The immediately releasable vesicle pool: Highly coupled secretion in chromaffin and other neuroendocrine cells

Journal of Neurochemistry

Volumn 116, Issue 2, 2011, Pages 155-163

  Álvarez, Yanina D ^a   Marengo, Fernando D ^a  

^a INSTITUTO DE FISIOLOGÍA   (Argentina)

Author keywords

chromaffin cells; exocytosis; P Q channels; voltage dependent Ca2+ channels

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; CYTOSKELETON PROTEIN;

ACTION POTENTIAL; CELL VACUOLE; CHROMAFFIN CELL; DEPOLARIZATION; EXOCYTOSIS; MOLECULAR DOCKING; MOLECULAR INTERACTION; NEUROSECRETORY CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; STIMULUS RESPONSE; SYNAPSE VESICLE;

ANIMALS; CALCIUM CHANNELS; CHROMAFFIN CELLS; EXOCYTOSIS; HUMANS; NEUROENDOCRINE CELLS; SYNAPTIC VESICLES; TIME FACTORS;

EID: 78650710916     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.07108.x     Document Type: Review

References (71)

1. Albillos A., Neher E., and, Moser T., (2000) R-Type Ca2+ channels are coupled to the rapid component of secretion in mouse adrenal slice chromaffin cells. J. Neurosci. 20, 8323-8330.
2. Aldea M., Jun K., Shin H. S., Andres-Mateos E., Solis-Garrido L. M., Montiel C., Garcia A. G., and, Albillos A., (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.
3. Alvarez Y. D., Ibanez L. I., Uchitel O. D., and, Marengo F. D., (2008) P/Q Ca2+ channels are functionally coupled to exocytosis of the immediately releasable pool in mouse chromaffin cells. Cell Calcium 43, 155-164.
4. Andres-Mateos E., Renart J., Cruces J., Solis-Garrido L. M., Serantes R., Lucas-Cerrillo A. M., Aldea M., Garcia A. G., and, Montiel C., (2005) Dynamic association of the Ca2+ channel alpha1A subunit and SNAP-25 in round or neurite-emitting chromaffin cells. Eur. J. Neurosci. 22, 2187-2198.
5. 2+ channel trigger secretion with different efficacies in chromaffin cells. Nature 367, 72-76.
6. Ashery U., Varoqueaux F., Voets T., Betz A., Thakur P., Koch H., Neher E., Brose N., and, Rettig J., (2000) Munc13-1 acts as a priming factor for large dense-core vesicles in bovine chromaffin cells. EMBO J. 19, 3586-3596.
7. Atwood H. L., and, Karunanithi S., (2002) Diversification of synaptic strength: presynaptic elements. Nat. Rev. Neurosci. 3, 497-516.
8. Augustine G. J., and, Neher E., (1992) Calcium requirements for secretion in bovine chromaffin cells. J. Physiol. 450, 247-271.
9. 2+ channels accounts for first-phase insulin secretion in mouse beta-cells. Diabetes 51, S74-S82.
10. Barg S., Ma X., Eliasson L., et al. (2001) Fast exocytosis with few Ca(2+) channels in insulin-secreting mouse pancreatic B cells. Biophys. J. 81, 3308-3323.
11. Bauer C. S., Woolley R. J., Teschemacher A. G., and, 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.
12. Becherer U., Moser T., Stuhmer W., and, Oheim M., (2003) Calcium regulates exocytosis at the level of single vesicles. Nat. Neurosci. 6, 846-853.
13. Borst J. G. G., Helmchen F., and, Sakmann B., (1995) Pre- and post synaptic whole-cell recording in the medial nucleus of the trapezoid body of the rat. J. Physiol. 489, 825-840.
14. Brandt B. L., Hagiwara S., Kidokoro Y., and, Miyazaki S., (1976) Action potentials in the rat chromaffin cell and effects of acetylcholine. J. Physiol. 263, 417-439.
15. Carabelli V., Marcantoni A., Comunanza V., and, Carbone E., (2007) Fast exocytosis mediated by T- and L-type channels in chromaffin cells: distinct voltage-dependence but similar Ca2+ -dependence. Eur. Biophys. J. 36, 753-762.
16. Chan S. A., Polo-Parada L., Landmesser L. T., and, Smith C., (2005a) Adrenal chromaffin cells exhibit impaired granule trafficking in NCAM knockout mice. J. Neurophysiol. 94, 1037-1047.
17. Chan S. A., Polo-Parada L., and, Smith C., (2005b) Action potential stimulation reveals an increased role for P/Q-calcium channel-dependent exocytosis in mouse adrenal tissue slices. Arch. Biochem. Biophys. 435, 65-73.
18. Chow R. H., Klingauf J., and, Neher E., (1994) Time course of Ca2+ concentration triggering exocytosis in neuroendocrine cells. Proc. Natl Acad. Sci. USA 91, 12765-12769.
19. Dinkelacker V., Voets T., Neher E., and, Moser T., (2000) The readily releasable pool of vesicles in chromaffin cells is replenished in a temperature-dependent manner and transiently overfills at 37 degrees C. J. Neurosci. 20, 8377-8383.
20. Elhamdani A., Zhou Z., and, 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.
21. Eliasson L., Renstrom E., Ding W. G., Proks P., and, Rorsman P., (1997) Rapid ATP-dependent priming of secretory granules precedes Ca(2+) -induced exocytosis in mouse pancreatic B-cells. J. Physiol. 503 (Pt 2), 399-412.
22. Engisch K. L., and, 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.
23. Fulop T., Radabaugh S., and, Smith C., (2005) Activity-dependent differential transmitter release in mouse adrenal chromaffin cells. J. Neurosci. 25, 7324-7332.
24. Gandia L., Borges R., Albillos A., and, Garcia A. G., (1995) Multiple calcium channel subtypes in isolated rat chromaffin cells. Pflugers Arch. 430, 55-63.
25. García A. G., García-De-Diego A. M., Gandía L., Borges R., and, García-Sancho J., (2006) Calcium signaling and exocytosis in adrenal chromaffin cells. Physiol. Rev. 86, 1093-1131.
26. Ge Q., Dong Y. M., Hu Z. T., Wu Z. X., and, Xu T., (2006) Characteristics of Ca2+-exocytosis coupling in isolated mouse pancreatic beta cells. Acta Pharmacol. Sin. 27, 933-938.
27. Giancippoli A., Novara M., de Luca A., Baldelli P., Marcantoni A., Carbone E., and, Carabelli V., (2006) Low-threshold exocytosis induced by cAMP-recruited CaV3.2 (alpha1H) channels in rat chromaffin cells. Biophys. J. 90, 1830-1841.
28. Giovannucci D. R., and, Stuenkel E. L., (1997) Regulation of secretory granule recruitment and exocytosis at rat neurohypophysial nerve endings. J. Physiol. 498 (Pt 3), 735-751.
29. Harkins A. B., Cahill A. L., Powers J. F., Tischler A. S., and, Fox A. P., (2004) Deletion of the synaptic protein interaction site of the N-type (CaV2.2) calcium channel inhibits secretion in mouse pheochromocytoma cells. Proc. Natl Acad. Sci. USA 101, 15219-15224.
30. Heinemann C., von Ruden L., Chow R. H., and, Neher E., (1993) A two-step model of secretion control in neuroendocrine cells. Pflugers Arch. 424, 105-112.
31. Heinemann C., Chow R. H., Neher E., and, Zucker R. S., (1994) Kinetics of the secretory response in bovine chromaffin cells following flash photolysis of caged Ca2+. Biophys. J. 67, 2546-2557.
32. Hernandez-Guijo J. M., de Pascual R., Garcia A. G., and, Gandia L., (1998) Separation of calcium channel current components in mouse chromaffin cells superfused with low- and high-barium solutions. Pflugers Arch. 436, 75-82.
33. Horrigan F. T., and, Bookman R. J., (1994) Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron 13, 1119-1129.
34. Inchauspe C. G., Martini F. J., Forsythe I. D., and, Uchitel O. D., (2004) Functional compensation of P/Q by N-type channels blocks short-term plasticity at the calyx of held presynaptic terminal. J. Neurosci. 24, 10379-10383.
35. Kim S. J., Lim W., and, Kim J., (1995) Contribution of L- and N-type calcium currents to exocytosis in rat adrenal medullary chromaffin cells. Brain Res. 675, 289-296.
36. Kits K. S., de Vlieger T. A., Kooi B. W., and, Mansvelder H. D., (1999) Diffusion barriers limit the effect of mobile calcium buffers on exocytosis of large dense core vesicles. Biophys. J. 76, 1693-1705.
37. Klingauf J., and, Neher E., (1997) Modeling buffered Ca2+ diffusion near the membrane: implications for secretion in neuroendocrine cells. Biophys. J. 72, 674-690.
38. Lara B., Gandia L., Martinez-Sierra R., Torres A., and, Garcia A. G., (1998) Q-type Ca2+ channels are located closer to secretory sites than L-type channels: functional evidence in chromaffin cells. Pflugers Arch. 435, 472-478.
39. Llinas R., Sugimori M., and, Silver R. B., (1992) Microdomains of high calcium concentration in a presynaptic terminal. Science 256, 677-679.
40. Lomax R. B., Michelena P., Nunez L., Garcia-Sancho J., Garcia A. G., and, Montiel C., (1997) Different contributions of L- and Q-type Ca2+ channels to Ca2+ signals and secretion in chromaffin cell subtypes. Am. J. Physiol. 272, C476-C484.
41. Lopez I., Giner D., Ruiz-Nuno A., Fuentealba J., Viniegra S., Garcia A. G., Davletov B., and, Gutierrez L. M., (2007) Tight coupling of the t-SNARE and calcium channel microdomains in adrenomedullary slices and not in cultured chromaffin cells. Cell Calcium 41, 547-558.
42. Lukyanetz E. A., and, Neher E., (1999) Different types of calcium channels and secretion from bovine chromaffin cells. Eur. J. Neurosci. 11, 2865-2873.
43. Marengo F. D., (2005) Calcium gradients and exocytosis in bovine adrenal chromaffin cells. Cell Calcium 38, 87-99.
44. Merrins M. J., and, Stuenkel E. L., (2008) Kinetics of Rab27a-dependent actions on vesicle docking and priming in pancreatic beta-cells. J. Physiol. 586, 5367-5381.
45. Mochida S., Westenbroek R. E., Yokoyama C. T., Zhong H., Myers S. J., Scheuer T., Itoh K., and, Catterall W. A., (2003) Requirement for the synaptic protein interaction site for reconstitution of synaptic transmission by P/Q-type calcium channels. Proc. Natl Acad. Sci. USA 100, 2819-2824.
46. Moser T., and, Neher E., (1997) Rapid exocytosis in single chromaffin cells recorded from mouse adrenal slices. J. Neurosci. 17, 2314-2323.
47. Neher E., (1998) Vesicle pools and Ca2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20, 389-399.
48. Neher E., and, Zucker R. S., (1993) Multiple calcium-dependent processes related to secretion in bovine chromaffin cells. Neuron 10, 21-30.
49. Novara M., Baldelli P., Cavallari D., Carabelli V., Giancippoli A., and, Carbone E., (2004) Exposure to cAMP and beta-adrenergic stimulation recruits Ca(V)3 T-type channels in rat chromaffin cells through Epac cAMP-receptor proteins. J. Physiol. 558, 433-449.
50. Oré L. O., and, Artalejo A. R., (2005) Intracellular Ca2+ microdomain-triggered exocytosis in neuroendocrine cells. Trends Neurosci. 27, 113-115.
51. Polo-Parada L., Chan S. A., and, 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.
52. 2+ channels in rat chromaffin cells. J. Neurophysiol. 81, 2267-2278.
53. Rettig J., Sheng Z. H., Kim D. K., Hodson C. D., Snutch T. P., and, Catterall W. A., (1996) Isoform-specific interaction of the alpha1A subunits of brain Ca2+ channels with the presynaptic proteins syntaxin and SNAP-25. Proc. Natl Acad. Sci. USA 93, 7363-7368.
54. Rettig J., Heinemann C., Ashery U., Sheng Z. H., Yokoyama C. T., Catterall W. A., and, Neher E., (1997) Alteration of Ca2+ dependence of neurotransmitter release by disruption of Ca2+ channel/syntaxin interaction. J. Neurosci. 17, 6647-6656.
55. Robinson I. M., Finnegan J. M., Monck J. R., Wightman R. M., and, Fernandez J. M., (1995) Colocalization of calcium entry and exocytotic release sites in adrenal chromaffin cells. Proc. Natl Acad. Sci. USA 92, 2474-2478.
56. Rosato S., and, Uchitel O. D., (1999) Calcium channels coupled to neurotransmitter release at neonatal rat neuromuscular junctions. J. Physiol. 514 (Pt 2), 533-540.
57. Santana F., Michelena P., Jaen R., Garcia A. G., and, Borges R., (1999) Calcium channel subtypes and exocytosis in chromaffin cells: a different view from the intact rat adrenal. Naunyn Schmiedebergs Arch. Pharmacol. 360, 33-37.
58. Segura J., Gil A., and, Soria B., (2000) Modeling study of exocytosis in neuroendocrine cells: influence of the geometrical parameters. Biophys. J. 79, 1771-1786.
59. Seward E. P., and, Nowycky M. C., (1996) Kinetics of stimulus-coupled secretion in dialyzed bovine chromaffin cells in response to trains of depolarizing pulses. J. Neurosci. 16, 553-562.
60. Sorensen J. B., (2004) Formation, stabilisation and fusion of the readily releasable pool of secretory vesicles. Pflugers Arch. 448, 347-362.
61. Trifarõ J. M., Gasman S., and, Gutiérrez L. M., (2008) Cytoskeletal control of vesicle transport and exocytosis in chromaffin cells. Acta Physiol. (Oxf) 192, 165-172.
62. Voets T., (2000) Dissection of three Ca2+-dependent steps leading to secretion in chromaffin cells from mouse adrenal slices. Neuron 28, 537-545.
63. Voets T., Neher E., and, Moser T., (1999) Mechanisms underlying phasic and sustained secretion in chromaffin cells from mouse adrenal slices. Neuron 23, 607-615.
64. Wan Q. F., Dong Y., Yang H., Lou X., Ding J., and, Xu T., (2004) Protein kinase activation increases insulin secretion by sensitizing the secretory machinery to Ca2+. J. Gen. Physiol. 124, 653-662.
65. 2+/calmodulin impacts on their ability to support exocytosis in chromaffin cells. J. Neurosci. 27, 5236-5248.
66. Xu T., Binz T., Niemann H., and, Neher E., (1998) Multiple kinetic components of exocytosis distinguished by neurotoxin sensitivity. Nat. Neurosci. 1, 192-200.
67. Xu J., Tang K. S., Lu V. B., Weerasinghe C. P., Tse A., and, 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.
68. Yang Y., and, Gillis K. D., (2004) A highly Ca2+ -sensitive pool of granules is regulated by glucose and protein kinases in insulin-secreting INS-1 cells. J. Gen. Physiol. 124, 641-651.
69. Yang Y., Udayasankar S., Dunning J., Chen P., and, Gillis K. D., (2002) A highly Ca2+ -sensitive pool of vesicles is regulated by protein kinase C in adrenal chromaffin cells. Proc. Natl Acad. Sci. USA 99, 17060-17065.
70. Yokoyama C. T., Myers S. J., Fu J., Mockus S. M., Scheuer T., and, Catterall W. A., (2005) Mechanism of SNARE protein binding and regulation of Cav2 channels by phosphorylation of the synaptic protein interaction site. Mol. Cell. Neurosci. 28, 1-17.
71. Zamponi G. W., (2003) Regulation of presynaptic calcium channels by synaptic proteins. J. Pharmacol. Sci. 92, 79-83.