147.CrossRefGoogle Scholar
32.Wasser, C., Ertunc, M., Liu, X. and Kavalali, E. T. (2007) Cholesterol-dependent balance between evoked and spontaneous synaptic vesicle recycling. The Journal of Physiology, 579, pp. 413–429.CrossRefGoogle ScholarPubMed
33.Darios, F., Wasser, C., Shakirzyanova, A., Giniatullin, A., Goodman, K., Munoz-Bravo, J. L., Raingo, J., Jorgacevski, J., Kreft, M., Zorec, R., Rosa, J. M., Gandia, L., Gutiérrez, L. M., Binz, T., Giniatullin, R., Kavalali, E. T. and Davletov, B. (2009) Sphingosine facilitates SNARE complex assembly and activates synaptic vesicle exocytosis. Neuron., 62, pp. 683–694.CrossRefGoogle Scholar
34.Albillos, A., Dernick, G., Horstmann, H., Almers, W., Alvarez de Toledo, G. and Lindau, M. (1997) The exocytotic event in chromaffin cells revealed by patch amperometry. Nature, 389, pp. 509–512.CrossRefGoogle Scholar
35.Angleson, J., Cochilla, A., Kilic, G., Nussinovitch, I. and Betz, W. (1999) Regulation of dense core release from neuroendocrine cells revealed by imaging single exocytic events. Nature Neuroscience, 2, pp. 440–446.CrossRefGoogle Scholar
36.Rahamimoff, R. and Fernandez, J. (1997) Pre- and postfusion regulation of transmitter release. Neuron, 18, pp. 17–27.CrossRefGoogle ScholarPubMed
37.Walker, A. and Farquhar, M. (1980) Preferential release of newly synthesized prolactin granules is the result of functional heterogeneity among mammotrophs. Endocrinology, 107, pp. 1095–1104.CrossRefGoogle ScholarPubMed
38.Sun, J., Wu, X. and Wu, L. (2002) Single and multiple vesicle fusion induce different rates of endocytosis at a central synapse. Nature, 417, pp. 555–559.CrossRefGoogle Scholar
39.Barg, S., Olofsson, C., Schriever-Abeln, J., Wendt, A., Gebre-Medhin, S., Renström., E. and Rorsman, P. (2002) Delay between fusion pore opening and peptide release from large dense-core vesicles in neuroendocrine cells. Neuron, 33, pp. 287–299.CrossRefGoogle ScholarPubMed
40.Tsuboi, T. and Rutter, G. (2003) Multiple forms of ‘kiss-and-run’ exocytosis revealed by evanescent wave microscopy. Current Biology: CB, 13, pp. 563–567.CrossRefGoogle ScholarPubMed
41.Obermüller, S., Lindqvist, A., Karanauskaite, J., Galvanovskis, J., Rorsman, P. and Barg, S. (2005) Selective nucleotide-release from dense-core granules in insulin-secreting cells. Journal of Cell Science, 118, pp. 4271–4282.CrossRefGoogle ScholarPubMed
42.Staal, R., Mosharov, E. and Sulzer, D. (2004) Dopamine neurons release transmitter via a flickering fusion pore. Nature Neuroscience, 7, pp. 341–346.CrossRefGoogle Scholar
43.de Toledo, Alvarez, Fernández-Chacón, R. and Fernández, J. (1993) Release of secretory products during transient vesicle fusion. Nature, 363, pp. 554–558.CrossRefGoogle Scholar
44.Miesenböck, G., De Angelis, D. and Rothman, J. (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature, 394, pp. 192–195.CrossRefGoogle ScholarPubMed
45.Spruce, A., Breckenridge, L., Lee, A. and Almers, W. (1990) Properties of the fusion pore that forms during exocytosis of a mast cell secretory vesicle. Neuron, 4, pp. 643–654.CrossRefGoogle ScholarPubMed
46.Takahashi, N., Kishimoto, T., Nemoto, T., Kadowaki, T. and Kasai, H. (2002) Fusion pore dynamics and insulin granule exocytosis in the pancreatic islet. Science, 297, pp. 1349–1352.CrossRefGoogle Scholar
47.Fulop, T., Radabaugh, S. and Smith, C. (2005) Activity-dependent differential transmitter release in mouse adrenal chromaffin cells. The Journal of Neuroscience: The Official Journal of Society of Neuroscience, 25, pp. 7324–7332.CrossRefGoogle ScholarPubMed
48.Elhamdani, A., Palfrey, H. and Artalejo, C. (2001) Quantal size is dependent on stimulation frequency and calcium entry in calf chromaffin cells. Neuron, 31, pp. 819–830.CrossRefGoogle ScholarPubMed
49.Vardjan, N., Jorgačevski, J., Stenovec, M., Kreft, M. and Zorec, R. (2009) Compound exocytosis in pituitary cells. Annals of the New York Academy of Sciences, 1152, pp. 63–75.CrossRefGoogle ScholarPubMed
50.LoGiudice, L. and Matthews, G. (2006) The synaptic vesicle cycle: is kissing overrated? Neuron, 51, pp. 676–677.CrossRefGoogle Scholar
51.Taraska, J., Perrais, D., Ohara-Imaizumi, M., Nagamatsu, S. and Almers, W. (2003) Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells. Proceedings of the National Academy of Sciences of the United States of America, 100, pp. 2070–2075.CrossRefGoogle ScholarPubMed
52.Thorn, P. and Parker, I. (2005) Two phases of zymogen granule lifetime in mouse pancreas: ghost granules linger after exocytosis of contents. The Journal of Physiology, 563, pp. 433–442.CrossRefGoogle ScholarPubMed
53.Ohara-Imaizumi, M., Nakamichi, Y., Tanaka, T., Katsuta, H., Ishida, H. and Nagamatsu, S. (2002) Monitoring of exocytosis and endocytosis of insulin secretory granules in the pancreatic beta-cell line MIN6 using pH-sensitive green fluorescent protein (pHluorin) and confocal laser microscopy. The Biochemical Journal, 363, pp. 73–80.CrossRefGoogle ScholarPubMed
54.Atluri, P. and Ryan, T. (2006) The kinetics of synaptic vesicle reacidification at hippocampal nerve terminals. The Journal of Neuroscience: The Official Journal of Society of Neuroscience, 26, pp. 2313–2320.CrossRefGoogle ScholarPubMed
55.Elhamdani, A., Azizi, F. and Artalejo, C. (2006) Double patch clamp reveals that transient fusion (kiss-and-run) is a major mechanism of secretion in calf adrenal chromaffin cells: high calcium shifts the mechanism from kiss-and-run to complete fusion. The Journal of Neuroscience: The Official Journal of Society of Neuroscience, 26, pp. 3030–3036.CrossRefGoogle Scholar
56.Harata, N., Aravanis, A. and Tsien, R. (2006) Kiss-and-run and full-collapse fusion as modes of exo-endocytosis in neurosecretion. Journal of Neurochemistry, 97, pp. 1546–1570.CrossRefGoogle ScholarPubMed
57.Churchward, M. A., Rogasevskaia, T., Brandman, D. M., Khosravani, H., Nava, P., Atkinson, J. K. and Coorssen, J. R. (2008) Specific lipids supply critical negative spontaneous curvature – an essential component of native Ca2+-triggered membrane fusion. Biophysical Journal, 94, pp. 3976–3986.CrossRefGoogle Scholar
58.Gonçalves, P. P., Stenovec, M., Chowdhury, H. H., Grilc, S., Kreft, M. and Zorec, R. (2008) Prolactin secretion sites contain syntaxin-1 and differ from ganglioside monosialic acid rafts in rat lactotrophs. Endocrinology, 149, pp. 4948–4957.CrossRefGoogle Scholar