|
|
||||||||
Physiological Reviews, Vol. 83, No. 2, April 2003, pp. 581-632; 10.1152/physrev.00031.2002.
Copyright ©2003 by the American Physiological Society
The Physiological Laboratory, University of Liverpool, Liverpool, United Kingdom
Burgoyne, Robert D. and
Alan Morgan.
Secretory Granule Exocytosis. Physiol. Rev. 83: 581-632, 2003.
Regulated exocytosis of secretory granules
or dense-core granules has been examined in many
well-characterized cell types including neurons, neuroendocrine,
endocrine, exocrine, and hemopoietic cells and also in other less
well-studied cell types. Secretory granule exocytosis occurs
through mechanisms with many aspects in common with synaptic vesicle
exocytosis and most likely uses the same basic protein components.
Despite the widespread expression and conservation of a core exocytotic
machinery, many variations occur in the control of secretory granule
exocytosis that are related to the specialized physiological role of
particular cell types. In this review we describe the wide range of
cell types in which regulated secretory granule exocytosis occurs and
assess the evidence for the expression of the conserved fusion
machinery in these cells. The signals that trigger and regulate
exocytosis are reviewed. Aspects of the control of exocytosis that are
specific for secretory granules compared with synaptic vesicles or for particular cell types are described and compared to define the range of
accessory control mechanisms that exert their effects on the core
exocytotic machinery.
This article has been cited by other articles:
![]() |
T.-M. Wang and D. W. Hilgemann Ca-dependent Nonsecretory Vesicle Fusion in a Secretory Cell J. Gen. Physiol., June 30, 2008; 132(1): 51 - 65. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Liu, C. Schirra, D. R. Stevens, U. Matti, D. Speidel, D. Hof, D. Bruns, N. Brose, and J. Rettig CAPS Facilitates Filling of the Rapidly Releasable Pool of Large Dense-Core Vesicles J. Neurosci., May 21, 2008; 28(21): 5594 - 5601. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Karatekin, V. S. Tran, S. Huet, I. Fanget, S. Cribier, and J.-P. Henry A 20-nm Step toward the Cell Membrane Preceding Exocytosis May Correspond to Docking of Tethered Granules Biophys. J., April 1, 2008; 94(7): 2891 - 2905. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Zikich, A. Mezer, F. Varoqueaux, A. Sheinin, H. J. Junge, E. Nachliel, R. Melamed, N. Brose, M. Gutman, and U. Ashery Vesicle Priming and Recruitment by ubMunc13-2 Are Differentially Regulated by Calcium and Calmodulin J. Neurosci., February 20, 2008; 28(8): 1949 - 1960. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Hammarlund, S. Watanabe, K. Schuske, and E. M. Jorgensen CAPS and syntaxin dock dense core vesicles to the plasma membrane in neurons J. Cell Biol., February 6, 2008; 180(3): 483 - 491. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. W. Barclay Munc-18-1 Regulates the Initial Release Rate of Exocytosis Biophys. J., February 1, 2008; 94(3): 1084 - 1093. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Kawato, R. Shirakawa, H. Kondo, T. Higashi, T. Ikeda, K. Okawa, S. Fukai, O. Nureki, T. Kita, and H. Horiuchi Regulation of Platelet Dense Granule Secretion by the Ral GTPase-Exocyst Pathway J. Biol. Chem., January 4, 2008; 283(1): 166 - 174. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. N. Medine, C. Rickman, L. H. Chamberlain, and R. R. Duncan Munc18-1 prevents the formation of ectopic SNARE complexes in living cells J. Cell Sci., December 15, 2007; 120(24): 4407 - 4415. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Shibasaki, H. Takahashi, T. Miki, Y. Sunaga, K. Matsumura, M. Yamanaka, C. Zhang, A. Tamamoto, T. Satoh, J.-i. Miyazaki, et al. Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP PNAS, December 4, 2007; 104(49): 19333 - 19338. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. I. Lopez, S. A. Belmonte, G. A. De Blas, and L. S. Mayorga Membrane-permeant Rab3A triggers acrosomal exocytosis in living human sperm FASEB J, December 1, 2007; 21(14): 4121 - 4130. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. I. Rybkin, M.-S. Kim, S. Bezprozvannaya, X. Qi, J. A. Richardson, C. F. Plato, J. A. Hill, R. Bassel-Duby, and E. N. Olson Regulation of atrial natriuretic peptide secretion by a novel Ras-like protein J. Cell Biol., November 5, 2007; 179(3): 527 - 537. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. V. Andreeva, M. A. Kutuzov, and T. A. Voyno-Yasenetskaya Regulation of surfactant secretion in alveolar type II cells Am J Physiol Lung Cell Mol Physiol, August 1, 2007; 293(2): L259 - L271. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. X. Li, A. K. Satoh, and D. F. Ready Myosin V, Rab11, and dRip11 direct apical secretion and cellular morphogenesis in developing Drosophila photoreceptors J. Cell Biol., May 21, 2007; 177(4): 659 - 669. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. R. Jog, M. J. Rane, G. Lominadze, G. C. Luerman, R. A. Ward, and K. R. McLeish The actin cytoskeleton regulates exocytosis of all neutrophil granule subsets Am J Physiol Cell Physiol, May 1, 2007; 292(5): C1690 - C1700. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Rickman, C. N. Medine, A. Bergmann, and R. R. Duncan Functionally and Spatially Distinct Modes of munc18-Syntaxin 1 Interaction J. Biol. Chem., April 20, 2007; 282(16): 12097 - 12103. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. T. W. Handley, L. P. Haynes, and R. D. Burgoyne Differential dynamics of Rab3A and Rab27A on secretory granules J. Cell Sci., March 15, 2007; 120(6): 973 - 984. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Perez-Vilar Mucin Granule Intraluminal Organization Am. J. Respir. Cell Mol. Biol., February 1, 2007; 36(2): 183 - 190. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Yu, K. Kasai, K. Nagashima, S. Torii, H. Yokota-Hashimoto, K. Okamoto, T. Takeuchi, H. Gomi, and T. Izumi Exophilin4/Slp2-a Targets Glucagon Granules to the Plasma Membrane through Unique Ca2+-inhibitory Phospholipid-binding Activity of the C2A Domain Mol. Biol. Cell, February 1, 2007; 18(2): 688 - 696. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Uchida, N. Iwashita, M. Ohara-Imaizumi, T. Ogihara, S. Nagai, J. B. Choi, Y. Tamura, N. Tada, R. Kawamori, K. I. Nakayama, et al. Protein Kinase C{delta} Plays a Non-redundant Role in Insulin Secretion in Pancreatic beta Cells J. Biol. Chem., January 26, 2007; 282(4): 2707 - 2716. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Courel, C. Rodemer, S. T. Nguyen, A. Pance, A. P. Jackson, D. T. O'Connor, and L. Taupenot Secretory Granule Biogenesis in Sympathoadrenal Cells: IDENTIFICATION OF A GRANULOGENIC DETERMINANT IN THE SECRETORY PROHORMONE CHROMOGRANIN A J. Biol. Chem., December 8, 2006; 281(49): 38038 - 38051. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. V. Kim, W. Z. Mehal, X. Dong, V. Heinrich, M. Pypaert, I. Mellman, M. Dembo, M. S. Mooseker, D. Wu, and R. A. Flavell Modulation of cell adhesion and motility in the immune system by Myo1f. Science, October 6, 2006; 314(5796): 136 - 139. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. G. Garcia, A. M. Garcia-De-Diego, L. Gandia, R. Borges, and J. Garcia-Sancho Calcium signaling and exocytosis in adrenal chromaffin cells. Physiol Rev, October 1, 2006; 86(4): 1093 - 1131. [Abstract] [Full Text] [PDF] |
||||
![]() |
W. Shin and K. D. Gillis Measurement of Changes in Membrane Surface Morphology Associated with Exocytosis Using Scanning Ion Conductance Microscopy Biophys. J., September 15, 2006; 91(6): L63 - L65. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Zissimopoulos, D. J. West, A. J. Williams, and F. A. Lai Ryanodine receptor interaction with the SNARE-associated protein snapin J. Cell Sci., June 1, 2006; 119(11): 2386 - 2397. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Takashi, J. Park, S. Fang, S. Koyama, I. Parikh, and K. B. Adler A Peptide Against the N-Terminus of Myristoylated Alanine-Rich C Kinase Substrate Inhibits Degranulation of Human Leukocytes In Vitro Am. J. Respir. Cell Mol. Biol., June 1, 2006; 34(6): 647 - 652. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. L. Davies, C. E. Gibbons, T. Vizard, and D. T. Ward Ca2+-sensing receptor induces Rho kinase-mediated actin stress fiber assembly and altered cell morphology, but not in response to aromatic amino acids Am J Physiol Cell Physiol, June 1, 2006; 290(6): C1543 - C1551. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. C. Gondre-Lewis, H. I. Petrache, C. A. Wassif, D. Harries, A. Parsegian, F. D. Porter, and Y. P. Loh Abnormal sterols in cholesterol-deficiency diseases cause secretory granule malformation and decreased membrane curvature. J. Cell Sci., May 1, 2006; 119(Pt 9): 1876 - 1885. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Wemhoner, M. Frick, P. Dietl, P. Jennings, and T. Haller A Fluorescent Microplate Assay for Exocytosis in Alveolar Type II Cells J Biomol Screen, April 1, 2006; 11(3): 286 - 295. [Abstract] [PDF] |
||||
![]() |
B. A. Scalettar How Neurosecretory Vesicles Release Their Cargo Neuroscientist, April 1, 2006; 12(2): 164 - 176. [Abstract] [PDF] |
||||
![]() |
M. T. Branham, L. S. Mayorga, and C. N. Tomes Calcium-induced Acrosomal Exocytosis Requires cAMP Acting through a Protein Kinase A-independent, Epac-mediated Pathway J. Biol. Chem., March 31, 2006; 281(13): 8656 - 8666. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. Kobayashi, T. Nishi, T. Hirata, A. Kihara, T. Sano, Y. Igarashi, and A. Yamaguchi Sphingosine 1-phosphate is released from the cytosol of rat platelets in a carrier-mediated manner J. Lipid Res., March 1, 2006; 47(3): 614 - 621. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Odling, C. Albertsson, J. T. Russell, and L. G. E. Martensson An in vivo study of exocytosis of cement proteins from barnacle Balanus improvisus (D.) cyprid larva J. Exp. Biol., March 1, 2006; 209(5): 956 - 964. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Perez-Vilar, R. Mabolo, C. T. McVaugh, C. R. Bertozzi, and R. C. Boucher Mucin Granule Intraluminal Organization in Living Mucous/Goblet Cells: ROLES OF PROTEIN POST-TRANSLATIONAL MODIFICATIONS AND SECRETION J. Biol. Chem., February 24, 2006; 281(8): 4844 - 4855. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Kubosaki, S. Nakamura, A. Clark, J. F. Morris, and A. L. Notkins Disruption of the Transmembrane Dense Core Vesicle Proteins IA-2 and IA-2{beta} Causes Female Infertility Endocrinology, February 1, 2006; 147(2): 811 - 815. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. J. O. Evans, J. W. Barclay, G. R. Prescott, S.-R. Jo, R. D. Burgoyne, M. J. Birnbaum, and A. Morgan Protein Kinase B/Akt Is a Novel Cysteine String Protein Kinase That Regulates Exocytosis Release Kinetics and Quantal Size J. Biol. Chem., January 20, 2006; 281(3): 1564 - 1572. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Chakrabarti, J. M. Zee, and K. D. Patel Regulation of matrix metalloproteinase-9 (MMP-9) in TNF-stimulated neutrophils: novel pathways for tertiary granule release J. Leukoc. Biol., January 1, 2006; 79(1): 214 - 222. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Rickman, J. L Jimenez, M. E. Graham, D. A. Archer, M. Soloviev, R. D. Burgoyne, and B. Davletov Conserved Prefusion Protein Assembly in Regulated Exocytosis Mol. Biol. Cell, January 1, 2006; 17(1): 283 - 294. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Iezzi, S. Theander, R. Janz, C. Loze, and C. B. Wollheim SV2A and SV2C are not vesicular Ca2+ transporters but control glucose-evoked granule recruitment J. Cell Sci., December 1, 2005; 118(23): 5647 - 5660. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Thiagarajan, J. Wilhelm, T. Tewolde, Y. Li, M. M. Rich, and K. L. Engisch Enhancement of Asynchronous and Train-Evoked Exocytosis in Bovine Adrenal Chromaffin Cells Infected With a Replication Deficient Adenovirus J Neurophysiol, November 1, 2005; 94(5): 3278 - 3291. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. Oynebraten, N. Barois, K. Hagelsteen, F.-E. Johansen, O. Bakke, and G. Haraldsen Characterization of a Novel Chemokine-Containing Storage Granule in Endothelial Cells: Evidence for Preferential Exocytosis Mediated by Protein Kinase A and Diacylglycerol J. Immunol., October 15, 2005; 175(8): 5358 - 5369. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Gomi, S. Mizutani, K. Kasai, S. Itohara, and T. Izumi Granuphilin molecularly docks insulin granules to the fusion machinery J. Cell Biol., October 10, 2005; 171(1): 99 - 109. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Seino and T. Shibasaki PKA-Dependent and PKA-Independent Pathways for cAMP-Regulated Exocytosis Physiol Rev, October 1, 2005; 85(4): 1303 - 1342. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Watanabe, K. Nomura, A. Ohyama, R. Ishikawa, Y. Komiya, K. Hosaka, E. Yamauchi, H. Taniguchi, N. Sasakawa, K. Kumakura, et al. Myosin-Va Regulates Exocytosis through the Submicromolar Ca2+-dependent Binding of Syntaxin-1A Mol. Biol. Cell, October 1, 2005; 16(10): 4519 - 4530. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. A. Meunier, S. L. Osborne, G. R.V. Hammond, F. T. Cooke, P. J. Parker, J. Domin, and G. Schiavo Phosphatidylinositol 3-Kinase C2{alpha} Is Essential for ATP-dependent Priming of Neurosecretory Granule Exocytosis Mol. Biol. Cell, October 1, 2005; 16(10): 4841 - 4851. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. R. L. Constable, M. E. Graham, A. Morgan, and R. D. Burgoyne Amisyn Regulates Exocytosis and Fusion Pore Stability by Both Syntaxin-dependent and Syntaxin-independent Mechanisms J. Biol. Chem., September 9, 2005; 280(36): 31615 - 31623. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Al-Nedawi, J. Szemraj, and C. S. Cierniewski Mast Cell-Derived Exosomes Activate Endothelial Cells to Secrete Plasminogen Activator Inhibitor Type 1 Arterioscler. Thromb. Vasc. Biol., August 1, 2005; 25(8): 1744 - 1749. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. H. CHOWDHURY, S. GRILC, and R. ZOREC Correlated ATP-Induced Changes in Membrane Area and Membrane Conductance in Single Rat Adipocytes Ann. N.Y. Acad. Sci., June 1, 2005; 1048(1): 281 - 286. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. V. FEDOROVICH, T. V. WASEEM, T. V. LAVRUKEVICH, and S. V. KONEV Role of Calcium in Exocytosis Induced by Hypotonic Swelling Ann. N.Y. Acad. Sci., June 1, 2005; 1048(1): 337 - 340. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Salaun, G. W. Gould, and L. H. Chamberlain Lipid Raft Association of SNARE Proteins Regulates Exocytosis in PC12 Cells J. Biol. Chem., May 20, 2005; 280(20): 19449 - 19453. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Perez-Vilar, J. C. Olsen, M. Chua, and R. C. Boucher pH-dependent Intraluminal Organization of Mucin Granules in Live Human Mucous/Goblet Cells J. Biol. Chem., April 29, 2005; 280(17): 16868 - 16881. [Abstract] [Full Text] [PDF] |
||||
![]() |
L B Hays, B Wicksteed, Y Wang, J F McCuaig, L H Philipson, J M Edwardson, and C J Rhodes Intragranular targeting of syncollin, but not a syncollinGFP chimera, inhibits regulated insulin exocytosis in pancreatic {beta}-cells J. Endocrinol., April 1, 2005; 185(1): 57 - 67. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. A. Silverman, S. Johnson, D. Gurkins, M. Farmer, J. E. Lochner, P. Rosa, and B. A. Scalettar Mechanisms of Transport and Exocytosis of Dense-Core Granules Containing Tissue Plasminogen Activator in Developing Hippocampal Neurons J. Neurosci., March 23, 2005; 25(12): 3095 - 3106. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Ruder, T. Reimer, I. Delgado-Martinez, R. Hermosilla, A. Engelsberg, R. Nehring, B. Dorken, and A. Rehm EBAG9 Adds a New Layer of Control on Large Dense-Core Vesicle Exocytosis via Interaction with Snapin Mol. Biol. Cell, March 1, 2005; 16(3): 1245 - 1257. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Hepp, N. Puri, A. C. Hohenstein, G. L. Crawford, S. W. Whiteheart, and P. A. Roche Phosphorylation of SNAP-23 Regulates Exocytosis from Mast Cells J. Biol. Chem., February 25, 2005; 280(8): 6610 - 6620. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. N. Bulayeva, A. L. Wozniak, L. L. Lash, and C. S. Watson Mechanisms of membrane estrogen receptor-{alpha}-mediated rapid stimulation of Ca2+ levels and prolactin release in a pituitary cell line Am J Physiol Endocrinol Metab, February 1, 2005; 288(2): E388 - E397. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. F. Ciufo, J. W. Barclay, R. D. Burgoyne, and A. Morgan Munc18-1 Regulates Early and Late Stages of Exocytosis via Syntaxin-independent Protein Interactions Mol. Biol. Cell, February 1, 2005; 16(2): 470 - 482. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Salaun, G. W. Gould, and L. H. Chamberlain The SNARE Proteins SNAP-25 and SNAP-23 Display Different Affinities for Lipid Rafts in PC12 Cells: REGULATION BY DISTINCT CYSTEINE-RICH DOMAINS J. Biol. Chem., January 14, 2005; 280(2): 1236 - 1240. [Abstract] [Full Text] [PDF] |
||||
![]() |
C.N. Tomes, G.A. De Blas, M.A. Michaut, E.V. Farre, O. Cherhitin, P.E. Visconti, and L.S. Mayorga {alpha}-SNAP and NSF are required in a priming step during the human sperm acrosome reaction Mol. Hum. Reprod., January 1, 2005; 11(1): 43 - 51. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Cocucci, G. Racchetti, P. Podini, M. Rupnik, and J. Meldolesi Enlargeosome, an Exocytic Vesicle Resistant to Nonionic Detergents, Undergoes Endocytosis via a Nonacidic Route Mol. Biol. Cell, December 1, 2004; 15(12): 5356 - 5368. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Burdakov Electrical Signaling in Central Orexin/Hypocretin Circuits: Tuning Arousal and Appetite to Fit the Environment Neuroscientist, August 1, 2004; 10(4): 286 - 291. [Abstract] [PDF] |
||||
![]() |
M. E. Graham, J. W. Barclay, and R. D. Burgoyne Syntaxin/Munc18 Interactions in the Late Events during Vesicle Fusion and Release in Exocytosis J. Biol. Chem., July 30, 2004; 279(31): 32751 - 32760. [Abstract] [Full Text] [PDF] |
||||