Calcium dependence of action potential-induced endocytosis in chromaffin cells

Pflugers Archiv European Journal of Physiology

Volumn 445, Issue 5, 2003, Pages 540-546

  Chan, Shyue An ^a   Chow, Robert ^b   Smith, Corey ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Action potential; Amperometry; Calcium; Capacitance; Chromaffin; Endocytosis

Indexed keywords

CALCINEURIN; CALCIUM; PHOSPHOPROTEIN PHOSPHATASE;

ACTION POTENTIAL; ADOLESCENT; ANIMAL CELL; ARTICLE; BINDING SITE; CALCIUM CELL LEVEL; CALCULATION; CELL ACTIVITY; CELL MEMBRANE; CHEMICAL REACTION KINETICS; CHROMAFFIN CELL; CONTROLLED STUDY; ELECTROCHEMISTRY; ELECTROPHYSIOLOGY; ENDOCYTOSIS; EXOCYTOSIS; NONHUMAN; PRIORITY JOURNAL; SECRETION; STIMULATION;

EID: 0037291198     PISSN: 00316768     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00424-002-0966-y     Document Type: Article

References (66)

1. Lingg G, Fischer CR, Schmidt W, Winkler H (1983) Exposure of an antigen of chromaffin granules on cell surface during exocytosis. Nature 301:610-611
2. Valtorta F, Jahn R, Fesce R, Greengard P, Ceccarelli B (1988) Synaptophysin (P38) at the frog neuromuscular junction: its incorporation into the axolemma and recycling after intense quantal secretion. J Cell Biol 107:2717-2727
3. Whalley T, Terasaki M, Cho MS, Vogel SS (1995) Direct membrane retrieval into large vesicles after exocytosis in sea urchin eggs. J Cell Biol 131:1183-1192
4. 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
5. 2+, exocytosis, and endocytosis in single melanotrophs of the rat pituitary. Neuron 5:723-733
6. 2+-stimulated exocytosis in single pituitary cells. J Cell Biol 124:667-675
7. Ramaswami M, Krishnan KS, Kelly RB (1994) Intermediates in synaptic vesicle recycling revealed by optical imaging of Drosophila neuromuscular junctions. Neuron 13:363-375
8. Koenig JH, Ikeda K (1996) Synaptic vesicles have two distinct recycling pathways. J Cell Biol 135:797-808
9. Klingauf J, Kavalali ET, Tsien RW (1998) Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature 394:581-585
10. Hsu SF, Jackson MB (1996) Rapid exocytosis and endocytosis in nerve terminals of the rat posterior pituitary. J Physiol (Lond) 494:539-553
11. Marks B, McMahon HT (1998) Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr Biol 8:740-749
12. 2+ influx inhibits dynamin and arrests synaptic vesicle endocytosis at the active zone. J Neurosci 20:949-957
13. von Gersdorff H, Matthews G (1994) Inhibition of endocytosis by elevated internal calcium in a synaptic terminal. Nature 370:652-655
14. Wu LG, Betz WJ (1996) Nerve activity but not intracellular calcium determines the time course of endocytosis at the frog neuromuscular junction. Neuron 17:769-779
15. Pamidimukkala J, Hay M (2001) Frequency dependence of endocytosis in aortic baroreceptor neurons and role of group III mGluRs. Am J Physiol 281:H387-H395
16. Sun JY, Wu XS, Wu LG (2002) Single and multiple vesicle fusion induce different rates of endocytosis at a central synapse. Nature 417:555-559
17. Marsh M, McMahon HT (1999) The structural era of endocytosis. Science 285:215-220
18. Cousin MA, Robinson PJ (2000) Two mechanisms of synaptic vesicle recycling in rat brain nerve terminals. J Neurochem 75:1645-1653
19. Sudhof TC (2000) The synaptic vesicle cycle revisited. Neuron 28:317-320
20. Valtorta F, Meldolesi J, Fesce R (2001) Synaptic vesicles: is kissing a matter of competence? Trends Cell Biol 11:324-328
21. Chan SA, Smith C (2001) Physiological stimuli evoke two forms of endocytosis in bovine chromaffin cells. J Physiol (Lond) 537:871-885
22. Artalejo CR, Elhamdani A, Palfrey HC (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
23. 2+ current run-down. Pflugers Arch 430:213-219
24. Smith C, Neher E (1997) Multiple forms of endocytosis in bovine adrenal chromaffin cells. J Cell Biol 139:885-894
25. Engisch KL, Nowycky MC (1998) Compensatory and excess retrieval: two types of endocytosis following single step depolarizations in bovine adrenal chromaffin cells. J Physiol (Lond) 506:591-608
26. 2+, GTP, and dynamin but not clathrin. Proc Natl Acad Sci USA 92:8328-8332
27. Artalejo CR, Elhamdani A, Palfrey HC (1996) Calmodulin is the divalent cation receptor for rapid endocytosis, but not exocytosis, in adrenal chromaffin cells. Neuron 16:195-205
28. Nucifora PG, Fox AP (1999) Tyrosine phosphorylation regulates rapid endocytosis in adrenal chromaffin cells. J Neurosci 19:9739-9746
29. Brandt B, Hagiwara S, Kidokoro Y, Miyazaki S (1976) Action potentials in the rat chromaffin cell and effects of acetylcholine. J Physiol (Lond) 263:417-439
30. Kidokoro Y (1980) Role of action potentials in hormone secretion. Biochem Res 1:117-123
31. Wakade AR (1981) Studies on secretion of catecholamines evoked by acetylcholine or transmural stimulation of the rat adrenal gland. J Physiol (Lond) 313:463-480
32. Holman ME, Coleman HA, Tonta MA, Parkington HC (1994) Synaptic transmission from splanchnic nerves to the adrenal medulla of guinea-pigs. J Physiol (Lond) 478:115-124
33. Wallace DJ, Chen C, Marley PD (2002) Histamine promotes excitability in bovine adrenal chromaffin cells by inhibiting an M-current. J Physiol (Lond) 540:921-939
34. 2+ concentration triggering exocytosis in neuroendocrine cells. Proc Natl Acad Sci USA 91:12765-12769
35. Horn R, Marty A (1988) Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 92:145-159
36. Gillis K, Pun R, Misler S (1991) Single cell assay of exocytosis from adrenal chromaffin cells using "perforated patch recording". Pflugers Arch 418:611-613
37. 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
38. Wightmann RM, Jankowski JA, Kennedy RT, Kawagoe KT, Schroeder TJ, Leszczyszyn DJ, Near JA, Dilberto EJJ, Viveros OH (1991) Temporally resolved catecholamine spikes correspond to single vesicle release from individual chromaffin cells. Proc Natl Acad Sci USA 88:10754-10758
39. Chow RH, von Rüden L, Neher E (1992) Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature 356:60-63
40. 2+ activation of protein kinase C. J Neurosci 19:589-598
41. Gillis KD (1995) Techniques for membrane capacitance measurements. In: Sakmann B, Neher E (eds) Single-channel recording, 2nd edn. Plenum, New York, Chapter 7, pp 155-198
42. Lee AK, Tse A (2001) Endocytosis in identified rat corticotrophs. J Physiol (Lond) 533:389-405
43. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450
44. Zhou Z, Neher E (1993) Mobile and immobile calcium buffers in bovine adrenal chromaffin cells. J Physiol (Lond) 469:245-273
45. Roberts WM (1993) Spatial calcium buffering in saccular hair cells. Nature 363:74-76
46. + channels. Nature Neurosci 3:566-571
47. + current at presynaptic terminals of goldfish retinal bipolar cells. Neurosci Res 27:219-228
48. Prakriya M, Lingle CJ (2000) Activation of BK channels in rat chromaffin cells requires summation of Ca(2+) influx from multiple Ca(2+) channels. J Neurophysiol 84:1123-1135
49. Gillis KD (2000) Admittance-based measurement of membrane capacitance using the EPC-9 patch-clamp amplifier. Pflugers Arch 439:655-664
50. Chen P, Hwang TC, Gillis KD (2001) The relationship between cAMP, Ca(2)+, and transport of CFTR to the plasma membrane. J Gen Physiol 118:135-144
51. Voets T, Neher E, Moser T (1999) Mechanisms underlying phasic and sustained secretion in chromaffin cells from mouse adrenal slices. Neuron 23:607-615
52. Robinson PJ, Sontag JM, Liu JP, Fykse EM, Slaughter C, McMahon H, Sudhof TC (1993) Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals. Nature 365:163-166
53. 2+ acts by two separate pathways to modulate the supply of release-competent vesicles in chromaffin cells. Neuron 20:1243-1253
54. Cousin MA, Robinson PJ (2001) The dephosphins: dephosphorylation by calcineurin triggers synaptic vesicle endocytosis. Trends Neurosci 24:659-665
55. Cousin MA, Tan TC, Robinson PJ (2001) Protein phosphorylation is required for endocytosis in nerve terminals: potential role for the dephosphins dynamin I and synaptojanin, but not AP180 or amphiphysin. J Neurochem 76:105-116
56. Galli T, Haucke V (2001) Cycling of synaptic vesicles: how far? How fast! Sci STKE 2001:RE1 PMID: 11752659
57. Graham ME, O'Callaghan DW, McMahon HT, Burgoyne RD (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
58. Mochly-Rosen D, Gordon AS (1998) Anchoring proteins for protein kinase C: a means for isozyme selectivity. FASEB J 12:35-42
59. Sena CM, Santos RM, Standen NB, Boarder MR, Rosario LM (2001) Isoform-specific inhibition of voltage-sensitive Ca(2+) channels by protein kinase C in adrenal chromaffin cells. FEBS Lett 492:146-150
60. Takekoshi K, Ishii K, Nanmoku T, Shibuya S, Kawakami Y, Isobe K, Nakai T (2001) Leptin stimulates catecholamine synthesis in a PKC-dependent manner in cultured porcine adrenal medullary chromaffin cells. Endocrinology 142:4861-4871
61. Almholt K, Arkhammar PO, Thastrup O, Tullin S (1999) Simultaneous visualization of the translocation of protein kinase Calpha-green fluorescent protein hybrids and intracellular calcium concentrations. Biochem J 337:211-218
62. Oancea E, Meyer T (1998) Protein kinase C as a molecular machine for decoding calcium and diacylglycerol signals. Cell 95:307-318
63. Lin X, Gelman IH (2002) Calmodulin and cyclin D anchoring sites on the src-suppressed C kinase substrate, Ssecks. Biochem Biophys Res Commun 290:1368-1375
64. Nauert JB, Klauck TM, Langeberg LK, Scott JD (1997) Gravin, an autoantigen recognized by serum from myasthenia gravis patients, is a kinase scaffold protein. Curr Biol 7:52-62
65. Marks B, McMahon HT (1998) Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr Biol 8:740-749
66. Takei K, Haucke V (2001) Clathrin-mediated endocytosis: membrane factors pull the trigger. Trends Cell Biol 11:385-391