Synaptotagmin-Ca2+ triggers two sequential steps in regulated exocytosis in rat PC12 cells: Fusion pore opening and fusion pore dilation

Journal of Physiology

Volumn 570, Issue 2, 2006, Pages 295-307

  Wang, Chih Tien ^a   Bai, Jihong ^a   Chang, Payne Y ^a   Chapman, Edwin R ^a   Jackson, Meyer B ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; LIGAND; SYNAPTOTAGMIN; ISOPROTEIN; SYNAPTOTAGMIN I; CALCIUM ION;

AMPEROMETRY; ANIMAL CELL; ARTICLE; CALCIUM BINDING; CELL FUSION; CELL INTERACTION; CELL KINETICS; CELL MEMBRANE PERMEABILITY; CELL STRAIN; CELL VACUOLE; CONTROLLED STUDY; EXOCYTOSIS; GENE MUTATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION; ANIMAL; CELL MEMBRANE POTENTIAL; CHEMISTRY; DRUG EFFECT; GENETICS; MUTATION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; STATISTICAL ANALYSIS; FUSION PORE; PC12 CELL LINE; PROTEIN DOMAIN;

ANIMALS; CALCIUM; CELL MEMBRANE PERMEABILITY; DATA INTERPRETATION, STATISTICAL; EXOCYTOSIS; LIGANDS; MEMBRANE POTENTIALS; MUTATION; PC12 CELLS; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RATS; SYNAPTOTAGMIN I;

EID: 33644865767     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2005.097378     Document Type: Article

References (32)

1. Albillos A, Dernick G, Horstmann H, Almers W, Alvarez De Toledo G & Lindau M (1997). The exocytotic event in chromaffin cells revealed by patch amperometry. Nature 389, 509-512.
2. Ales E, Tabares L, Poyato JM, Valero V, Lindau M & Alvarez De Toledo G (1999). High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nature Cell Biol 1, 40-44.
3. Alvarez De Toledo G, Fernandez-Chacon R & Fernandez JM (1993). Release of secretory products during transient vesicle fusion. Nature 363, 554-558.
4. Bai J, Tucker WC & Chapman ER (2004 a). PIP 2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane. Nature Struct Mol Biol 11, 36-44.
5. Bai J, Wang C-T, Richards DA, Jackson MB & Chapman ER (2004 b). Fusion pore dynamics are regulated by synaptotagmin-t-SNARE interactions. Neuron 41, 929-942.
6. Brose N, Petrenko AG, Südhof TC & Jahn R (1992). Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science 256, 1021-1025.
7. 2+ sensor that triggers exocytosis? Nature Rev Mol Cell Biol 3, 498-508.
8. Chow RH & Von Rüden L (1995). Electrochemical detection of secretion from single cells. In Single-Channel Recording, ed. Sakmann B & Neher E, pp. 245-275. Plenum Press, New York.
9. Colliver TL, Hess EJ, Pothos EN, Sulzer D & Ewing AG (2000). Quantitative and statistical analysis of the shape of amperometric spikes recorded from two populations of cells. J Neurochem 74, 1086-1097.
10. Colquhoun D & Sigworth F (1995). Fitting and statistical analysis of single channel records. In Single-Channel Recording, ed. Sakmann B & Neher E, pp. 483-587. Plenum Press, New York.
11. 2+-binding sites that cooperate to engage t-SNAREs and trigger exocytosis. J Cell Biol 154, 1117-1123.
12. Fernandez-Chacon R & Alvarez De Toledo G (1995). Cytosolic calcium facilitates release of secretory products after exocytotic vesicle fusion. FEBS Lett 363, 221-225.
13. Fernandez-Chacon R, Königstorfer A, Gerber SH, Garcia J, Matos MF, Stevens CF, Brose N, Rizo J, Rosenmund C & Südhof TC (2001). Synaptotagmin I functions as a calcium regulator of release probability. Nature 410, 41-49.
14. Fukuda M, Moreira JE, Lewis FM, Sugimori M, Niinobe M, Mikoshiba K & Llinas R (1995). Role of the C2B domain of synaptotagmin in vesicular release and recycling as determined by specific antibody injection into the squid giant synapse preterminal. Proc Natl Acad Sci 92, 10708-10712.
15. Haller M, Heinemann C, Chow RH, Heidelberger R & Neher E (1998). Comparison of secretory responses as measured by membrane capacitance and by amperometry. Biophys J 74, 2100-2113.
16. Hay J & Martin TFJ (1992). Resolution of regulated secretion into sequential MgATP-dependent and calcium-dependent stages mediated by distinct cytosolic proteins. J Cell Biol 119, 139-151.
17. Jahn R & Südhof TC (1999). Membrane fusion and exocytosis. Ann Rev Biochem 68, 863-911.
18. Klenchin VA, Kowalchyk JA & Martin TFJ (1998). Large dense-core vesicle exocytosis in PC12 cells. Methods 16, 204-208.
19. 2+ sensor for neurotransmitter release. Trends Neurosci 26, 413-422.
20. 2+-binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature 418, 340-344.
21. 2+-dependent neurotransmitter release. J Neurosci 24, 8542-8550.
22. Pawlu C, DeAntonio A & Heckmann M (2004). Postfusional control of quantal current shape. Neuron 42, 607-618.
23. Perin MS, Fried VA, Mignery GA, Jahn R & Südhof TC (1990). Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 345, 260-263.
24. 2+. J General Physiol 122, 265-276.
25. Stevens CF & Sullivan JM (2003). The synaptotagmin C2A domain is part of the calcium sensor controlling fast synaptic transmission. Neuron 39, 299-308.
26. 2+-regulated membrane fusion by synaptotagmin and SNAREs. Science 304, 435-438.
27. 2+ ions bind to the tip of a C2-domain? EMBO J 17, 3921-3930.
28. Wang C-T, Grishanin R, Earles CA, Chang P-Y, Martin TFJ, Chapman ER & Jackson MB (2001). Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science 294, 1111-1115.
29. Wang C-T, Lu J-C, Bai J, Chang P-Y, Martin TFJ, Chapman ER & Jackson MB (2003 a). Different domains of synaptotagmin control the choice between kiss-and-run and full fusion. Nature 424, 943-947.
30. Wang P, Wang C-T, Bai J, Jackson MB & Chapman ER (2003 b). Mutations in the effector binding loops in the C2A and C2B domains of synaptotagmin I disrupt exocytosis in a nonadditive manner. J Biol Chem 278, 47030-47037.
31. Wu Y, He Y, Bai J, Ji S, Tucker WC, Chapman ER & Sui S (2003). Visualization of synaptotagmin I oligomers assembled onto lipid monolayers. Proc Natl Acad Sci 100, 2082-2087.
32. Zhou Z, Misler S & Chow RH (1996). Rapid fluctuations in transmitter release from single vesicles in bovine adrenal chromaffin cells. Biophys J 70, 1543-1552.