 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
The Journal of Neuroscience, October 1, 2000, 20(19):7334-7344
Biogenesis of Regulated Exocytotic Carriers in Neuroendocrine Cells
Benjamin A. Eaton, Michael Haugwitz, Dana Lau, and Hsiao-Ping H. Moore Department of Molecular and Cell Biology, University of California at Berkeley, Berkeley, California 94720-3200
Ca2+-triggered exocytosis is a hallmark of neurosecretory granules, but the cellular pathway leading to the assembly of these regulated exocytotic carriers is poorly understood. Here we used the pituitary AtT-20 cell line to study the biogenesis of regulated exocytotic carriers involved in peptide hormone secretion. We show that immature secretory granules (ISGs) freshly budded from the trans-Golgi network (TGN) exhibit characteristics of unregulated exocytotic carriers. During a subsequent maturation period they undergo an important switch to become regulated exocytotic carriers. We have identified a novel sorting pathway responsible for this transition. The SNARE proteins, VAMP4 and synaptotagmin IV (Syt IV), enter ISGs initially but are sorted away during maturation. Sorting is achieved by vesicle budding from the ISGs, because it can be inhibited by brefeldin A (BFA). Inhibition of this sorting pathway with BFA arrested the maturing granules in a state that responded poorly to stimuli, suggesting that the transition to regulated exocytotic carriers requires the removal of a putative inhibitor. In support of this, we found that overexpression of Syt IV reduced the stimulus-responsiveness of maturing granules. We conclude that secretory granules undergo a switch from unregulated to regulated secretory carriers during biogenesis. The existence of such a switch may provide a mechanism for cells to modulate their secretory activities under different physiological conditions.
Key words: regulated exocytosis; secretory granules; membrane remodeling; organelle biogenesis; SNARE proteins; protein sorting
Copyright © 2000 Society for Neuroscience 0270-6474/00/20197334-11$05.00/0
This article has been cited by other articles:
J. A. Sobota, N. Back, B. A. Eipper, and R. E. Mains
Inhibitors of the V0 subunit of the vacuolar H+-ATPase prevent segregation of lysosomal- and secretory-pathway proteins
J. Cell Sci., October 1, 2009; 122(19): 3542 - 3553.
[Abstract] [Full Text] [PDF]
W. W.Y. Lui-Roberts, F. Ferraro, T. D. Nightingale, and D. F. Cutler
Aftiphilin and {gamma}-Synergin Are Required for Secretagogue Sensitivity of Weibel-Palade Bodies in Endothelial Cells
Mol. Biol. Cell, December 1, 2008; 19(12): 5072 - 5081.
[Abstract] [Full Text] [PDF]
F. Ferraro, X.-M. Ma, J. A. Sobota, B. A. Eipper, and R. E. Mains
Kalirin/Trio Rho Guanine Nucleotide Exchange Factors Regulate a Novel Step in Secretory Granule Maturation
Mol. Biol. Cell, December 1, 2007; 18(12): 4813 - 4825.
[Abstract] [Full Text] [PDF]
H. L. Zenner, L. M. Collinson, G. Michaux, and D. F. Cutler
High-pressure freezing provides insights into Weibel-Palade body biogenesis
J. Cell Sci., June 15, 2007; 120(12): 2117 - 2125.
[Abstract] [Full Text] [PDF]
Y. Haberman, I. Ziv, Y. Gorzalczany, K. Hirschberg, L. Mittleman, M. Fukuda, and R. Sagi-Eisenberg
Synaptotagmin (Syt) IX is an essential determinant for protein sorting to secretory granules in mast cells
Blood, April 15, 2007; 109(8): 3385 - 3392.
[Abstract] [Full Text] [PDF]
J. A. Sobota, F. Ferraro, N. Back, B. A. Eipper, and R. E. Mains
Not All Secretory Granules Are Created Equal: Partitioning of Soluble Content Proteins
Mol. Biol. Cell, December 1, 2006; 17(12): 5038 - 5052.
[Abstract] [Full Text] [PDF]
M. Ahras, G. P. Otto, and S. A. Tooze
Synaptotagmin IV is necessary for the maturation of secretory granules in PC12 cells
J. Cell Biol., April 24, 2006; 173(2): 241 - 251.
[Abstract] [Full Text] [PDF]
T. Kim, M. C. Gondre-Lewis, I. Arnaoutova, and Y. P. Loh
Dense-Core Secretory Granule Biogenesis
Physiology, April 1, 2006; 21(2): 124 - 133.
[Abstract] [Full Text] [PDF]
T. Kim and Y. P. Loh
Protease Nexin-1 Promotes Secretory Granule Biogenesis by Preventing Granule Protein Degradation
Mol. Biol. Cell, February 1, 2006; 17(2): 789 - 798.
[Abstract] [Full Text] [PDF]
L. R. Mulcahy, C. A. Vaslet, and E. A. Nillni
Prohormone-Convertase 1 Processing Enhances Post-Golgi Sorting of Prothyrotropin-releasing Hormone-derived Peptides
J. Biol. Chem., December 2, 2005; 280(48): 39818 - 39826.
[Abstract] [Full Text] [PDF]
M. Fukuda, E. Kanno, M. Satoh, C. Saegusa, and A. Yamamoto
Synaptotagmin VII Is Targeted to Dense-core Vesicles and Regulates Their Ca2+-dependent Exocytosis in PC12 Cells
J. Biol. Chem., December 10, 2004; 279(50): 52677 - 52684.
[Abstract] [Full Text] [PDF]
M. Fukuda and A. Yamamoto
Effect of Forskolin on Synaptotagmin IV Protein Trafficking in PC12 Cells
J. Biochem., August 1, 2004; 136(2): 245 - 253.
[Abstract] [Full Text] [PDF]
C. Morenilla-Palao, R. Planells-Cases, N. Garcia-Sanz, and A. Ferrer-Montiel
Regulated Exocytosis Contributes to Protein Kinase C Potentiation of Vanilloid Receptor Activity
J. Biol. Chem., June 11, 2004; 279(24): 25665 - 25672.
[Abstract] [Full Text] [PDF]
R. Kuliawat, E. Kalinina, J. Bock, L. Fricker, T. E. McGraw, S. R. Kim, J. Zhong, R. Scheller, and P. Arvan
Syntaxin-6 SNARE Involvement in Secretory and Endocytic Pathways of Cultured Pancreatic {beta}-Cells
Mol. Biol. Cell, April 1, 2004; 15(4): 1690 - 1701.
[Abstract] [Full Text] [PDF]
R. D. Burgoyne and A. Morgan
Secretory Granule Exocytosis
Physiol Rev, April 1, 2003; 83(2): 581 - 632.
[Abstract] [Full Text] [PDF]
M. Fukuda, E. Kanno, Y. Ogata, C. Saegusa, T. Kim, Y. P. Loh, and A. Yamamoto
Nerve Growth Factor-dependent Sorting of Synaptotagmin IV Protein to Mature Dense-core Vesicles That Undergo Calcium-dependent Exocytosis in PC12 Cells
J. Biol. Chem., January 24, 2003; 278(5): 3220 - 3226.
[Abstract] [Full Text] [PDF]
E. Grimberg, Z. Peng, I. Hammel, and R. Sagi-Eisenberg
Synaptotagmin III is a critical factor for the formation of the perinuclear endocytic recycling compartment and determination of secretory granules size
J. Cell Sci., January 1, 2003; 116(1): 145 - 154.
[Abstract] [Full Text] [PDF]
C. Lavoie, T. Meerloo, P. Lin, and M. G. Farquhar
Calnuc, an EF-Hand Ca2+-Binding Protein, Is Stored and Processed in the Golgi and Secreted by the Constitutive-Like Pathway in AtT20 Cells
Mol. Endocrinol., November 1, 2002; 16(11): 2462 - 2474.
[Abstract] [Full Text] [PDF]
E. Taverna, M. Francolini, A. Jeromin, S. Hilfiker, J. Roder, and P. Rosa
Neuronal calcium sensor 1 and phosphatidylinositol 4-OH kinase {beta} interact in neuronal cells and are translocated to membranes during nucleotide-evoked exocytosis
J. Cell Sci., October 15, 2002; 115(20): 3909 - 3922.
[Abstract] [Full Text] [PDF]
N. Nishimura, H. Plutner, K. Hahn, and W. E. Balch
The delta subunit of AP-3 is required for efficient transport of VSV-G from the trans-Golgi network to the cell surface
PNAS, May 14, 2002; 99(10): 6755 - 6760.
[Abstract] [Full Text] [PDF]
A. D. Blagoveshchenskaya, M. J. Hannah, S. Allen, and D. F. Cutler
Selective and Signal-dependent Recruitment of Membrane Proteins to Secretory Granules Formed by Heterologously Expressed von Willebrand Factor
Mol. Biol. Cell, May 1, 2002; 13(5): 1582 - 1593.
[Abstract] [Full Text] [PDF]
F. Wendler, L. Page, S. Urbe, and S. A. Tooze
Homotypic Fusion of Immature Secretory Granules During Maturation Requires Syntaxin 6
Mol. Biol. Cell, June 1, 2001; 12(6): 1699 - 1709.
[Abstract] [Full Text] [PDF]
M. R. Alam, T. C. Steveson, R. C. Johnson, N. Bäck, B. Abraham, R. E. Mains, and B. A. Eipper
Signaling Mediated by the Cytosolic Domain of Peptidylglycine {alpha}-Amidating Monooxygenase
Mol. Biol. Cell, March 1, 2001; 12(3): 629 - 644.
[Abstract] [Full Text]
A Gut, C. Kiraly, M Fukuda, K Mikoshiba, C. Wollheim, and J Lang
Expression and localisation of synaptotagmin isoforms in endocrine (&bgr;)-cells: their function in insulin exocytosis
J. Cell Sci., January 5, 2001; 114(9): 1709 - 1716.
[Abstract] [PDF]
A. Y. Huang, A. M. Castle, B. T. Hinton, and J. D. Castle
Resting (Basal) Secretion of Proteins Is Provided by the Minor Regulated and Constitutive-like Pathways and Not Granule Exocytosis in Parotid Acinar Cells
J. Biol. Chem., June 15, 2001; 276(25): 22296 - 22306.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|