A persistent activity-dependent facilitation in chromaffin cells is caused by Ca2+ activation of protein kinase C

Journal of Neuroscience

Volumn 19, Issue 2, 1999, Pages 589-598

  Smith, Corey ^a,b  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Chromaffin; Exocytosis; Facilitation; Membrane capacitance; Plasticity; Vesicle pools

Indexed keywords

CALCIUM ION; PROTEIN KINASE C;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CATTLE; CELL ACTIVITY; CHROMAFFIN CELL; CONTROLLED STUDY; ENZYME ACTIVATION; EXOCYTOSIS; FACILITATION; MEMBRANE VESICLE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL;

EID: 0033556325     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-02-00589.1999     Document Type: Article

References (58)

1. Ämmälä C, Ashcroft FM, Rorsman P (1993) Calcium-independent potentiation of insulin release by cyclic AMP in single h cells. Nature 363:356-358.
2. Ämmälä C, Eliasson L, Bokvist K, Berggrcn P-O, Honkanen RE, Sjöholm Å, Rorsman P (1994) Activation of protein kinases and inhibition of protein phosphatases play a central role in the regulation of exocytosis in mouse pancreatic b-cells. Proc Natl Acad Sci USA 91:4343-4347.
3. Betz WJ (1970) Depression of transmitter release at the neuromuscular junction of the frog. J Phvsiol (Lond) 206:629-644.
4. Bittner MA, Holz RW (1992) Kinetic analysis of secretion from permeabilized adrenal chromaffin cells reveals distinct components. J Biol Chem 267:16219-16225.
5. Burgoyne RD (1995) Fast exocytosis and endocytosis triggered by depolarization in single adrenal chromaffin cells before rapid Ca2+ current run-down. Pflügers Arch 430:213-219.
6. Byrne JH, Kandel ER (1996) Presynaptic facilitation revisited: state and time dependence. J Neurosci 16:425-435.
7. Chow RH, Klingauf J, Neher E (1994) Time course of Ca2+ concentration triggering exocytosis in neuroendocrinc cells. Proc Natl Acad Sci USA 91:12765-12769.
8. Chow RH, Klingauf J, Heinemann C, Zucker RS, Neher E (1996) Mechanisms determining the time course of secretion in neuroendocrine cells. Neuron 16:369-76.
9. Currie KPM, Fox AP (1996) ATP serves as a negative feedback inhibitor of voltage-gated Ca2+ channel currents in cultured bovine adrenal chromaffin cells. Neuron 16:1027-1036.
10. Elmqvist D, Quastel DMJ (1965) A quantitative study of end-plate potentials in isolated human muscle. J Physiol (Lond) 178:505-529.
11. Engisch KL, Nowycky MC (1996) Calcium dependence of large densecored vesicle exocytosis evoked by calcium influx in bovine adrenal chromaffin cells. J Neurosci 16:1359-1369.
12. 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.
13. Engisch KL, Chernevskaya NI, Nowycky MC (1997) Short-term changes in the Ca2+-exocytosis relationship during repetitive pulse protocols in bovine adrenal chromaffin cells. J Neurosci 17:9010-9025.
14. Fisher SA, Fischer TM, Carew TJ (1997) Multiple overlapping processes underlying short-term synaptic enhancement. Trends Neurosci 20:170-177.
15. Forsythe ID, Tsujimoto T, Barnes-Davies M, Cuttle MF, Takahashi T (1998) Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse. Neuron 20:797-807.
16. Gillis KD (1995) Chapter 7. Techniques for membrane capacitance measurements. In: Single-channel recording, Ed 2, (Sakmann B, Neher E, eds), pp 155-198. New York: Plenum.
17. Gillis KD, Mößner R, Neher E (1996) Protein kinasc C enhances exocytosis from chromaffin cells by increasing the size of the readily releasable pool of secretory granules. Neuron 16:1209-1220.
18. Greengard P, Valtorta F, Czernik AJ, Benfenati F (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259:780-785.
19. Grynkiewicz G, Poenie M, Tsien R (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450.
20. Heinemann C, von Rüden L, Chow RH, Neher E (1993) A two-step model of secretion control in neuroendocrine cells. Pflügers Arch 424:105-122.
21. Heinemann C, Chow R, Neher E, Zucker R (1994) Kinetics of the secretory response in bovine chromaffin cells following flash photolysis of caged Ca++. Biophys J 67:2546-2557.
22. Horrigan FT, Bookman RJ (1994) Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron 13:1119-1129.
23. Hsu S-F, Augustine GJ, Jackson MB (1996) Adaptation of Ca2+-triggered exocytosis in presynaptic terminals. Neuron 17:501-512.
24. Klingauf J, Neher E (1997) Modeling buffered Ca2+ diffusion near the membrane: implications for secretion in neuroendocrine cells. Biophys J 72:674-690.
25. Knight D, Baker P (1983) Stimulus-secretion coupling in isolated bovine adrenal medullary cells. Q J Exp Physiol 68:123-143.
26. Kumar GK, Overholt JL, Bright GR, Kwong YH, Hongwen L, Gratzl M, Prabhakar NR (1998) Release of dopamine and norepinephrine by hypoxia from PC-12 cells. Am J Physiol 274: C1592-C1600.
27. Li L, Chin LS, Shupliakov O, Brodin L, Sihra TS, Hvalby O, Jensen V, Zheng D, McNamara JO, Greengard P (1995) Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice. Proc Natl Acad Sci USA 92:9235-9239.
28. Lindau M, Neher E (1988) Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflügers Arch 411:137-146.
29. Lindgren CA, Smith DO (1987) Extracellular ATP modulates calcium uptake and transmitter release at the neuromuscular junction. J Neurosci 7:1567-1573.
30. Ma XM, Lightman SL (1998) The arginine vasopressin and corticotropin-releasing hormone gene transcription responses to varied frequencies of repeated stress in rats. J Physiol (Lond) 510:605-614.
31. Malenka RC (1994) Synaptic plasticity in the hippocampus: LTP and LTD. Cell 78:535-8.
32. Moser T, Neher E (1997) Rapid exocytosis in single chromaffin cells recorded from mouse adrenal slices. J Neurosci 17:2314-2323.
33. Neher E (1998) Vesicle pools and Ca2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20:389-399.
34. Neher E, Augustine GJ (1992) Calcium gradients and buffers in bovine chromaffin cells. J Physiol (Lond) 450:273-301.
35. Neher E, Marty A (1982) Discrete changes in cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc Natl Acad Sci USA 79:6712-6716.
36. Neher E, Zucker RS (1993) Multiple calcium-dependent processes related to secretion in bovine chromaffin cells. Neuron 10:21-30.
37. Renström E, Eliasson L, Rorsman P (1997) Protein kinase A-dependent and -independent stimulation of exocytosis by cAMP in mouse pancreatic B-cells. J Physiol (Lond) 502:105-118.
38. Richter DW, Lalley PM, Pierretichte O, Haji A, Bischoff AM, Wilken B, Hanefeld F (1997) Intracellular signal pathways controlling respiratory neurons. Respir Physiol 110:113-123.
39. Seward EP, Nowycky MC (1996) Kinetics of stimulus-coupled secretion in dialyzed bovine chromaffin cells in response to trains of depolarizing pulses. J Neurosci 16:553-562.
40. Smith C, Neher E (1997) Multiple forms of endocytosis in bovine adrenal chromaffin cells. J Cell Biol 139:885-894.
41. Smith C, Moser T, Xu T, Neher E (1998) Cytosolic Ca2+ acts by two separate pathways to modulate the supply of release-competent vesicles in chromaffin cells. Neuron 20:1243-1253.
42. Stevens CF, Tsujimoto T (1995) Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. Proc Natl Acad Sci USA 92:846-849.
43. Takahashi N, Kadowaki T, Yazaki Y, Miyashita Y, Kasai H (1997) Multiple exocytotic pathways in pancreatic beta cells. J Cell Biol 138:55-64.
44. Tang Y, Zucker RS (1997) Mitochondrial involvement in post-tetanic potentiation of synaptic transmission. Neuron 18:483-491.
45. TerBush DR, Bittner MA, Holz RW (1988) Ca2+ influx causes rapid translocation of protein kinase C to membranes. Studies of the effects of secretagogues in adrenal chromaffin cells. J Biol Chem 263:18873-18879.
46. Thomas P, Waring DW (1997) Modulation of stimulus-secretion coupling in single rat gonadotrophs. J Physiol (Lond) 504:705-719.
47. Thomas P, Wong JG, Lee AK, Almers W (1993) A low affinity Ca2+ receptor controls the final steps in peptide secretion from pituitary melanotrophs. Neuron 11:93-104.
48. Vitale ML, Seward EP, Trifaró J-M (1995) Chromaffin cell cortical actin network dynamics control the size of the release-ready vesicle pool and the initial rate of exocytosis. Neuron 14:353-363.
49. Vogel SS, Blank PS, Zimmerberg J (1996) Poisson-distributed active fusion complexes underlie the control of the rate and extent of exocytosis by calcium. J Cell Biol 134:329-338.
50. von Rüden L, Neher E (1993) A Ca-dependent early step in the release of catecholamines from adrenal chromaffin cells. Science 262:1061-1065.
51. Wang C, Zucker RS (1998) Regulation of synaptic vesicle recycling by calcium and serotonin. Neuron 21:155-167.
52. Xu T, Binz T, Niemann H, Neher E (1998) Multiple kinetic components of exocytosis distinguished by neurotoxin sensitivity. Nat Neurosci 1:192-200.
53. Xu T, Naraghi M, Kang H, Neher E (1997) Kinetic studies of Ca2+ binding and Ca2+ clearance in the cytosol of adrenal chromaffin cells. Biophys J 73:532-545.
54. Zador AM, Dobrunz LE (1997) Dynamic synapses in the cortex. Neuron 19:1-4.
55. Zhou Z, Misler S (1995) Action potential-induced quantal secretion of catecholamines from rat adrenal chromaffin cells. J Biol Chem 270:3498-3505.
56. Zhou Z, Neher E (1993) Mobile and immobile calcium buffers in bovine adrenal chromaffin cells. J Physiol (Lond) 469:245-273.
57. Zucker R (1989) Short-term synaptic plasticity. Annu Rev Neurosci 12:13-31.
58. Zucker RS (1996) Exocytosis: a molecular and physiological perspective. Neuron 17:1049-1055.