Docking of LDCVs is modulated by lower intracellular [Ca2+] than priming

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Pasche, Mathias ^a,b   Matti, Ulf ^a   Hof, Detlef ^a   Rettig, Jens ^a   Becherer, Ute ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CALCIUM;

ANIMAL CELL; ARTICLE; AXIAL VESICLE MOBILITY; CALCIUM CELL LEVEL; CELL MEMBRANE; CELL MEMBRANE STEADY POTENTIAL; CELL MEMBRANE TRANSPORT; CELL SECRETION; CHROMAFFIN CELL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; COW; EXOCYTOSIS; FLUORESCENCE MICROSCOPY; LARGE DENSE CORE VESICLE; LATERAL VESICLE MOBILITY; MEMBRANE CAPACITANCE; MEMBRANE ELECTROPHYSIOLOGY; MEMBRANE FUSION; MEMBRANE VESICLE; MOLECULAR BIOLOGY; MOLECULAR DOCKING; MOLECULAR PRIMING; NONHUMAN; REGULATORY MECHANISM; TOTAL INTERNAL REFLECTION FLUORESCENCE MICROSCOPY; ANIMAL; CATTLE; CELL CULTURE; CYTOLOGY; METABOLISM; NEUROSECRETORY CELL; SECRETORY VESICLE;

ANIMALS; CALCIUM; CATTLE; CELL MEMBRANE; CELLS, CULTURED; MEMBRANE FUSION; NEUROENDOCRINE CELLS; SECRETORY VESICLES;

EID: 84860999574     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036416     Document Type: Article

References (40)

1. Verhage M, Sorensen JB, (2008) Vesicle docking in regulated exocytosis. Traffic 9: 1414-1424.
2. Plattner H, Artalejo AR, Neher E, (1997) Ultrastructural organization of bovine chromaffin cell cortex-analysis by cryofixation and morphometry of aspects pertinent to exocytosis. J Cell Biol 139: 1709-1717.
3. Becherer U, Rettig J, (2006) Vesicle pools, docking, priming, and release. Cell Tissue Res 326: 393-407.
4. Steyer JA, Horstmann H, Almers W, (1997) Transport, docking and exocytosis of single secretory granules in live chromaffin cells. Nature 388: 474-478.
5. Oheim M, Loerke D, Stuhmer W, Chow RH, (1998) The last few milliseconds in the life of a secretory granule. Docking, dynamics and fusion visualized by total internal reflection fluorescence microscopy (TIRFM). Eur Biophys J 27: 83-98.
6. Johns LM, Levitan ES, Shelden EA, Holz RW, Axelrod D, (2001) Restriction of secretory granule motion near the plasma membrane of chromaffin cells. J Cell Biol 153: 177-190.
7. Nofal S, Becherer U, Hof D, Matti U, Rettig J, (2007) Primed vesicles can be distinguished from docked vesicles by analyzing their mobility. J Neurosci 27: 1386-1395.
8. Toonen RF, Kochubey O, de Wit H, Gulyas-Kovacs A, Konijnenburg B, et al. (2006) Dissecting docking and tethering of secretory vesicles at the target membrane. Embo J 25: 3725-3737.
9. Yizhar O, Ashery U, (2008) Modulating vesicle priming reveals that vesicle immobilization is necessary but not sufficient for fusion-competence. PLoS ONE 3: e2694.
10. Neher E, Zucker RS, (1993) Multiple calcium-dependent processes related to secretion in bovine chromaffin cells. Neuron 10: 21-30.
11. Neher E, Sakaba T, (2008) Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59: 861-872.
12. Voets T, (2000) Dissection of three Ca2+-dependent steps leading to secretion in chromaffin cells from mouse adrenal slices. Neuron 28: 537-545.
13. von Ruden L, Neher E, (1993) A Ca-dependent early step in the release of catecholamines from adrenal chromaffin cells. Science 262: 1061-1065.
14. Becherer U, Pasche M, Nofal S, Hof D, Matti U, et al. (2007) Quantifying exocytosis by combination of membrane capacitance measurements and total internal reflection fluorescence microscopy in chromaffin cells. PLoS ONE 2: e505.
15. Voets T, Neher E, Moser T, (1999) Mechanisms underlying phasic and sustained secretion in chromaffin cells from mouse adrenal slices. Neuron 23: 607-615.
16. Limpert E, Stahel W, Abbt M, (2005) Log-normal Distributions across the Sciences: Keys and Clues. BioScience 51: 341-352.
17. Friedrich R, Groffen AJ, Connell E, van Weering JR, Gutman O, et al. (2008) DOC2B acts as a calcium switch and enhances vesicle fusion. J Neurosci 28: 6794-6806.
18. Allersma MW, Bittner MA, Axelrod D, Holz RW, (2006) Motion matters: secretory granule motion adjacent to the plasma membrane and exocytosis. Mol Biol Cell 17: 2424-2438.
19. Soerensen JB, Matti U, Wei SH, Nehring RB, Voets T, et al. (2002) The SNARE protein SNAP-25 is linked to fast calcium triggering of exocytosis. Proc Natl Acad Sci U S A 99: 1627-1632.
20. Degtyar VE, Allersma MW, Axelrod D, Holz RW, (2007) Increased motion and travel, rather than stable docking, characterize the last moments before secretory granule fusion. Proc Natl Acad Sci U S A 104: 15929-15934.
21. Karatekin E, Tran VS, Huet S, Fanget I, Cribier S, et al. (2008) A 20-nm step toward the cell membrane preceding exocytosis may correspond to docking of tethered granules. Biophys J 94: 2891-2905.
22. Gulyas-Kovacs A, de Wit H, Milosevic I, Kochubey O, Toonen R, et al. (2007) Munc18-1: sequential interactions with the fusion machinery stimulate vesicle docking and priming. J Neurosci 27: 8676-8686.
23. Trifaro JM, Gasman S, Gutierrez LM, (2008) Cytoskeletal control of vesicle transport and exocytosis in chromaffin cells. Acta Physiol (Oxf) 192: 165-172.
24. de Wit H, Walter AM, Milosevic I, Gulyas-Kovacs A, Riedel D, et al. (2009) Synaptotagmin-1 docks secretory vesicles to syntaxin-1/SNAP-25 acceptor complexes. Cell 138: 935-946.
25. Young SM Jr, Neher E, (2009) Synaptotagmin has an essential function in synaptic vesicle positioning for synchronous release in addition to its role as a calcium sensor. Neuron 63: 482-496.
26. Klingauf J, Neher E, (1997) Modeling buffered Ca2+ diffusion near the membrane: implications for secretion in neuroendocrine cells. Biophys J 72: 674-690.
27. Brandt BL, Hagiwara S, Kidokoro Y, Miyazaki S, (1976) Action potentials in the rat chromaffin cell and effects of acetylcholine. J Physiol 263: 417-439.
28. Fulop T, Radabaugh S, Smith C, (2005) Activity-dependent differential transmitter release in mouse adrenal chromaffin cells. J Neurosci 25: 7324-7332.
29. Ashery U, Varoqueaux F, Voets T, Betz A, Thakur P, et al. (2000) Munc13-1 acts as a priming factor for large dense-core vesicles in bovine chromaffin cells. Embo J 19: 3586-3596.
30. Stevens DR, Rettig J, (2009) The Ca(2+)-dependent activator protein for secretion CAPS: do I dock or do I prime? Mol Neurobiol 39: 62-72.
31. Junge HJ, Rhee JS, Jahn O, Varoqueaux F, Spiess J, et al. (2004) Calmodulin and Munc13 form a Ca2+ sensor/effector complex that controls short-term synaptic plasticity. Cell 118: 389-401.
32. Duncan RR, Betz A, Shipston MJ, Brose N, Chow RH, (1999) Transient, phorbol ester-induced DOC2-Munc13 interactions in vivo. J Biol Chem 274: 27347-27350.
33. Orita S, Naito A, Sakaguchi G, Maeda M, Igarashi H, et al. (1997) Physical and functional interactions of Doc2 and Munc13 in Ca2+-dependent exocytotic machinery. J Biol Chem 272: 16081-16084.
34. Dumitrescu Pene T, Rose SD, Lejen T, Marcu MG, Trifaro JM, (2005) Expression of various scinderin domains in chromaffin cells indicates that this protein acts as a molecular switch in the control of actin filament dynamics and exocytosis. J Neurochem 92: 780-789.
35. Rodriguez Del Castillo A, Lemaire S, Tchakarov L, Jeyapragasan M, Doucet JP, et al. (1990) Chromaffin cell scinderin, a novel calcium-dependent actin filament-severing protein. Embo J 9: 43-52.
36. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, et al. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567-1572.
37. Gillis KD, Mossner R, Neher E, (1996) Protein kinase C enhances exocytosis from chromaffin cells by increasing the size of the readily releasable pool of secretory granules. Neuron 16: 1209-1220.
38. Axelrod D, (2001) Total internal reflection fluorescence microscopy in cell biology. Traffic 2: 764-774.
39. Keyel PA, Watkins SC, Traub LM, (2004) Endocytic adaptor molecules reveal an endosomal population of clathrin by total internal reflection fluorescence microscopy. J Biol Chem 279: 13190-13204.
40. Fish KN, (2009) Total internal reflection fluorescence (TIRF) microscopy. Curr Protocol Cytom 50: 12.18.11-12.18.13.