Synaptotagmin IV Modulation of Vesicle Size and Fusion Pores in PC12 Cells

Biophysical Journal

Volumn 98, Issue 6, 2010, Pages 968-978

  Zhang, Zhenjie ^a,b   Zheng, Zhen ^a   Jackson, Meyer B ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA C VIRUS;

EID: 77949589647     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.11.024     Document Type: Article

References (40)

1. 2+-dependent phospholipid binding to the C2A domain of synaptotagmin IV. J. Biol. Chem. 271:8430-8434.
2. 2+ binding. J. Biol. Chem. 272:14314-14319.
3. Wang, P., C. T. Wang, ..., E. R. Chapman. 2003. 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.
4. 2+ binding to synaptotagmin 4. Nat. Struct. Mol. Biol. 11:844-849.
5. Zhang, Z., A. Bhalla, ..., M. B. Jackson. 2009. Synaptotagmin IV: a multifunctional, regulator of peptidergic nerve terminals. Nat. Neurosci. 12:163-171.
6. Pawlu, C., A. DiAntonio, and M. Heckmann. 2004. Postfusional control of quanta! current shape. Neuron. 42:607-618.
7. Dean, C., H. Liu, ..., E. R. Chapman. 2009. Synaptotagmin-IV modulates synaptic function and long-term potentiation by regulating BDNF release. Nat. Neurosci. 12:767-776.
8. Wang, C. T., J. C. Lu, ..., M. B. Jackson. 2003. Different domains of synaptotagmin control the choice between kiss-and-run and full fusion, Nature. 424:943-947.
9. Wang, C-T., R. Grishanin, ..., M. B. Jackson. 2001. Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of densecore vesicles. Science. 294:1111-1115.
10. Clements, J. D. 1996. Transmitter timecourse in the synaptic cleft: its role in central synaptic function. Trends Neurosci. 19:163-1.71.
11. Jackson, M. B. 2007. In search of the fusion pore of exocytosis. Biophys. Chem. 126:201-208.
12. Stiles, J. R., D. Van Helden, ..., M. M. Salpeter. 1996. Miniature endplate current rise times less than 100 microseconds from improved dual recordings can be modeled with passive acetylcholine diffusion from a synaptic vesicle. Proc. Natl. Acad. Sci. USA. 93:5747-5752.
13. Fulop, T., S. Radabaugh, and C. Smith. 2005. Activity-dependent differential, transmitter release in mouse adrenal chromaffin cells. J. Neurosci. 25:7324-7332.
14. Tucker, W. C., J. M. Edwardson, ..., E. R. Chapman. 2003. Identification of synaptotagmin effectors via acute inhibition of secretion from cracked PC12 cells. J. Cell Biol. 162:199-209.
15. Hay, J. C., and T. F. J. Martin. 1992. Resolution of regulated secretion into sequential MgATP-dependent and calcium-dependent stages mediated by distinct cytosolic proteins. J. Cell Biol. 119:139-151.
16. Debus, K., and M. Lindau. 2000. Resolution of patch capacitance recordings and of fusion pore conductances in small vesicles. Biophys. J. 78:2983-2997.
17. Klyachko, V., Z. Zhang, and M. B. Jackson, 2007. Low-noise recording of single vesicle capacitance steps in cell-attached membrane patches. In Methods in Molecular Biology: Exocytosis and Endocytosis Methods and Protocols. A. I. Ivanov, editor. Humana Press, Totowa, NJ.
18. Lindau, M. 1991. Time-resolved capacitance measurements: monitoring exocytosis in single cells. Q. Rev. Biophys. 24:75-101.
19. Lollike, K., N. Borregaard, and M. Lindau. 1995. The exocytotic fusion pore of small granules has a conductance similar to an ion channel. J. Cell Biol. 129:99-104.
20. Jackson, M. B. 2006. Molecular and Cellular Biophysics. Cambridge University Press, Cambridge.
21. Bauerfeind, R., A. Régnier-Vigouroux, ..., W. B. Huttner. 1993. Selective storage of acetylcholine, but not catecholamines, in neuroendocrine synaptic-like microvesicles of early endosomal origin. Neuron. 1.1: 105-121.
22. Gentet, L. J., G. J. Stuart, and J. D. Clements. 2000. Direct measurement of specific membrane capacitance in neurons. Biophys. J. 79:314-320.
23. Neher, E., and A. Marty. 1982. Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc. Natl. Acad. Sci. USA. 79:6712-6716.
24. Fernandez, J. M., E. Neher, and B. D. Gomperts. 1984. Capacitance measurements reveal stepwise fusion events in degranulating mast cells. Nature. 312:453-455.
25. Klyachko, V. A., and M. B. Jackson. 2002. Capacitance steps and fusion pores of small and large-dense-core vesicles in nerve terminals. Nature. 418:89-92.
26. He, L., X.-S. Wu, ..., L. G. Wu. 2006. Two modes of fusion pore opening revealed by cell-attached recordings at a synapse. Nature. 444:102-105.
27. Chizmadzhev, Y. A., P. I. Kuzmin, ..., F. S. Cohen. 2000. Dynamics of fusion pores connecting membranes of different tensions. Biophys. J. 78:2241-2256.
28. Jackson, M. B., and E. R. Chapman. 2008. The fusion pores of Ca(2+)-triggered exocytosis. Nat. Struct. Mol. Biol. 15:684-689.
29. 2+ triggers two sequential steps in regulated exocytosis in rat PC12 cells: fusion pore opening and fusion pore dilation. J. Physiol. 570:295-307.
30. Eaton, B. A., M. Haugwitz, ..., H. P. Moore. 2000. Biogenesis of regulated exocytotic carriers in neuroendocrine cells. J. Neurosci. 20:7334-7344.
31. Albulos, A., G. Dernick, ..., M. Lindau. 1997. The exocytotic event in chromaffin cells revealed by patch amperometry. Nature. 389:509-512.
32. Han, X., and M. B. Jackson. 2005. Electrostatic interactions between the syntaxin membrane anchor and neurotransmitter passing through the fusion pore. Biophys. J. 88:L20-L22.
33. 2+-triggered exocytosis. Science. 304:289-292.
34. Montecucco, C., G. Schiavo, and S. Pantano. 2005. SNARE complexes and neuroexocytosis: how many, how close? Trends Biochem. Sci. 30:367-372.
35. Hua, Y., and R. H. Scheller. 2001. Three SNARE complexes cooperate to mediate membrane fusion. Proc. Natl. Acad. Sci. USA. 98:8065-8070.
36. Jaiswal, J. K., V. M. Rivera, and S. M. Simon, 2009. Exocytosis of postGolgi vesicles is regulated by components of the endocytic machinery. Cell. 137:1308-1319.
37. Tsuboi, T., H. T. McMahon, and G. A. Rutter. 2004. Mechanisms of dense core vesicle recapture following "kiss and run" (" cavicapture") exocytosis in insulin-secreting cells. J. Biol. Chem. 279:47115-47124.
38. Grass, I., S. Thiel, ..., V. Haucke. 2004. Recognition of a basic AP-2 binding motif within the C2B domain of synaptotagmin is dependent on multimerization. J. Biol. Chem. 279:54872-54880.
39. Takei, K., and V. Haucke. 2001. Clathrin-mediated endocytosis: membrane factors pull the trigger. Trends Cell Biol. 11:385-391.
40. Poskanzer, K. E., K. W. Marek, ..., G. W. Davis. 2003. Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature. 426:559-563.