Fusion pore: An evolutionary invention of nucleated cells

European Review

Volumn 18, Issue 3, 2010, Pages 347-364

  Vardjan, N ^a,b   Stenovec, M ^a,b   Jorgacevski J ^b   Kreft, M ^a,b   Zorec, R ^a,b  

^a Celica Biomedical Sciences Center   (Slovenia)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL ANALYSIS; EDUCATION; EVOLUTIONARY BIOLOGY; EVOLUTIONARY THEORY;

EUKARYOTA; RUMEX;

EID: 77957265399     PISSN: 10627987     EISSN: 14740575     Source Type: Journal    
DOI: 10.1017/S1062798710000074     Document Type: Article

References (58)

1. G. M. Cooper (2000) The Origin and Evolution of Cells (Massachusetts: Sunderland) pp. 5-10.
2. H. S. Yoon, J. Hackett, C. Ciniglia, G. Pinto and D. Bhattacharya (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Molecular Biology and Evolution, 21, pp. 809-818. (Pubitemid 38529723)
3. B. Katz and R. Miledi (1967) A study of synaptic transmission in the absence of nerve impulses. The Journal of Physiology, 192, pp. 407-436.
4. B. Katz (1969) The Release of Neural Transmitter Substances (Liverpool: Liverpool University Press).
5. S. Jones (1998) Overview of voltage-dependent calcium channels. Journal of Bioenergetics and Biomembranes, 30, pp. 299-312. (Pubitemid 28436152)
6. S. Takamori, M. Holt, K. Stenius, E. Lemke, M. Grønborg, D. Riedel, H. Urlaub, S. Schenck, B. Brügger, P. Ringler, S. Mü ller, B. Rammner, F. Gräter, J. Hub, B. De Groot, G. Mieskes, Y. Moriyama, J. Klingauf, H. Grubmü ller, J. Heuser, F. Wieland and R. Jahn (2006) Molecular anatomy of a trafficking organelle. Cell, 127, pp. 831-846. (Pubitemid 44716256)
7. E. Neher and A. Marty (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. (Pubitemid 13220246)
8. B. Ceccarelli, W. Hurlbut and A. Mauro (1973) Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. The Journal of Cell Biology, 57, pp. 499-524.
9. J. Heuser and T. Reese (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.
10. J. Fernandez, E. Neher and B. Gomperts (1984) Capacitance measurements reveal stepwise fusion events in degranulating mast cells. Nature, 312, pp. 453-455. (Pubitemid 15217840)
11. M. Stenovec, M. Kreft, I. Poberaj, W. Betz and R. Zorec (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. (Pubitemid 39561573)
12. N. Vardjan, M. Stenovec, J. Jorgacevski, M. Kreft and R. Zorec (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. (Pubitemid 46663566)
13. J. Jorgacevski, M. Stenovec, M. Kreft, A. Bajić, B. Rituper, N. Vardjan, S. Stojilkovic and R. Zorec (2008) Hypotonicity and peptide discharge from a single vesicle. American Journal of Physiology. Cell Physiology, 295, pp. C624-C631.
14. A. Henkel, H. Meiri, H. Horstmann, M. Lindau and W. Almers (2000) Rhythmic opening and closing of vesicles during constitutive exo- and endocytosis in chromaffin cells. The EMBO Journal, 19, pp. 84-93. (Pubitemid 30009228)
15. G. Thiel, M. Kreft and R. Zorec (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.
16. K. Debus and M. Lindau (2000) Resolution of patch capacitance recordings and of fusion pore conductances in small vesicles. Biophysical Journal, 78, pp. 2983-2997. (Pubitemid 30396929)
17. V. Murthy and C. Stevens (1999) Reversal of synaptic vesicle docking at central synapses. Nature Neuroscience, 2, pp. 503-507. (Pubitemid 30491229)
18. R. Jahn and R. Scheller (2006) SNAREs - engines for membrane fusion. Nature Reviews. Molecular Cell Biology, 7, pp. 631-643. (Pubitemid 44268209)
19. D. Deitcher, A. Ueda, B. Stewart, R. Burgess, Y. Kidokoro and T. Schwarz (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. (Pubitemid 28141410)
20. S. Schoch, F. Deák, A. Königstorfer, M. Mozhayeva, Y. Sara, T. Südhof and E. T. Kavalali (2001) SNARE function analyzed in synaptobrevin/ VAMP knockout mice. Science, 294, pp. 1117-1122. (Pubitemid 33041870)
21. P. Washbourne, P. Thompson, M. Carta, E. Costa, J. Mathews, G. Lopez-Benditó, Z. Molnár, M. Becher, C. Valenzuela, L. Partridge and M. Wilson (2002) Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nature Neuroscience, 5, pp. 19-26. (Pubitemid 34038778)
22. F. Deák, S. Schoch, X. Liu, T. Südhof and E. T. Kavalali (2004) Synaptobrevin is essential for fast synaptic-vesicle endocytosis. Nature Cell Biology, 6, pp. 1102-1108. (Pubitemid 39468011)
23. S. Hua, D. Raciborska, W. Trimble and M. Charlton (1998) Different VAMP/synaptobrevin complexes for spontaneous and evoked transmitter release at the crayfish neuromuscular junction. Journal of Neurophysiology, 80, pp. 3233-3246. (Pubitemid 29029246)
24. M. Geppert, Y. Goda, R. Hammer, C. Li, T. Rosahl, C. Stevens and T. Südhof (1994) Synaptotagmin I: A major Ca21 sensor for transmitter release at a central synapse. Cell, 79, pp. 717-727. (Pubitemid 124000776)
25. M. Kreft, V. Kuster, S. Grilc, M. Rupnik, I. Milisav and R. Zorec (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. (Pubitemid 36120092)
26. Z. Pang, J. Sun, J. Rizo, A. Maximov and T. Südhof (2006) Genetic analysis of synaptotagmin 2 in spontaneous and Ca2+-triggered neurotransmitter release. The EMBO Journal, 25, pp. 2039-2050. (Pubitemid 43756221)
27. A. Maximov, O. Shin, X. Liu and T. Südhof (2007) Synaptotagmin-12, a synaptic vesicle phosphoprotein that modulates spontaneous neurotransmitter release. The Journal of Cell Biology, 176, pp. 113-124. (Pubitemid 46041685)
28. T. Wucherpfennig, M. Wilsch-Bräuninger and M. González- Gaitán (2003) Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. The Journal of Cell Biology, 161, pp. 609-624. (Pubitemid 36578584)
29. T. Virmani, M. Ertunc, Y. Sara, M. Mozhayeva and E. T. Kavalali (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. (Pubitemid 41692622)
30. Y. Sara, T. Virmani, F. Deák, X. Liu and E. T. Kavalali (2005) An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron, 45, pp. 563-573. (Pubitemid 40249868)
31. T. Groemer and J. Klingauf (2007) Synaptic vesicles recycling spontaneously and during activity belong to the same vesicle pool. Nature Neuroscience, 10, pp. 145-147. (Pubitemid 46174836)
32. C. Wasser, M. Ertunc, X. Liu and E. T. Kavalali (2007) Cholesteroldependent balance between evoked and spontaneous synaptic vesicle recycling. The Journal of Physiology, 579, pp. 413-429. (Pubitemid 46351759)
33. F. Darios, C. Wasser, A. Shakirzyanova, A. Giniatullin, K. Goodman, J. L. Munoz-Bravo, J. Raingo, J. Jorgacevski, M. Kreft, R. Zorec, J. M. Rosa, L. Gandia, L. M. Gutiérrez, T. Binz, R. Giniatullin, E. T. Kavalali and B. Davletov (2009) Sphingosine facilitates SNARE complex assembly and activates synaptic vesicle exocytosis. Neuron., 62, pp. 683-694.
34. A. Albillos, G. Dernick, H. Horstmann, W. Almers, G. Alvarez de Toledo and M. Lindau (1997) The exocytotic event in chromaffin cells revealed by patch amperometry. Nature, 389, pp. 509-512. (Pubitemid 27435328)
35. J. Angleson, A. Cochilla, G. Kilic, I. Nussinovitch and W. Betz (1999) Regulation of dense core release from neuroendocrine cells revealed by imaging single exocytic events. Nature Neuroscience, 2, pp. 440-446. (Pubitemid 30491254)
36. R. Rahamimoff and J. Fernandez (1997) Pre- and postfusion regulation of transmitter release. Neuron, 18, pp. 17-27. (Pubitemid 27053827)
37. A. Walker and M. Farquhar (1980) Preferential release of newly synthesized prolactin granules is the result of functional heterogeneity among mammotrophs. Endocrinology, 107, pp. 1095-1104. (Pubitemid 10019103)
38. J. Sun, X. Wu and L. Wu (2002) Single and multiple vesicle fusion induce different rates of endocytosis at a central synapse. Nature, 417, pp. 555-559. (Pubitemid 34595923)
39. S. Barg, C. Olofsson, J. Schriever-Abeln, A. Wendt, S. Gebre-Medhin, E. Renström. and P. Rorsman (2002) Delay between fusion pore opening and peptide release from large dense-core vesicles in neuroendocrine cells. Neuron, 33, pp. 287-299. (Pubitemid 34127760)
40. T. Tsuboi and G. Rutter (2003) Multiple forms of 'kiss-and-run' exocytosis revealed by evanescent wave microscopy. Current Biology: CB, 13, pp. 563-567. (Pubitemid 36391933)
41. S. Obermü ller, A. Lindqvist, J. Karanauskaite, J. Galvanovskis, P. Rorsman and S. Barg (2005) Selective nucleotide-release from dense-core granules in insulin-secreting cells. Journal of Cell Science, 118, pp. 4271-4282. (Pubitemid 41488964)
42. R. Staal, E. Mosharov and D. Sulzer (2004) Dopamine neurons release transmitter via a flickering fusion pore. Nature Neuroscience, 7, pp. 341-346. (Pubitemid 38429173)
43. Alvarez de Toledo, R. Fernández-Chacón and J. Fernández (1993) Release of secretory products during transient vesicle fusion. Nature, 363, pp. 554-558. (Pubitemid 23186644)
44. G. Miesenböck, D. De Angelis and J. Rothman (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature, 394, pp. 192-195. (Pubitemid 28325974)
45. A. Spruce, L. Breckenridge, A. Lee and W. Almers (1990) Properties of the fusion pore that forms during exocytosis of a mast cell secretory vesicle. Neuron, 4, pp. 643-654. (Pubitemid 20185081)
46. N. Takahashi, T. Kishimoto, T. Nemoto, T. Kadowaki and H. Kasai (2002) Fusion pore dynamics and insulin granule exocytosis in the pancreatic islet. Science, 297, pp. 1349-1352. (Pubitemid 34913173)
47. T. Fulop, S. Radabaugh and C. Smith (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. (Pubitemid 41129804)
48. A. Elhamdani, H. Palfrey and C. Artalejo (2001) Quantal size is dependent on stimulation frequency and calcium entry in calf chromaffin cells. Neuron, 31, pp. 819-830. (Pubitemid 32907376)
49. N. Vardjan, J. Jorgačevski, M. Stenovec, M. Kreft and R. Zorec (2009) Compound exocytosis in pituitary cells. Annals of the New York Academy of Sciences, 1152, pp. 63-75.
50. L. LoGiudice and G. Matthews (2006) The synaptic vesicle cycle: Is kissing overrated? Neuron, 51, pp. 676-677. (Pubitemid 44374916)
51. J. Taraska, D. Perrais, M. Ohara-Imaizumi, S. Nagamatsu and W. Almers (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. (Pubitemid 36254575)
52. P. Thorn and I. Parker (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. (Pubitemid 40360903)
53. M. Ohara-Imaizumi, Y. Nakamichi, T. Tanaka, H. Katsuta, H. Ishida and S. Nagamatsu (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. (Pubitemid 34280614)
54. P. Atluri and T. Ryan (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. (Pubitemid 44699040)
55. A. Elhamdani, F. Azizi and C. Artalejo (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.
56. N. Harata, A. Aravanis and R. Tsien (2006) Kiss-and-run and full-collapse fusion as modes of exo-endocytosis in neurosecretion. Journal of Neurochemistry, 97, pp. 1546-1570. (Pubitemid 43873652)
57. M. A. Churchward, T. Rogasevskaia, D. M. Brandman, H. Khosravani, P. Nava, J. K. Atkinson and J. R. Coorssen (2008) Specific lipids supply critical negative spontaneous curvature - an essential component of native Ca2+-triggered membrane fusion. Biophysical Journal, 94, pp. 3976-3986.
58. P. P. Gonçalves, M. Stenovec, H. H. Chowdhury, S. Grilc, M. Kreft and R. Zorec (2008) Prolactin secretion sites contain syntaxin-1 and differ from ganglioside monosialic acid rafts in rat lactotrophs. Endocrinology, 149, pp. 4948-4957.