The mouth of a dense-core vesicle opens and closes in a concerted action regulated by calcium and amphiphysin

Journal of Cell Biology

Volumn 182, Issue 5, 2008, Pages 1017-1028

  Llobet, Artur ^a,b   Wu, Minnie ^a,c   Lagnado, Leon ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITY OF BARCELONA   (Spain)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIPHYSIN; CALCIUM; DYNAMIN; STRONTIUM;

ANIMAL CELL; ARTICLE; ENDOCYTOSIS; LIGATION; MEMBRANE; MEMBRANE VESICLE; MICROSCOPY; MOUTH; MUTANT; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM;

ANIMALS; CALCIUM; CATTLE; CELLS, CULTURED; DYNAMINS; INTRACELLULAR MEMBRANES; MEMBRANE FUSION; MICROSCOPY, INTERFERENCE; NERVE TISSUE PROTEINS; SECRETORY VESICLES;

EID: 51649128866     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200807034     Document Type: Article

References (60)

1. Albillos, A., 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. 389:509-512.
2. Ales, E., L. Tabares, J.M. Poyato, V. Valero, M. Lindau, and G. Alvarez de Toledo. 1999. High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nat. Cell Biol. 1:40-44.
3. Artalejo, C.R., A. Elhamdani, and H.C. Palfrey. 2002. Sustained stimulation shifts the mechanism of endocytosis from dynamin-1-dependent rapid endocytosis to clathrin- and dynamin-2-mediated slow endocytosis in chromaffin cells. Proc. Natl. Acad. Sci. USA. 99:6358-6363.
4. Barer, R., and S. Joseph. 1954. Refractometry of living cells. Q. J. Microsc. Sci. 95:399-423.
5. Barg, S., C.S. Olofsson, J. Schriever-Abeln, A. Wendt, S. Gebre-Medhin, E. Renstrom, and P. Rorsman. 2002. Delay between fusion pore opening and peptide release from large dense-core vesicles in neuroendocrine cells. Neuron. 33:287-299.
6. Beaumont, V., A. Llobet, and L. Lagnado. 2005. Expansion of calcium microdomains regulates fast exocytosis at a ribbon synapse. Proc. Natl. Acad. Sci. USA. 102:10700-10705.
7. Becherer, U., M. Pasche, S. Nofal, D. Hof, U. Matti, and J. Rettig. 2007. Quantifying exocytosis by combination of membrane capacitance measurements and total internal reflection fluorescence microscopy in chromaffin cells. PLoS ONE. 2:e505.
8. Benedeczky, I. 1983. The functional morphology of chromaffin cells. Acta Biol. Hung. 34:137-154.
9. 2+ concentration to SNARE-mediated membrane fusion. Mol. Biol. Cell. 16:4755-4764.
10. Chow, R.H., L. von Ruden, and E. Neher. 1992. Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature. 356:60-63.
11. Elhamdani, A., F. Azizi, and C.R. Artalejo. 2006a. 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. J. Neurosci. 26:3030-3036.
12. Elhamdani, A., F. Azizi, E. Solomaha, H.C. Palfrey, and C.R. Artalejo. 2006b. Two mechanistically distinct forms of endocytosis in adrenal chromaffin cells: differential effects of SH3 domains and amphiphysin antagonism. FEBS Lett. 580:3263-3269.
13. Ellis-Davies, G.C., and J.H. Kaplan. 1994. Nitrophenyl-EGTA, a photolabile chelator that selectively binds Ca2+ with high affinity and releases it rapidly upon photolysis. Proc. Natl. Acad. Sci. USA. 91:187-191.
14. Felmy, F. 2007. Modulation of cargo release from dense core granules by size and actin network. Traffic. 8:983-997.
15. Fulop, T., and C. Smith. 2006. Physiological stimulation regulates the exocytic mode through calcium activation of protein kinase C in mouse chromaffin cells. Biochem. J. 399:111-119.
16. Fulop, T., S. Radabaugh, and C. Smith. 2005. Activity-dependent differential transmitter release in mouse adrenal chromaffin cells. J. Neurosci. 25:7324-7332.
17. Gad, H., N. Ringstad, P. Low, O. Kjaerulff, J. Gustafsson, M. Wenk, G. Di Paolo, Y. Nemoto, J. Crun, M.H. Ellisman, et al. 2000. Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron. 27:301-312.
18. Gingell, D., and I. Todd. 1979. Interference reflection microscopy. A quantitative theory for image interpretation and its application to cell-substratum separation measurement. Biophys. J. 26:507-526.
19. Gong, L.W., G.A. de Toledo, and M. Lindau. 2007. Exocytotic catecholamine release is not associated with cation flux through channels in the vesicle membrane but Na+ influx through the fusion pore. Nat. Cell Biol. 9:915-922.
20. Grynszpan-Winograd, O. 1971. Morphological aspects of exocytosin in the adrenal medulla. Philos. Trans. R. Soc. Lond. B Biol. Sci. 261:291-292.
21. Helmchen, F. 2000. Calibration of fluorescent calcium indicators. In Imaging Neurons: a Laboratory Manual. R. Yuste, E. Lanni, and A. Konnerth, editors. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 32.1-32.9.
22. Henkel, A.W., and W. Almers. 1996. Fast steps in exocytosis and endocytosis studied by capacitance measurements in endocrine cells. Curr. Opin. Neurobiol. 6:350-357.
23. Holroyd, P., T. Lang, D. Wenzel, P. De Camilli, and R. Jahn. 2002. Imaging direct, dynamin-dependent recapture of fusing secretory granules on plasma membrane lawns from PC12 cells. Proc. Natl. Acad. Sci. USA. 99:16806-16811.
24. Horrigan, F.T., and R.J. Bookman. 1994. Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron. 13:1119-1129.
25. Hurley, J.H., and B. Wendland. 2002. Endocytosis: driving membranes around the bend. Cell. 111:143-146.
26. Itoh, T., and P. De Camilli. 2006. BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim. Biophys. Acta. 1761:897-912.
27. Johns, L.M., E.S. Levitan, E.A. Shelden, R.W. Holz, and D. Axelrod. 2001. Restriction of secretory granule motion near the plasma membrane of chromaffin cells. J. Cell Biol. 153:177-190.
28. Lee, M.C., and R. Schekman. 2004. Cell biology. BAR domains go on a bender. Science. 303:479-480.
29. Lindau, M., and G. Alvarez de Toledo. 2003. The fusion pore. Biochim. Biophys. Acta. 1641:167-173.
30. Llobet, A., V. Beaumont, and L. Lagnado. 2003. Real-time measurement of exocytosis and endocytosis using interference of light. Neuron. 40:1075-1086.
31. McMahon, H.T., and J.L. Gallop. 2005. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature. 438:590-596.
32. Merrifield, C.J., M.E. Feldman, L. Wan, and W. Almers. 2002. Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat. Cell Biol. 4:691-698.
33. 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.
34. Nemoto, T., T. Kojima, A. Oshima, H. Bito, and H. Kasai. 2004. Stabilization of exocytosis by dynamic F-actin coating of zymogen granules in pancreatic acini. J. Biol. Chem. 279:37544-37550.
35. Neves, G., and L. Lagnado. 1999. The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells. J. Physiol. 515:181-202.
36. Patzak, A., and H. Winkler. 1986. Exocytotic exposure and recycling of membrane antigens of chromaffin granules: ultrastructural evaluation after immunolabeling. J. Cell Biol. 102:510-515.
37. Perrais, D., and C.J. Merrifield. 2005. Dynamics of endocytic vesicle creation. Dev. Cell. 9:581-592.
38. Perrais, D., I. Kleppe, J. Taraska, and W. Almers. 2004. Recapture after exocytosis causes differential retention of protein in granules of bovine chromaffin cells. J. Physiol. 560:413-428.
39. Peter, B.J., H.M. Kent, I.G. Mills, Y. Vallis, P.J. Butler, P.R. Evans, and H.T. McMahon. 2004. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science. 303:495-499.
40. Praefcke, G.J., and H.T. McMahon. 2004. The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell Biol. 5:133-147.
41. Rettig, J., and E. Neher. 2002. Emerging roles of presynaptic proteins in Ca++-triggered exocytosis. Science. 298:781-785.
42. Schmidt, W., A. Patzak, G. Lingg, H. Winkler, and H. Plattner. 1983. Membrane events in adrenal chromaffin cells during exocytosis: a freeze-etching analysis after rapid cryofixation. Eur. J. Cell Biol. 32:31-37.
43. 2+ binding site of synaptotagmin 1 C2B domain triggers fast exocyosis without stimulating SNARE interactions. Neuron. 37:99-108.
44. Smith, C., and E. Neher. 1997. Multiple forms of endocytosis in bovine adrenal chromaffin cells. J. Cell Biol. 139:885-894.
45. Steyer, J.A., H. Horstmann, and W. Almers. 1997. Transport, docking and exocytosis of single secretory granules in live chromaffin cells. Nature. 388:474-478.
46. Sudhof, T.C. 2002. Synaptotagmins: why so many? J. Biol. Chem. 277:7629-7632.
47. Takei, K., P.S. McPherson, S.L. Schmid, and P. De Camilli. 1995. Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature. 374:186-190.
48. Takei, K., V.I. Slepnev, V. Haucke, and P. De Camilli. 1999. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell Biol. 1:33-39.
49. Taraska, J.W., and W. Almers. 2004. Bilayers merge even when exocytosis is transient. Proc. Natl. Acad. Sci. USA. 101:8780-8785.
50. Taraska, J.W., D. Perrais, M. Ohara-Imaizumi, S. Nagamatsu, and W. A lmers. 2003. Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells. Proc. Natl. Acad. Sci. USA. 100:2070-2075.
51. Tsuboi, T., and G.A. Rutter. 2003. Multiple forms of "kiss-and- run" exocytosis revealed by evanescent wave microscopy. Curr. Biol. 13:563-567.
52. 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.
53. Verschueren, H. 1985. Interference reflection microscopy in cell biology: methodology and applications. J. Cell Sci. 75:279-301.
54. Wang, C.T., R. Grishanin, C.A. Earles, P.Y. Chang, T.F. Martin, E.R. Chapman, and M.B. Jackson. 2001. Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science. 294:1111-1115.
55. Wang, C.T., J.C. Lu, J. Bai, P.Y. Chang, T.F. Martin, E.R. Chapman, and M.B. Jackson. 2003. Different domains of synaptotagmin control the choice between kiss-and-run and full fusion. Nature. 424:943-947.
56. Weber, I. 2003. Reflection interference contrast microscopy. Methods Enzymol. 361:34-47.
57. Wigge, P., K. Kohler, Y. Vallis, C.A. Doyle, D. Owen, S.P. Hunt, and H.T. McMahon. 1997. Amphiphysin heterodimers: potential role in clathrin-mediated endocytosis. Mol. Biol. Cell. 8:2003-2015.
58. Yamada, H., E. Ohashi, T. Abe, N. Kusumi, S.A. Li, Y. Yoshida, M. Watanabe, K. Tomizawa, Y. Kashiwakura, H. Kumon, et al. 2007. Amphiphysin 1 is important for actin polymerization during phagocytosis. Mol. Biol. Cell. 18:4669-4680.
59. Yoshida, Y., M. Kinuta, T. Abe, S. Liang, K. Araki, O. Cremona, G. Di Paolo, Y. Moriyama, T. Yasuda, P. De Camilli, and K. Takei. 2004. The stimulatory action of amphiphysin on dynamin function is dependent on lipid bilayer curvature. EMBO J. 23:3483-3491.
60. Yu, H.Y., and W.M. Bement. 2007. Control of local actin assembly by membrane fusion-dependent compartment mixing. Nat. Cell Biol. 9:149-159.