How Neurosecretory Vesicles Release Their Cargo

The Neuroscientist

Volumn 12, Issue 2, 2006, Pages 164-176

  Scalettar, Bethe A ^a  

^a LEWIS AND CLARK COLLEGE   (United States)

Author keywords

Dense core granule; Fluorescence microscopy; Regulated exocytosis; Synaptic vesicle

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS;

ANIMAL; EXOCYTOSIS; FLUORESCENCE MICROSCOPY; HUMAN; INSTRUMENTATION; METABOLISM; METHODOLOGY; NERVE FIBER TRANSPORT; NEUROSECRETION; PHYSIOLOGY; REVIEW; SECRETION; SECRETORY VESICLE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; SYNAPTOSOME;

ANIMALS; AXONAL TRANSPORT; EXOCYTOSIS; HUMANS; MICROSCOPY, FLUORESCENCE; NEUROSECRETION; NEUROSECRETORY SYSTEMS; NEUROTRANSMITTER AGENTS; PRESYNAPTIC TERMINALS; SECRETORY VESICLES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 33646713911     PISSN: 10738584     EISSN: None     Source Type: Journal    
DOI: 10.1177/1073858405284258     Document Type: Review

References (73)

1. Alberts B. Johnson A. Lewis J, Raff M, Roberts K, Walter P. 2002. Molecular biology of the cell. New York: Garland Science.
2. Allersma MW, Wang L. Axelrod D. Holz RW. 2004. Visualization of regulated exocytosis with a granule-membrane probe using total internal reflection microscopy. Mol Biol Cell 15: 4658–4668.
3. 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 U S A 99: 6358–6363.
4. Arvan P. Castle D. 1998. Sorting and storage during secretory granule biogenesis: looking backward and looking forward. Biochem J 332(Pt 3):593–610.
5. Axelrod D. 2003. Total internal reflection fluorescence microscopy in cell biology. Methods Enzymol 361: 1–33.
6. Baranes D. Lederfein D, Huang YY, Chen M, Bailey CH, Kandel ER. 1998. Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron 21: 813–825.
7. Barg S, Olofsson CS, Schriever-Abeln J, Wendt A, Gebre-Medhin S, Renstrom E, and others. 2002. Delay between fusion pore opening and peptide release from large dense-core vesicles in neuroendocrine cells. Neuron 33: 287–299.
8. Becherer U. Moser T, Stuhmer W, Oheim M. 2003. Calcium regulates exocytosis at the level of single vesicles. Nat Neurosci 6: 846–853.
9. Berg H. 1983. Random walks in biology. Princeton, NJ: Princeton University Press.
10. Brigadski T. Hartmann M, Lessmann V. 2005. Differential vesicular targeting and time course of synaptic secretion of the mammalian neurotrophins. J Neurosci 25: 7601–7614.
11. Burgoyne RD, Morgan A. 2003. Secretory granule exocytosis. Physiol Rev 83: 581–632.
12. Burke NV, Han W. Li D, Takimoto K, Watkins SC, Levitan ES. 1997. Neuronal peptide release is limited by secretory granule mobility. Neuron 19: 1095–1102.
13. Ceccarelli B. Hurlbut WP, Mauro A. 1973. Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol 57: 499–524.
14. Chen ZL, Strickland S. 1997. Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 91: 917–925.
15. Chuang JZ, Milner TA, Zhu M. Sung CH. 1999. A 29 kDa intracellular chloride channel p64H1 is associated with large dense-core vesicles in rat hippocampal neurons. J Neurosci 19: 2919–2928.
16. Desnos C. Schonn JS, Huet S, Tran VS, El-Amraoui A, Raposo G, and others. 2003. Rab27A and its effector MyRIP link secretory granules to F-actin and control their motion towards release sites. J Cell Biol 163: 559–570.
17. Duncan RR, Greaves J, Wiegand UK, Matskevich I, Bodammer G, Apps DK, and others. 2003. Functional and spatial segregation of secretory vesicle pools according to vesicle age. Nature 422: 176–180.
18. Dutton A, Dyball RE. 1979. Phasic firing enhances vasopressin release from the rat neurohypophysis. J Physiol 290: 433–440.
19. Eliasson L, Renstrom E, Ding WG, Proks P, 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.
20. 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 U S A 99: 7124–7129.
21. Halban PA, Irminger JC. 1994. Sorting and processing of secretory proteins. Biochem J 299(Pt 1):1–18.
22. Hall ZW. 1992. The nerve terminal. In: Hall, ZW. An introduction to molecular neurobiology. Sunderland, MA: Sinauer Associates. 148-178.
23. Han W, Ng YK, Axelrod D, Levitan ES. 1999. Neuropeptide release by efficient recruitment of diffusing cytoplasmic secretory vesicles. Proc Natl Acad Sci U S A 96: 14577–14582.
24. Hannah MJ, Schmidt AA, Huttner WB. 1999. Synaptic vesicle biogenesis. Annu Rev Cell Dev Biol 15: 733–798.
25. Hartmann M, Heumann R, Lessmann V. 2001. Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J 20: 5887–5897.
26. Haubensak W. Narz F. Heumann R, Lessmann V. 1998. BDNF-GFP containing secretory granules are localized in the vicinity of synaptic junctions of cultured cortical neurons. J Cell Sci 111: 1483–1493.
27. Heinemann C. Chow RH, Neher E, Zucker RS. 1994. Kinetics of the secretory response in bovine chromaffin cells following flash photolysis of caged Ca2+. Biophys J 67: 2546–2557.
28. Heuser JE, Reese TS. 1973. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57: 315–344.
29. Hide I, Bennett JP, Pizzey A, Boonen G, Bar-Sagi D, Gomperts BD, and others. 1993. Degranulation of individual mast cells in response to Ca2+ and guanine nucleotides: an all-or-none event. J Cell Biol 123: 585–593.
30. 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 U S A 99: 16806–16811.
31. Horrigan FT, Bookman RJ. 1994. Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron 13: 1119–1129.
32. Johns LM, Levitan ES, Shelden EA, Holz RW, Axelrod D. 2001. Restriction of secretory granule motion near the plasma membrane of chromaffin cells. J Cell Biol 153: 177–190.
33. Kandel ER. 2001. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294: 1030–1038.
34. Lang T, Wacker I, Wunderlich I, Rohrbach A, Giese G, Soldati T, and others. 2000. Role of actin cortex in the subplasmalemmal transport of secretory granules in PC-12 cells. Biophys J 78: 2863–2877.
35. Langford GM. 2002. Myosin-V, a versatile motor for short-range vesicle transport. Traffic 3: 859–865.
36. Loerke D. Stuhmer W, Oheim M. 2002. Quantifying axial secretorygranule motion with variable-angle evanescent-field excitation. J Neurosci Methods 119: 65–73.
37. MacGregor RR, Hamilton JW, Cohn DV. 1975. The by-pass of tissue hormone stores during the secretion of newly synthesized parathyroid hormone. Endocrinology 97: 178–188.
38. Manneville JB, Etienne-Manneville S. Skehel P, Carter T, Ogden D, Ferenczi M. 2003. Interaction of the actin cytoskeleton with microtubules regulates secretory organelle movement near the plasma membrane in human endothelial cells. J Cell Sci 116: 3927–3938.
39. Morgan A. Burgoyne RD. 1997. Common mechanisms for regulated exocytosis in the chromaffin cell and the synapse. Semin Cell Dev Biol 8: 141–149.
40. Neco P. Gil A, Del Mar Frances M, Viniegra S, Gutierrez LM. 2002. The role of myosin in vesicle transport during bovine chromaffin cell secretion. Biochem J 368: 405–413.
41. Neco P. Giner D, Viniegra S, Borges R, Villarroel A, Gutierrez LM. 2004. New roles of myosin II during vesicle transport and fusion in chromaffin cells. J Biol Chem 279: 27450–27457.
42. Neher E. Zucker RS. 1993. Multiple calcium-dependent processes related to secretion in bovine chromaffin cells. Neuron 10: 21–30.
43. Ng YK, Lu X. Gulacsi A, Han W, Saxton MJ, Levitan ES. 2003. Unexpected mobility variation among individual secretory vesicles produces an apparent refractory neuropeptide pool. Biophys J 84: 4127–4134.
44. Ng YK, Lu X. Levitan ES. 2002. Physical mobilization of secretory vesicles facilitates neuropeptide release by nerve growth factor-differentiated PC12 cells. J Physiol 542: 395–402.
45. Ng YK, Lu X. Watkins SC, Ellis-Davies GC, Levitan ES. 2002. Nerve growth factor-induced differentiation changes the cellular organization of regulated peptide release by PC12 cells. J Neurosci 22: 3890–3897.
46. Ohara-Imaizumi M. Nakamichi Y, Tanaka T, Ishida H, Nagamatsu S. 2002. Imaging exocytosis of single insulin secretory granules with evanescent wave microscopy: distinct behavior of granule motion in biphasic insulin release. J Biol Chem 277: 3805–3808.
47. Oheim M. 2004. A deeper look into single-secretory vesicle dynamics. Biophys J 87: 1403–1405.
48. Oheim M. Loerke D, Stuhmer W, Chow RH. 1998. The last few milliseconds in the life of a secretory granule. Docking, dynamics and fusion visualized by total internal reflection fluorescence microscopy (TIRFM). Eur Biophys J 27: 83–98.
49. Oheim M. Loerke D, Stuhmer W, Chow RH. 1999. Multiple stimulation-dependent processes regulate the size of the releasable pool of vesicles. Eur Biophys J 28: 91–101.
50. Oheim M. Stuhmer W. 2000a. Interaction of secretory organelles with the membrane. J Membr Biol 178: 163–173.
51. Oheim M. Stuhmer W. 2000b. Tracking chromaffin granules on their way through the actin cortex. Eur Biophys J 29: 67–89.
52. Parsons TD, Coorssen JR, Horstmann H. Almers W. 1995. Docked granules, the exocytic burst, and the need for ATP hydrolysis in endocrine cells. Neuron 15: 1085–1096.
53. Pittman RN, DiBenedetto AJ. 1995. PC12 cells overexpressing tissue plasminogen activator regenerate neurites to a greater extent and migrate faster than control cells in complex extracellular matrix. J Neurochem 64: 566–575.
54. Plattner H. Artalejo AR, Neher E. 1997. Ultrastructural organization of bovine chromaffin cell cortex-analysis by cryofixation and morphometry of aspects pertinent to exocytosis. J Cell Biol 139: 1709–1717.
55. Rose SD, Lejen T. Casaletti L, Larson RE, Pene TD, Trifaro JM. 2003. Myosins II and V in chromaffin cells: myosin V is a chromaffin vesicle molecular motor involved in secretion. J Neurochem 85: 287–298.
56. Rothman JE, Warren G. 1994. Implications of the SNARE hypothesis for intracellular membrane topology and dynamics. Curr Biol 4: 220–233.
57. Rudolf R, Kogel T, Kuznetsov SA, Salm T, Schlicker O, Hellwig A, and others. 2003. Myosin Va facilitates the distribution of secretory granules in the F-actin rich cortex of PC12 cells. J Cell Sci 116: 1339–1348.
58. Ryan TA. 2003. Kiss-and-run, fuse-pinch-and-linger, fuse-and-collapse: the life and times of a neurosecretory granule. Proc Natl Acad Sci U S A 100: 2171–2173.
59. Scalettar BA, Rosa P, Taverna E, Francolini M, Tsuboi T, Terakawa S, and others. 2002. Neuronal calcium sensor-1 binds to regulated secretory organelles and functions in basal and stimulated exocytosis in PC12 cells. J Cell Sci 115: 2399–2412.
60. Shakiryanova D. Tully A, Hewes RS, Deitcher DL, Levitan ES. 2005. Activity-dependent liberation of synaptic neuropeptide vesicles. Nat Neurosci 8: 173–178.
61. Silverman MA, Johnson S, Gurkins D, Farmer M, Lochner JE, Rosa P, and others. 2005. Mechanisms of transport and exocytosis of dense-core granules containing tissue plasminogen activator in developing hippocampal neurons. J Neurosci 25: 3095–3106.
62. Steyer JA, Almers W. 1999. Tracking single secretory granules in live chromaffin cells by evanescent-field fluorescence microscopy. Biophys J 76: 2262–2271.
63. Steyer JA, Horstmann H. Almers W. 1997. Transport, docking and exocytosis of single secretory granules in live chromaffin cells. Nature 388: 474–478.
64. Sudhof TC. 2004. The synaptic vesicle cycle. Annu Rev Neurosci 27: 509–547.
65. Taraska JW, 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 U S A 100: 2070–2075.
66. Thorn NA. 1966. In vitro studies of the release mechanism for vasopressin in rats. Acta Endocrinol (Copenh) 53: 644–654.
67. Tooze SA. 1998. Biogenesis of secretory granules in the trans-Golgi network of neuroendocrine and endocrine cells. Biochim Biophys Acta 1404: 231–244.
68. Trifaro J. Rose SD, Lejen T, Elzagallaai A. 2000. Two pathways control chromaffin cell cortical F-actin dynamics during exocytosis. Biochimie 82: 339–352.
69. Trifaro JM, Vitale ML. 1993. Cytoskeleton dynamics during neurotransmitter release. Trends Neurosci 16: 466–472.
70. Tsuboi T. Kikuta T, Warashina A, Terakawa S. 2001. Protein kinase Cdependent supply of secretory granules to the plasma membrane. Biochem Biophys Res Commun 282: 621–628.
71. Voets T. Neher E, Moser T. 1999. Mechanisms underlying phasic and sustained secretion in chromaffin cells from mouse adrenal slices. Neuron 23: 607–615.
72. Wiegand UK, Duncan RR, Greaves J. Chow RH, Shipston MJ, Apps DK. 2003. Red, yellow, green go!—A novel tool for microscopic segregation of secretory vesicle pools according to their age. Biochem Soc Trans 31: 851–856.
73. Xu T. Ashery U, Burgoyne RD, Neher E. 1999. Early requirement for alpha-SNAP and NSF in the secretory cascade in chromaffin cells. EMBO J 18: 3293–3304.