Compensatory endocytosis in chromaffin cells

Acta Physiologica

Volumn 192, Issue 2, 2008, Pages 195-201

  Barg, S ^a   Machado, J D ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSIDAD DE LA LAGUNA   (Spain)

Author keywords

Capacitance; Clathrin; Dynamin; Exocytosis; Fluorescence microscopy; Secretion

Indexed keywords

MEMBRANE PROTEIN;

ADRENAL CELL; CELL GRANULE; CHROMAFFIN CELL; CONFERENCE PAPER; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; PRIORITY JOURNAL; SECRETION;

ANIMALS; CELL MEMBRANE; CELLS, CULTURED; CHROMAFFIN CELLS; CHROMAFFIN GRANULES; ELECTROPHYSIOLOGY; ENDOCYTOSIS; HUMANS; MEMBRANE FUSION;

EID: 38549087820     PISSN: 17481708     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2007.01813.x     Document Type: Conference Paper

References (63)

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, J.M., Valero, V., Lindau, M. Alvarez de Toledo, G. 1999. High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nat Cell Biol 1, 40 44.
3. Allersma, M.W., Wang, L., Axelrod, D. Holz, R.W. 2004. Visualization of regulated exocytosis with a granule-membrane probe using total internal reflection microscopy. Mol Biol Cell 15, 4658 4668.
4. Alvarez de Toledo, G., Fernandez-Chacon, R. Fernandez, J.M. 1993. Release of secretory products during transient vesicle fusion. Nature 363, 554 558.
5. Aravanis, A.M., Pyle, J.L. Tsien, R.W. 2003. Single synaptic vesicles fusing transiently and successively without loss of identity. Nature 423, 643 647.
6. 2+, GTP, and dynamin but not clathrin. Proc Natl Acad Sci USA 92, 8328 8332.
7. Artalejo, C.R., Elhamdani, A. Palfrey, H.C. 1996. Calmodulin is the divalent cation receptor for rapid endocytosis, but not exocytosis, in adrenal chromaffin cells. Neuron 16, 195 205.
8. Artalejo, C.R., Elhamdani, A. Palfrey, H.C. 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.
9. Barg, S., Olofsson, C.S., Schriever-Abeln, J., Wendt, A., Gebre-Medhin, S., Renstrom, E. Rorsman, P. 2002. Delay between fusion pore opening and peptide release from large dense-core vesicles in neuroendocrine cells. Neuron 33, 287 299.
10. Bauer, R.A., Khera, R.S., Lieber, J.L. Angleson, J.K. 2004. Recycling of intact dense core vesicles in neurites of NGF-treated PC12 cells. FEBS Lett 571, 107 111.
11. Bauerfeind, R., Takei, K. De Camilli, P. 1997. Amphiphysin I is associated with coated endocytic intermediates and undergoes stimulation-dependent dephosphorylation in nerve terminals. J Biol Chem 272, 30984 30992.
12. 2+ current run-down. Pflugers Arch 430, 213 219.
13. Burgoyne, R.D. 1998. Two forms of triggered endocytosis in regulated secretory cells. J Physiol 506, 589.
14. Ceccarelli, B., Hurlbut, W.P. Mauro, A. 1973. Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol 57, 499 524.
15. Chan, S.A. Smith, C. 2001. Physiological stimuli evoke two forms of endocytosis in bovine chromaffin cells. J Physiol 537, 871 885.
16. Chan, S.A. Smith, C. 2003. Low frequency stimulation of mouse adrenal slices reveals a clathrin-independent, protein kinase C-mediated endocytic mechanism. J Physiol 553, 707 717.
17. Dernick, G., Alvarez de Toledo, G. Lindau, M. 2003. Exocytosis of single chromaffin granules in cell-free inside-out membrane patches. Nat Cell Biol 5, 358 362.
18. Elhamdani, A., Palfrey, H.C. Artalejo, C.R. 2001. Quantal size is dependent on stimulation frequency and calcium entry in calf chromaffin cells. Neuron 31, 819 830.
19. Eliasson, L., Proks, P., Ammala, C., Ashcroft, F.M., Bokvist, K., Renstrom, E., Rorsman, P. Smith, P.A. 1996. Endocytosis of secretory granules in mouse pancreatic beta-cells evoked by transient elevation of cytosolic calcium. J Physiol 493, 755 767.
20. Engisch, K.L. Nowycky, M.C. 1998. Compensatory and excess retrieval: two types of endocytosis following single step depolarizations in bovine adrenal chromaffin cells. J Physiol 506, 591 608.
21. Felmy, F. 2007. Modulation of cargo release from dense core granules by size and actin network. Traffic 8, 983 997.
22. Fulop, T., Radabaugh, S. Smith, C. 2005. Activity-dependent differential transmitter release in mouse adrenal chromaffin cells. J Neurosci 25, 7324 7332.
23. von Grafenstein, H. Knight, D.E. 1992. Membrane recapture and early triggered secretion from the newly formed endocytotic compartment in bovine chromaffin cells. J Physiol 453, 15 31.
24. von Grafenstein, H. Knight, D.E. 1993. Triggered exocytosis and endocytosis have different requirements for calcium and nucleotides in permeabilized bovine chromaffin cells. J Membr Biol 134, 1 13.
25. Graham, M.E., O'Callaghan, D.W., McMahon, H.T. Burgoyne, R.D. 2002. Dynamin-dependent and dynamin-independent processes contribute to the regulation of single vesicle release kinetics and quantal size. Proc Natl Acad Sci USA 99, 7124 7129.
26. Grass, I., Thiel, S., Honing, S. Haucke, V. 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.
27. Grote, E. Kelly, R.B. 1996. Endocytosis of VAMP is facilitated by a synaptic vesicle targeting signal. J Cell Biol 132, 537 547.
28. Haucke, V. De Camilli, P. 1999. AP-2 recruitment to synaptotagmin stimulated by tyrosine-based endocytic motifs. Science 285, 1268 1271.
29. Henkel, A.W., Meiri, H., Horstmann, H., Lindau, M. Almers, W. 2000. Rhythmic opening and closing of vesicles during constitutive exo- and endocytosis in chromaffin cells. EMBO J 19, 84 93.
30. Henkel, A.W., Horstmann, H. Henkel, M.K. 2001. Direct observation of membrane retrieval in chromaffin cells by capacitance measurements. FEBS Lett 505, 414 418.
31. Heuser, J.E. Reese, T.S. 1973. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57, 315 344.
32. Holroyd, P., Lang, T., Wenzel, D., De Camilli, P. Jahn, R. 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.
33. Kasai, H., Kishimoto, T., Nemoto, T., Hatakeyama, H., Liu, T.T. Takahashi, N. 2006. Two-photon excitation imaging of exocytosis and endocytosis and determination of their spatial organization. Adv Drug Deliv Rev 58, 850 877.
34. 2+-triggered peptide secretion in single cells imaged with green fluorescent protein and evanescent-wave microscopy. Neuron 18, 857 863.
35. Liu, T.T., Kishimoto, T., Hatakeyama, H., Nemoto, T., Takahashi, N. Kasai, H. 2005. Exocytosis and endocytosis of small vesicles in PC12 cells studied with TEPIQ (two-photon extracellular polar-tracer imaging-based quantification) analysis. J Physiol 568, 917 929.
36. MacDonald, P.E., Obermuller, S., Vikman, J., Galvanovskis, J., Rorsman, P. Eliasson, L. 2005. Regulated exocytosis and kiss-and-run of synaptic-like microvesicles in INS-1 and primary rat beta-cells. Diabetes 54, 736 743.
37. Machado, J.D., Gomez, J.F., Betancor, G., Camacho, M., Brioso, M.A. Borges, R. 2002. Hydralazine reduces the quantal size of secretory events by displacement of catecholamines from adrenomedullary chromaffin secretory vesicles. Circ Res 91, 830 836.
38. Merrifield, C.J., Feldman, M.E., Wan, L. Almers, W. 2002. Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4, 691 698.
39. Neher, E. Marty, A. 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.
40. Neher, E. Zucker, R.S. 1993. Multiple calcium-dependent processes related to secretion in bovine chromaffin cells. Neuron 10, 21 30.
41. Nucifora, P.G. Fox, A.P. 1998. Barium triggers rapid endocytosis in calf adrenal chromaffin cells. J Physiol 508 (Pt 2 483 494.
42. Nucifora, P.G. Fox, A.P. 1999. Tyrosine phosphorylation regulates rapid endocytosis in adrenal chromaffin cells. J Neurosci 19, 9739 9746.
43. Obermuller, S., Lindqvist, A., Karanauskaite, J., Galvanovskis, J., Rorsman, P. Barg, S. 2005. Selective nucleotide-release from dense-core granules in insulin-secreting cells. J Cell Sci 118, 4271 4282.
44. Oomori, Y., Okuno, S., Fujisawa, H., Satoh, T. Ono, K. 1991. Exocytosis in pheochromocytoma cells after exposure to a high concentration of potassium. Acta Anat (Basel) 140, 280 283.
45. Patzak, A. Winkler, H. 1986. Exocytotic exposure and recycling of membrane antigens of chromaffin granules: ultrastructural evaluation after immunolabeling. J Cell Biol 102, 510 515.
46. Patzak, A., Aunis, D. Langley, K. 1987. Membrane recycling after exocytosis: an ultrastructural study of cultured chromaffin cells. Exp Cell Res 171, 346 356.
47. Perrais, D. Merrifield, C.J. 2005. Dynamics of endocytic vesicle creation. Dev Cell 9, 581 592.
48. Perrais, D., Kleppe, I.C., Taraska, J.W. Almers, W. 2004. Recapture after exocytosis causes differential retention of protein in granules of bovine chromaffin cells. J Physiol 560, 413 428.
49. Phillips, J.H., Burridge, K., Wilson, S.P. Kirshner, N. 1983. Visualization of the exocytosis/endocytosis secretory cycle in cultured adrenal chromaffin cells. J Cell Biol 97, 1906 1917.
50. Rosa, J.M., de Diego, A.M., Gandia, L. Garcia, A.G. 2007. L-type calcium channels are preferentially coupled to endocytosis in bovine chromaffin cells. Biochem Biophys Res Commun 357, 834 839.
51. Rutter, G.A. Tsuboi, T. 2004. Kiss and run exocytosis of dense core secretory vesicles. Neuroreport 15, 79 81.
52. Ryan, T.A. 2003. Kiss-and-run, fuse-pinch-and-linger, fuse-and-collapse: the life and times of a neurosecretory granule. Proc Natl Acad Sci USA 100, 2171 2173.
53. Sampo, B., Kaech, S., Kunz, S. Banker, G. 2003. Two distinct mechanisms target membrane proteins to the axonal surface. Neuron 72, 611 624.
54. Smillie, K.J. Cousin, M.A. 2005. Dynamin I phosphorylation and the control of synaptic vesicle endocytosis. Biochem Soc Symp 72, 87 97.
55. Smith, C. Neher, E. 1997. Multiple forms of endocytosis in bovine adrenal chromaffin cells. J Cell Biol 139, 885 894.
56. Staal, R.G., Mosharov, E.V. Sulzer, D. 2004. Dopamine neurons release transmitter via a flickering fusion pore. Nat Neurosci 7, 341 346.
57. Tabares, L., Ales, E., Lindau, M. Alvarez de Toledo, G. 2001. Exocytosis of catecholamine (CA)-containing and CA-free granules in chromaffin cells. J Biol Chem 276, 39974 39979.
58. Taraska, J.W. Almers, W. 2004. Bilayers merge even when exocytosis is transient. Proc Natl Acad Sci USA 101, 8780 8785.
59. Taraska, J.W., Perrais, D., Ohara-Imaizumi, M., Nagamatsu, S. Almers, W. 2003. Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells. Proc Natl Acad Sci USA 100, 2070 2075.
60. 2+-stimulated exocytosis in single pituitary cells. J Cell Biol 124, 667 675.
61. Tsuboi, T., McMahon, H.T. Rutter, G.A. 2004. Mechanisms of dense core vesicle recapture following 'kiss and run' ('cavicapture') exocytosis in insulin-secreting cells. J Biol Chem 279, 47115 47124.
62. Viveros, O.H. Wilson, S.P. 1983. The adrenal chromaffin cell as a model to study the co-secretion of enkephalins and catecholamines. J Auton Nerv Syst 7, 41 58.
63. Zhou, Z., Misler, S. Chow, R.H. 1996. Rapid fluctuations in transmitter release from single vesicles in bovine adrenal chromaffin cells. Biophys J 70, 1543 1552.