Measuring secretion in chromaffin cells using electrophysiological and electrochemical methods

Acta Physiologica

Volumn 192, Issue 2, 2008, Pages 173-184

  Borges, R ^a   Camacho, M ^a   Gillis, K D ^b  

^a UNIVERSIDAD DE LA LAGUNA   (Spain)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Adrenal; Amperometry; Catecholamine; Cell capacitance; Exocytosis; Patch amperometry

Indexed keywords

AMPEROMETRY; CAPACITANCE BLOOD VESSEL; CELL SECRETION; CHROMAFFIN CELL; CONFERENCE PAPER; ELECTROCHEMISTRY; ELECTROPHYSIOLOGY; ENDOCYTOSIS; EXOCYTOSIS; PRIORITY JOURNAL;

ANIMALS; CELLS, CULTURED; CHROMAFFIN CELLS; CHROMAFFIN GRANULES; ELECTROPHYSIOLOGY; EXOCYTOSIS; HUMANS; PATCH-CLAMP TECHNIQUES;

EID: 38549178798     PISSN: 17481708     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2007.01814.x     Document Type: Conference Paper

References (145)

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. 2+ channels are coupled to the rapid component of secretion in mouse adrenal slice chromaffin cells. J Neurosci 20, 8323 8330.
3. Aldea, M., Jun, K., Shin, H.S., Andres-Mateos, E., Solis-Garrido, L.M., Montiel, C. et al. 2002. A perforated patch-clamp study of calcium currents and exocytosis in chromaffin cells of wild-type and alpha(1A) knockout mice. J Neurochem 81, 911 921.
4. 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.
5. Alvarez de Toledo, G., Fernandez-Chacon, R. Fernandez, J.M. 1993. Release of secretory products during transient vesicle fusion. Nature, 363, 554 558.
6. Amatore, C., Bouret, Y., Travis, E.R. Wightman, R.M. 2000. Adrenaline release by chromaffin cells: constrained swelling of the vesicle matrix leads to full fusion. Angew Chem Int Ed, 39, 1952.
7. Amatore, C., Arbault, S., Chen, Y., Crozatier, C., Lemaitre, F. Verchier, Y. 2006. Coupling of electrochemistry and fluorescence microscopy at indium tin oxide microelectrodes for the analysis of single exocytotic events. Angew Chem Int Ed Engl, 45, 4000 4003.
8. Archer, D.A., Graham, M.E. Burgoyne, R.D. 2002. Complexin regulates the closure of the fusion pore during regulated vesicle exocytosis. J Biol Chem, 277, 18249 18252.
9. Artalejo, C.R., Adams, M.E. Fox, A.P. 1994. Three types of Ca2+ channel trigger secretion with different efficacies in chromaffin cells. Nature 367, 72 76.
10. 2+, GTP, and dynamin but not clathrin. Proc Natl Acad Sci USA, 92, 8328 8332.
11. Artalejo, C.R., Elhamadani, 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.
12. Augustine, G.J. Neher, E. 1992. Calcium requirements for secretion in bovine chromaffin cells. J Physiol, 450, 247 271.
13. Barclay, J.W., Aldea, M., Craig, T.J., Morgan, A. Burgoyne, R.D. 2004. Regulation of the fusion pore conductance during exocytosis by cyclin-dependent kinase 5. J Biol Chem, 279, 41495 41503.
14. Barnett, D.W. Misler, S. 1997. An optimized approach to membrane capacitance estimation using dual-frequency excitation. Biophys J, 72, 1641 1658.
15. Bauer, C.S., Woolley, R.J., Teschemacher, A.G. Seward, E.P. 2007. Potentiation of exocytosis by phospholipase C-coupled G-protein-coupled receptors requires the priming protein Munc13-1. J Neurosci 27, 212 219.
16. Borges, R., Travis, E.R., Hochstetler, S.E. Wightman, R.M. 1997. Effects of external osmotic pressure on vesicular secretion from bovine adrenal medullary cells. J Biol Chem, 272, 8325 8331.
17. Breckenridge, L.J. Almers, W. 1987. Currents through the fusion pore that forms during exocytosis of a secretory vesicle. Nature, 328, 814 817.
18. Brede, M., Nagy, G., Philipp, M., Sorensen, J.B., Lohse, M.J. Hein, L. 2003. Differential control of adrenal and sympathetic catecholamine release by alpha 2-adrenoceptor subtypes. Mol Endocrinol 17, 1640 1646.
19. Cahill, P.S. Wightman, R.M. 1995. Simultaneous amperometric measurement of ascorbate and catecholamine secretion from individual bovine adrenal-medullary cells. Anal Chem, 67, 2599 2605.
20. Camacho, M., Machado, J.D., Montesinos, M.S., Criado, M. Borges, R. 2006. Intragranular pH rapidly modulates exocytosis in adrenal chromaffin cells. J Neurochem, 96, 324 334.
21. Carabelli, V., Giancippoli, A., Baldelli, P., Carbone, E. Artalejo, A.R. 2003. Distinct potentiation of L-type currents and secretion by cAMP in rat chromaffin cells. Biophys J, 85, 1326 1337.
22. Chan, S.A. Smith, C. 2001. Physiological stimuli evoke two forms of endocytosis in bovine chromaffin cells. J Physiol, 537, 871 885.
23. 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.
24. Chen, P., Hwang, T.C. Gillis, K.D. 2001. The relationship between cAMP, Ca(2)+, and transport of CFTR to the plasma membrane. J Gen Physiol, 118, 135 144.
25. Chen, P., Xu, B., Tokranova, N., Feng, X., Castracane, J. Gillis, K.D. 2003. Amperometric detection of quantal catecholamine secretion from individual cells on micromachined silicon chips. Anal Chem, 75, 518 524.
26. Chow, R.H., von Ruden, L. Neher, E. 1992a. Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature, 356, 60 63.
27. Chow, R.H., Klingauf, J. Neher, E. 1994. Time course of Ca2+ concentration triggering exocytosis in neuroendocrine cells. Proc Natl Acad Sci USA, 91, 12765 12769.
28. Chow, R.H., Klingauf, J., Heinemann, C., Zucker, R.S. Neher, E. 1996. Mechanisms determining the time course of secretion in neuroendocrine cells. Neuron, 16, 369 376.
29. Ciolkowski, E.L., Cooper, B.R., Jankowski, J.A., Jorgenson, J.W. Wightman, R.M. 1992. Direct observation of epinephrine and norepinephrine cosecretion from individual adrenal-medullary chromaffin cells. J Am Chem Soc, 114, 2815 2821.
30. Cole, K.S. 1935. Electrical impedance of Hipponoe eggs. J Gen Physiol, 18, 877 887.
31. Colliver, T.L., Pyott, S.J., Achalabun, M. Ewing, A.G. 2000. VMAT-mediated changes in quantal size and vesicular volume. J Neurosci, 20, 5276 5282.
32. Coorssen, J.R., Schmitt, H. Almers, W. 1996. Ca2+ triggers massive exocytosis in Chinese hamster ovary cells. EMBO J, 15, 3787 3791.
33. Criado, M., Gil, A., Viniegra, S. Gutierrez, L.M. 1999. A single amino acid near the C terminus of the synaptosomeassociated protein of 25 kDa (SNAP-25) is essential for exocytosis in chromaffin cells. Proc Natl Acad Sci USA, 96, 7256 7261.
34. Debus, K. Lindau, M. 2000. Resolution of patch capacitance recordings and of fusion pore conductances in small vesicles. Biophys J, 78, 2983 2997.
35. 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.
36. Dernick, G., Gong, L.W., Tabares, L., de Toledo, G.A. Lindau, M. 2005. Patch amperometry: high-resolution measurements of single-vesicle fusion and release. Nat Methods, 2, 699 708.
37. Dias, A.F., Dernick, G., Valero, V., Yong, M.G., James, C.D., Craighead, H.G. Lindau, M. 2002. An electrochemical detector array to study cell biology on the nanoscale. Nanotechnology, 13, 285 289.
38. Donnelly, D.F. 1994. A novel method for rapid measurement of membrane resistance, capacitance, and access resistance. Biophys J, 66, 873 877.
39. Elhamdani, A., Zhou, Z. Artalejo, C.R. 1998. Timing of dense-core vesicle exocytosis depends on the facilitation L-type Ca channel in adrenal chromaffin cells. J Neurosci, 18, 6230 6240.
40. Elhamdani, A., Martin, T.F., Kowalchyk, J.A. Artalejo, C.R. 1999. Ca(2+)-dependent activator protein for secretion is critical for the fusion of dense-core vesicles with the membrane in calf adrenal chromaffin cells. J Neurosci 19, 7375 7383.
41. 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.
42. Elhamdani, A., Azizi, F. Artalejo, C.R. 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.
43. Elhamdani, A., Azizi, F., Solomaha, E., Palfrey, H.C. Artalejo, C.R. 2006b. Two mechanistically distinct forms of endocytosis in adrenal chromaffin cells: differential effects of SH3 domains and amphiphysin antagonism. FEBS Lett, 580, 3263 3269.
44. Engisch, K.L. Nowycky, M.C. 1996. Calcium dependence of large dense-cored vesicle exocytosis evoked by calcium influx in bovine adrenal chromaffin cells. J Neurosci 16, 1359 1369.
45. 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.
46. Engisch, K.L., Chernevskaya, N.I. Nowycky, M.C. 1997. Short-term changes in the Ca2+-exocytosis relationship during repetitive pulse protocols in bovine adrenal chromaffin cells. J Neurosci 17, 9010 9025.
47. Ennion, S.J., Powell, A.D. Seward, E.P. 2004. Identification of the P2Y(12) receptor in nucleotide inhibition of exocytosis from bovine chromaffin cells. Mol Pharmacol 66, 601 611.
48. Fidler, N. Fernandez, J.M. 1989. Phase tracking: an improved phase detection technique for cell membrane capacitance measurements. Biophys J, 56, 1153 1162.
49. Fomina, A.F. Nowycky, M.C. 1999. A current activated on depletion of intracellular Ca2+ stores can regulate exocytosis in adrenal chromaffin cells. J Neurosci 19, 3711 3722.
50. Fulop, T. Smith, C. 2006. Physiological stimulation regulates the exocytic mode through calcium activation of protein kinase C in mouse chromaffin cells. Biochem J 399, 111 119.
51. von Gersdorff, H. Matthews, G. 1994. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature, 367, 735 739.
52. Gillis, K.D. 1995. Techniques for membrane capacitance measurements. In : B. Sakmann E. Neher (eds) Single-channel Recording, 2nd edn. Plenum Press, New York and London. pp. 155 198.
53. Gillis, K.D. 2000. Admittance-based measurement of membrane capacitance using the EPC-9 patch-clamp amplifier. Pflugers Arch, 439, 655 664.
54. Gillis, K.D., 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.
55. Gomez, J.F., Brioso, M.A., Machado, J.D., Sanchez, J.L. Borges, R. 2002. New approaches for analysis of amperometrical recordings. Chromaffin Cell: Transmitter Biosynthesis, Storage, Release, Actions, and Informatics. Ann Ny Acad Sci, 971, 647 654.
56. Gong, L.W., Hafez, I., Alvarez de Toledo, G. Lindau, M. 2003. Secretory vesicles membrane area is regulated in tandem with quantal size in chromaffin cells. J Neurosci, 23, 7917 7921.
57. Graham, M.E. Burgoyne, R.D. 2000. Comparison of cysteine string protein (Csp) and mutant alpha-SNAP overexpression reveals a role for Csp in late steps of membrane fusion in dense-core granule exocytosis in adrenal chromaffin cells. J Neurosci, 20, 1281 1289.
58. Graham, M.E., Fisher, R.J. Burgoyne, R.D. 2000. Measurement of exocytosis by amperometry in adrenal chromaffin cells: effects of clostridial neurotoxins and activation of protein kinase C on fusion pore kinetics. Biochimie, 82, 469 479.
59. Graham, M.E., Washbourne, P., Wilson, M.C. Burgoyne, R.D. 2001. SNAP-25 with mutations in the zero layer supports normal membrane fusion kinetics. J Cell Sci, 114, 4397 4405.
60. 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.
61. Graham, M.E., Barclay, J.W. Burgoyne, R.D. 2004. Syntaxin/Munc18 interactions in the late events during vesicle fusion and release in exocytosis. J Biol Chem, 279, 32751 32760.
62. Gutierrez, L.M., Gil, A. Viniegra, S. 1998. Preferential localization of exocytotic active zones in the terminals of neurite-emitting chromaffin cells. Eur J Cell Biol, 76, 274 278.
63. Hafez, I., Kisler, K., Berberian, K., Dernick, G., Valero, V., Yong, M.G. et al. 2005. Electrochemical imaging of fusion pore openings by electrochemical detector arrays. Proc Natl Acad Sci USA, 102, 13879 13884.
64. Hallermann, S., Pawlu, C., Jonas, P. Heckmann, M. 2003. A large pool of releasable vesicles in a cortical glutamatergic synapse. Proc Natl Acad Sci USA, 100, 8975 8980.
65. Harkins, A.B. Fox, A.P. 2000. Activation of purinergic receptors by ATP inhibits secretion in bovine adrenal chromaffin cells. Brain Res 885, 231 239.
66. 2+. Biophys J, 67, 2546 2557.
67. 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.
68. Henkel, A.W., Horstmann, H. Henkel, M.K. 2001a. Direct observation of membrane retrieval in chromaffin cells by capacitance measurements. FEBS Lett, 505, 414 418.
69. Henkel, A.W., Kang, G. Kornhuber, J. 2001b. A common molecular machinery for exocytosis and the 'kiss-and-run' mechanism in chromaffin cells is controlled by phosphorylation. J Cell Sci, 114, 4613 4620.
70. Henkel, A.W., Vogt, T.K. Henkel, M.K. 2004. Staurosporine restores GTPgammaS induced block of rapid endocytosis in chromaffin cells. FEBS Lett 571, 103 106.
71. Horrigan, F. Bookman, R. 1994. Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron, 13, 1119 1129.
72. Jankowski, J.A., Finnegan, J.M. Wightman, R.M. 1994. Extracellular ionic composition alters kinetics of vesicular release of catecholamines and quantal size during exocytosis at adrenal-medullary cells. J Neurochem, 63, 1739 1747.
73. Johannes, L., Lledo, P.M., Roa, M., Vincent, J.D., Henry, J.P. Darchen, F. 1994. The GTPase Rab3a negatively controls calcium-dependent exocytosis in neuroendocrine cells. EMBO J 13, 2029 2037.
74. Johannes, L., Lledo, P.M., Chameau, P., Vincent, J.D., Henry, J.P. Darchen, F. 1998. Regulation of the Ca2+ sensitivity of exocytosis by Rab3a. J Neurochem 71, 1127 1133.
75. Kibble, A.V., Barnard, R.J.O. Burgoyne, R.D. 1996. Patch-clamp capacitance analysis of the effects of alpha-SNAP on exocytosis in adrenal chromaffin cells. J Cell Sci 109, 2417 2422.
76. Kissinger, P.T., Felice, L.J., Riggin, R.M., Pachla, L.A. Wenke, D.C. 1974. Electrochemical detection of selected organic components in the eluate from high-performance liquid-chromatography. Clin Chem, 20, 992 997.
77. Leszczyszyn, D.J., Jankowski, J.A., Viveros, O.H., Diliberto, E.J. Jr., Near, J.A. Wightman, R.M. 1990. Nicotinic receptor-mediated catecholamine secretion from individual chromaffin cells. Chemical evidence for exocytosis. J Biol Chem, 265, 14736 14737.
78. Lim, W., Kim, S.J., Yan, H.D. Kim, J. 1997. Ca2+-channel-dependent and -independent inhibition of exocytosis by extracellular ATP in voltage-clamped rat adrenal chromaffin cells. Pflugers Arch 435, 34 42.
79. Lindau, M. Neher, E. 1988. Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflugers Arch, 411, 137 146.
80. Liu, J. Misler, S. 1998. alpha-Latrotoxin alters spontaneous and depolarization-evoked quantal release from rat adrenal chromaffin cells: evidence for multiple modes of action. J Neurosci 18, 6113 6125.
81. Lukyanetz, E.A. Neher, E. 1999. Different types of calcium channels and secretion from bovine chromaffin cells. Eur J Neurosci 11, 2865 2873.
82. Machado, J.D., Segura, F., Brioso, M.A. Borges, R. 2000. Nitric oxide modulates a late step of exocytosis. J Biol Chem, 275, 20274 20279.
83. Machado, J.D., Alonso, C., Morales, A., Gomez, J.F. Borges, R. 2002a. Nongenomic regulation of the kinetics of exocytosis by estrogens. J Pharmacol Exp Ther, 301, 631 637.
84. Machado, J.D., Gomez, J.F., Betancor, G., Camacho, M., Brioso, M.A. Borges, R. 2002b. Hydralazine reduces the quantal size of secretory events by displacement of catecholamines from adrenomedullary chromaffin secretory vesicles. Cir Res, 91, 830 836.
85. Machado, J.D., Montesinos, M.S. Borges, R. 2008. Good practices in single cell amperometry. In : A. Ivanov (ed Exocytosis and Endocytosis Methods and Protocols. Humana Press, New York (in press).
86. Moser, T. Neher, E. 1997. Estimation of mean exocytic vesicle capacitance in mouse adrenal chromaffin cells. Proc Natl Acad Sci USA, 94, 6735 6740.
87. Mosharov, E.V. Sulzer, D. 2005. Analysis of exocytotic events recorded by amperometry. Nat Methods, 2, 651 658.
88. Mosharov, E.V., Gong, L.W., Khanna, B., Sulzer, D. Lindau, M. 2003. Intracellular patch electrochemistry: regulation of cytosolic catecholamines in chromaffin cells. J Neurosci, 23, 5835 5845.
89. Mundorf, M.L., Hochstetler, S.E. Wightman, R.M. 1999. Amine weak bases disrupt vesicular storage and promote exocytosis in chromaffin cells. J Neurochem, 73, 2397 2405.
90. 2+ participates in the catalysis of exocytosis. J Biol Chem, 275, 9136 9142.
91. Nagy, G., Matti, U., Nehring, R.B., Binz, T., Rettig, J., Neher, E. et al. 2002. Protein kinase C-dependent phosphorylation of synaptosome-associated protein of 25 kDa at Ser187 potentiates vesicle recruitment. J Neurosci 22, 9278 9286.
92. Nagy, G., Kim, J.H., Pang, Z.P., Matti, U., Rettig, J., Sudhof, T.C. et al. 2006. Different effects on fast exocytosis induced by synaptotagmin 1 and 2 isoforms and abundance but not by phosphorylation. J Neurosci 26, 632 643.
93. Neco, P., Giner, D., Viniegra, S., Borges, R., Villarroel, A. Gutierrez, L.M. 2004. New roles of myosin II during vesicle transport and fusion in chromaffin cells. J Biol Chem, 279, 27450 27457.
94. Neef, A., Heinemann, C. Moser, T. 2007. Measurements of membrane patch capacitance using a software-based lock-in system. Pflugers Arch, 454, 335 344.
95. 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.
96. Neher, E. Zucker, R.S. 1993. Multiple calcium-dependent processes related to secretion in bovine chromaffin cells. Neuron, 10, 21 30.
97. Oberhauser, A.F., Robinson, I.M. Fernandez, J.M. 1996. Simultaneous capacitance and amperometric measurements of exocytosis: a comparison. Biophys J, 71, 1131 1139.
98. Okada, Y., Hazama, A., Hashimoto, A., Maruyama, Y. Kubo, M. 1992. Exocytosis upon osmotic swelling in human epithelial cells. Biochim Biophys Acta, 1107, 201 205.
99. Pan, C.Y., Jeromin, A., Lundstrom, K., Yoo, S.H., Roder, J. Fox, A.P. 2002. Alterations in exocytosis induced by neuronal Ca2+ sensor-1 in bovine chromaffin cells. J Neurosci 22, 2427 2433.
100. Penner, R., Neher, E. Dreyer, F. 1986. Intracellularly injected tetanus toxin inhibits exocytosis in bovine adrenal chromaffin cells. Nature 324, 76 78.
101. Pihel, K., Schroeder, T.J. Wightman, R.M. 1994. Rapid and selective cyclic voltammetric measurements of epinephrine and norepinephrine as a method to measure secretion from single bovine adrenal-medullary cells. Anal Chem, 66, 4532 4537.
102. Polo-Parada, L., Chan, S.A. Smith, C. 2006. An activity-dependent increased role for L-type calcium channels in exocytosis is regulated by adrenergic signaling in chromaffin cells. Neuroscience 143, 445 459.
103. Ponchon, J.L., Cespuglio, R., Gonon, F., Jouvet, M. Pujol, J.F. 1979. Normal pulse polarography with carbon fiber electrodes for in vitro and in vivo determination of catecholamines. Anal Chem, 51, 1483 1486.
104. Pothos, E.N., Przedborski, S., Davila, V., Schmitz, Y. Sulzer, D. 1998. D2-like dopamine autoreceptor activation reduces quantal size in PC12 cells. J Neurosci, 18, 5575 5585.
105. Pothos, E.N., Larsen, K.E., Krantz, D.E., Liu, Y., Haycock, J.W., Setlik, W. et al. 2000. Synaptic vesicle transporter expression regulates vesicle phenotype and quantal size. J Neurosci, 20, 7297 7306.
106. Powell, A.D., Teschemacher, A.G. Seward, E.P. 2000. P2Y purinoceptors inhibit exocytosis in adrenal chromaffin cells via modulation of voltage-operated calcium channels. J Neurosci 20, 606 616.
107. Pusch, M. Neher, E. 1988. Rates of diffusional exchange between small cells and a measuring patch pipette. Pflugers Arch, 411, 204 211.
108. Robinson, I.M., Finnegan, J.M., Monck, J.R., Wightman, R.M. Fernandez, J.M. 1995. Colocalization of calcium entry and exocytotic release sites in adrenal chromaffin cells. Proc Natl Acad Sci USA, 92, 2474 2478.
109. Rohlicek, V. Schmid, A. 1994. Dual-frequency method for synchronous measurement of cell capacitance, membrane conductance and access resistance on single cells. Pflugers Arch, 428, 30 38.
110. 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.
111. von Ruden, L. Neher, E. 1993. A Ca-dependent early step in the release of catecholamines from adrenal chromaffin cells. Science, 262, 1061 1065.
112. m and its phase angle. Biophys J, 87, 714 727.
113. Schroeder, T.J., Jankowski, J.A., Kawagoe, K.T., Wightman, R.M., Lefrou, C. Amatore, C. 1992. Analysis of diffusional broadening of vesicular packets of catecholamines released from biological cells during exocytosis. Anal Chem, 64, 3077 3083.
114. Schroeder, T.J., Jankowski, J.A., Senyshyn, J., Holz, R.W. Wightman, R.M. 1994. Zones of exocytotic release on bovine adrenal medullary cells in culture. J Biol Chem, 269, 17215 17220.
115. Schweizer, F.E., Schafer, T., Tapparelli, C., Grob, M., Karli, U.O., Heumann, R. et al. 1989. Inhibition of exocytosis by intracellularly applied antibodies against a chromaffin granule-binding protein. Nature 339, 709 712.
116. Segura, F., Brioso, M.A., Gomez, J.F., Machado, J.D. Borges, R. 2000. Automatic analysis for amperometrical recordings of exocytosis. J Neurosci Methods, 103, 151 156.
117. Smith, C. 1999. A persistent activity-dependent facilitation in chromaffin cells is caused by Ca2+ activation of protein kinase C. J Neurosci 19, 589 598.
118. Smith, C. Neher, E. 1997. Multiple forms of endocytosis in bovine adrenal chromaffin cells. J Cell Biol, 139, 885 894.
119. 2+ acts by two separate pathways to modulate the supply of release-competent vesicles in chromaffin cells. Neuron, 20, 1243 1253.
120. Sorensen, J.B. 2004. Formation, stabilisation and fusion of the readily releasable pool of secretory vesicles. Pflugers Arch, 448, 347 362.
121. Sorensen, J.B., Matti, U., Wei, S.H., Nehring, R.B., Voets, T., Ashery, U. et al. 2002. The SNARE protein SNAP-25 is linked to fast calcium triggering of exocytosis. Proc Natl Acad Sci USA 99, 1627 1632.
122. Sorensen, J.B., Fernandez-Chacon, R., Sudhof, T.C. Neher, E. 2003. Examining synaptotagmin 1 function in dense core vesicle exocytosis under direct control of Ca2+. J Gen Physiol 122, 265 276.
123. Spegel, C., Heiskanen, A., Acklid, J., Wolff, A., Taboryski, R., Emneus, J. et al. 2007. On-chip determination of dopamine exocytosis using mercaptopropionic acid modified microelectrodes. Electroanalysis, 19, 263 271.
124. Speidel, D., Bruederle, C.E., Enk, C., Voets, T., Varoqueaux, F., Reim, K. et al. 2005. CAPS1 regulates catecholamine loading of large dense-core vesicles. Neuron 46, 75 88.
125. Sun, X. Gillis, K.D. 2006. On-chip amperometric measurement of quantal catecholamine release using transparent indium tin oxide electrodes. Anal Chem, 78, 2521 2525.
126. Sun, J.Y., Wu, X.S., Wu, W., Jin, S.X., Dondzillo, A. Wu, L.G. 2004. Capacitance measurements at the calyx of Held in the medial nucleus of the trapezoid body. J Neurosci Methods, 134, 121 131.
127. 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.
128. Teschemacher, A.G. Seward, E.P. 2000. Bidirectional modulation of exocytosis by angiotensin II involves multiple G-protein-regulated transduction pathways in chromaffin cells. J Neurosci 20, 4776 4785.
129. Thompson, R.E., Lindau, M. Webb, W.W. 2001. Robust, high-resolution, whole cell patch-clamp capacitance measurements using square wave stimulation. Biophys J, 81, 937 948.
130. Ulate, G., Scott, S.R., Gonzalez, J., Gilabert, J.A. Artalejo, A.R. 2000. Extracellular ATP regulates exocytosis in inhibiting multiple Ca(2+) channel types in bovine chromaffin cells. Pflugers Arch 439, 304 314.
131. 2+-dependent steps leading to secretion in chromaffin cells from mouse adrenal slices. Neuron, 28, 537 545.
132. Voets, T., Moser, T., Lund, P.E., Chow, R.H., Geppert, M., Sudhof, T.C. et al. 2001a. Intracellular calcium dependence of large dense-core vesicle exocytosis in the absence of synaptotagmin I. Proc Natl Acad Sci USA, 98, 11680 11685.
133. Voets, T., Toonen, R.F., Brian, E.C., de Wit, H., Moser, T., Rettig, J. et al. 2001b. Munc18-1 promotes large dense-core vesicle docking. Neuron, 31, 581 591.
134. Wei, S., Xu, T., Ashery, U., Kollewe, A., Matti, U., Antonin, W. et al. 2000. Exocytotic mechanism studied by truncated and zero layer mutants of the C-terminus of SNAP-25. EMBO J 19, 1279 1289.
135. Wykes, R.C., Bauer, C.S., Khan, S.U., Weiss, J.L. Seward, E.P. 2007. Differential regulation of endogenous N- and P/Q-type Ca2+ channel inactivation by Ca2+/calmodulin impacts on their ability to support exocytosis in chromaffin cells. J Neurosci 27, 5236 5248.
136. Xu, T., Binz, T., Niemann, H. Neher, E. 1998. Multiple kinetic components of exocytosis distinguished by neurotoxin sensitivity. Nat Neurosci, 1, 192 200.
137. Xu, T., Ashery, U., Burgoyne, R.D. Neher, E. 1999. Early requirement for alpha-SNAP and NSF in the secretory cascade in chromaffin cells. EMBO J 18, 3293 3304.
138. Xu, J., Xu, Y., Ellis-Davies, G.C., Augustine, G.J. Tse, F.W. 2002. Differential regulation of exocytosis by alpha- and beta-SNAPs. J Neurosci 22, 53 61.
139. Xu, J., Tang, K.S., Lu, V.B., Weerasinghe, C.P., Tse, A. Tse, F.W. 2005. Maintenance of quantal size and immediately releasable granules in rat chromaffin cells by glucocorticoid. Am J Physiol Cell Physiol 289, C1122 C1133.
140. 2+-sensitive pool of vesicles is regulated by protein kinase C in adrenal chromaffin cells. Proc Natl Acad Sci USA, 99, 17060 17065.
141. Yang, Y., Craig, T.J., Chen, X., Ciufo, L.F., Takahashi, M., Morgan, A. et al. 2007. Phosphomimetic mutation of Ser-187 of SNAP-25 increases both syntaxin binding and highly Ca2+-sensitive exocytosis. J Gen Physiol 129, 233 244.
142. Yizhar, O., Matti, U., Melamed, R., Hagalili, Y., Bruns, D., Rettig, J. et al. 2004. Tomosyn inhibits priming of large dense-core vesicles in a calcium-dependent manner. Proc Natl Acad Sci USA 101, 2578 2583.
143. Zeniou-Meyer, M., Zabari, N., Ashery, U., Chasserot-Golaz, S., Haeberle, A.M., Demais, V. et al. 2007. Phospholipase D1 production of phosphatidic acid at the plasma membrane promotes exocytosis of large dense-core granules at a late stage. J Biol Chem 282, 21746 21757.
144. 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.
145. Zimmerberg, J., Curran, M., Cohen, F.S. Brodwick, M. 1987. Simultaneous electrical and optical measurements show that membrane fusion precedes secretory granule swelling during exocytosis of beige mouse mast cells. Proc Natl Acad Sci USA, 84, 1585 1589.