 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
The Journal of Neuroscience, November 1, 2002, 22(21):9278-9286
Protein Kinase C-Dependent Phosphorylation of Synaptosome-Associated Protein of 25 kDa at Ser187 Potentiates Vesicle Recruitment
Gábor Nagy1, Ulf Matti2, Ralf B. Nehring1, Thomas Binz2, Jens Rettig1, Erwin Neher1, and Jakob B. Sørensen1 1 Max Planck Institute for Biophysical Chemistry, 37077 Göttingen, Germany, and 2 Institute for Physiological Chemistry, Medical University Hannover, 30625 Hannover, Germany
Activation of protein kinase C (PKC) constitutes a key event in the upregulation of secretory strength in neurons and neurosecretory cells during extensive stimulation, presumably by speeding up vesicle supply. However, the molecular targets and their mode of action remain elusive. We studied the only PKC-dependent phosphorylation site in the neuronal soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) complex, Ser187, in synaptosome-associated protein of 25 kDa (SNAP-25). This phosphorylation site is located within the negatively charged C-terminal end of SNAP-25, which has been shown to be of critical importance in calcium-triggered exocytosis. We combined mutational studies that used overexpression in chromaffin cells with capacitance measurements and flash photolysis of caged calcium, allowing for high time resolution during both the stimulation and measurement of exocytosis. Overexpression of mutants simulating the phosphorylated form of Ser187 accelerated vesicle recruitment after the emptying of the releasable vesicle pools. Overexpression of mutants simulating the nonphosphorylated form, or block of PKC, impaired the refilling of the vesicle pools to similar extents. Biochemical studies verified the phosphorylation of a subpopulation of SNAP-25 after elevation of intracellular calcium concentrations. Some of the mutations led to a moderately decreased fast exocytotic burst component, which did not seem to be associated with the phosphorylation state of SNAP-25. Thus the C terminus of SNAP-25 plays a role for both fast exocytosis triggering and vesicle recruitment, and the latter process is regulated by PKC-dependent phosphorylation.
Key words: chromaffin cell; exocytosis; membrane capacitance; protein kinase C; SNARE proteins; SNAP-25
Copyright © 2002 Society for Neuroscience 0270-6474/02/22219278-09$05.00/0
This article has been cited by other articles:
W. Liu, Y. Wei, P. Sun, W.-H. Wang, T. R. Kleyman, and L. M. Satlin
Mechanoregulation of BK channel activity in the mammalian cortical collecting duct: role of protein kinases A and C
Am J Physiol Renal Physiol, October 1, 2009; 297(4): F904 - F915.
[Abstract] [Full Text] [PDF]
M. Nojiri, K. M. Loyet, V. A. Klenchin, G. Kabachinski, and T. F. J. Martin
CAPS Activity in Priming Vesicle Exocytosis Requires CK2 Phosphorylation
J. Biol. Chem., July 10, 2009; 284(28): 18707 - 18714.
[Abstract] [Full Text] [PDF]
M. G. Pedersen and A. Sherman
Newcomer insulin secretory granules as a highly calcium-sensitive pool
PNAS, May 5, 2009; 106(18): 7432 - 7436.
[Abstract] [Full Text] [PDF]
H. Cai, K. Reim, F. Varoqueaux, S. Tapechum, K. Hill, J. B. Sorensen, N. Brose, and R. H. Chow
Complexin II plays a positive role in Ca2+-triggered exocytosis by facilitating vesicle priming
PNAS, December 9, 2008; 105(49): 19538 - 19543.
[Abstract] [Full Text] [PDF]
G. Nagy, I. Milosevic, R. Mohrmann, K. Wiederhold, A. M. Walter, and J. B. Sorensen
The SNAP-25 Linker as an Adaptation Toward Fast Exocytosis
Mol. Biol. Cell, September 1, 2008; 19(9): 3769 - 3781.
[Abstract] [Full Text] [PDF]
X. Lou, N. Korogod, N. Brose, and R. Schneggenburger
Phorbol Esters Modulate Spontaneous and Ca2+-Evoked Transmitter Release via Acting on Both Munc13 and Protein Kinase C
J. Neurosci., August 13, 2008; 28(33): 8257 - 8267.
[Abstract] [Full Text] [PDF]
L. Eliasson, F. Abdulkader, M. Braun, J. Galvanovskis, M. B. Hoppa, and P. Rorsman
Novel aspects of the molecular mechanisms controlling insulin secretion
J. Physiol., July 15, 2008; 586(14): 3313 - 3324.
[Abstract] [Full Text] [PDF]
R. Friedrich, A. J. Groffen, E. Connell, J. R. T. van Weering, O. Gutman, Y. I. Henis, B. Davletov, and U. Ashery
DOC2B Acts as a Calcium Switch and Enhances Vesicle Fusion
J. Neurosci., July 2, 2008; 28(27): 6794 - 6806.
[Abstract] [Full Text] [PDF]
N. D. Amin, Y.-L. Zheng, S. Kesavapany, J. Kanungo, T. Guszczynski, R. K. Sihag, P. Rudrabhatla, W. Albers, P. Grant, and H. C. Pant
Cyclin-Dependent Kinase 5 Phosphorylation of Human Septin SEPT5 (hCDCrel-1) Modulates Exocytosis
J. Neurosci., April 2, 2008; 28(14): 3631 - 3643.
[Abstract] [Full Text] [PDF]
D. Pozzi, S. Condliffe, Y. Bozzi, M. Chikhladze, C. Grumelli, V. Proux-Gillardeaux, M. Takahashi, S. Franceschetti, C. Verderio, and M. Matteoli
Activity-dependent phosphorylation of Ser187 is required for SNAP-25-negative modulation of neuronal voltage-gated calcium channels
PNAS, January 8, 2008; 105(1): 323 - 328.
[Abstract] [Full Text] [PDF]
Y. Shu, X. Liu, Y. Yang, M. Takahashi, and K. D. Gillis
Phosphorylation of SNAP-25 at Ser187 Mediates Enhancement of Exocytosis by a Phorbol Ester in INS-1 Cells
J. Neurosci., January 2, 2008; 28(1): 21 - 30.
[Abstract] [Full Text] [PDF]
N. Korogod, X. Lou, and R. Schneggenburger
Posttetanic potentiation critically depends on an enhanced Ca2+ sensitivity of vesicle fusion mediated by presynaptic PKC
PNAS, October 2, 2007; 104(40): 15923 - 15928.
[Abstract] [Full Text] [PDF]
J.-Y. Hu, Y. Chen, and S. Schacher
Protein Kinase C Regulates Local Synthesis and Secretion of a Neuropeptide Required for Activity-Dependent Long-Term Synaptic Plasticity
J. Neurosci., August 15, 2007; 27(33): 8927 - 8939.
[Abstract] [Full Text] [PDF]
A. Gulyas-Kovacs, H. de Wit, I. Milosevic, O. Kochubey, R. Toonen, J. Klingauf, M. Verhage, and J. B. Sorensen
Munc18-1: Sequential Interactions with the Fusion Machinery Stimulate Vesicle Docking and Priming
J. Neurosci., August 8, 2007; 27(32): 8676 - 8686.
[Abstract] [Full Text] [PDF]
T. Rose, S. Efendic, and M. Rupnik
Ca2+-Secretion Coupling Is Impaired in Diabetic Goto Kakizaki rats
J. Gen. Physiol., June 1, 2007; 129(6): 493 - 508.
[Abstract] [Full Text] [PDF]
W. S. Sossin
Isoform specificity of protein kinase Cs in synaptic plasticity
Learn. Mem., April 2, 2007; 14(4): 236 - 246.
[Abstract] [Full Text] [PDF]
Y. Yang, T. J. Craig, X. Chen, L. F. Ciufo, M. Takahashi, A. Morgan, and K. D. Gillis
Phosphomimetic Mutation of Ser-187 of SNAP-25 Increases both Syntaxin Binding and Highly Ca2+-sensitive Exocytosis
J. Gen. Physiol., March 26, 2007; 129(3): 233 - 244.
[Abstract] [Full Text] [PDF]
G. Houeland, A. Nakhost, W. S. Sossin, and V. F. Castellucci
PKC Modulation of Transmitter Release by SNAP-25 at Sensory-to-Motor Synapses in Aplysia
J Neurophysiol, January 1, 2007; 97(1): 134 - 143.
[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]
M. D. Fullerton, L. Wagner, Z. Yuan, and M. Bakovic
Impaired trafficking of choline transporter-like protein-1 at plasma membrane and inhibition of choline transport in THP-1 monocyte-derived macrophages
Am J Physiol Cell Physiol, April 1, 2006; 290(4): C1230 - C1238.
[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]
G. Nagy, J. H. Kim, Z. P. Pang, U. Matti, J. Rettig, T. C. Sudhof, and J. B. Sorensen
Different Effects on Fast Exocytosis Induced by Synaptotagmin 1 and 2 Isoforms and Abundance But Not by Phosphorylation
J. Neurosci., January 11, 2006; 26(2): 632 - 643.
[Abstract] [Full Text] [PDF]
G. Nagy, I. Milosevic, D. Fasshauer, E. M. Muller, B. L. de Groot, T. Lang, M. C. Wilson, and J. B. Sorensen
Alternative Splicing of SNAP-25 Regulates Secretion through Nonconservative Substitutions in the SNARE Domain
Mol. Biol. Cell, December 1, 2005; 16(12): 5675 - 5685.
[Abstract] [Full Text] [PDF]
S. A. Andric, D. Zivadinovic, A. E. Gonzalez-Iglesias, A. Lachowicz, M. Tomic, and S. S. Stojilkovic
Endothelin-induced, Long Lasting, and Ca2+ Influx-independent Blockade of Intrinsic Secretion in Pituitary Cells by Gz Subunits
J. Biol. Chem., July 22, 2005; 280(29): 26896 - 26903.
[Abstract] [Full Text] [PDF]
I. Milosevic, J. B. Sorensen, T. Lang, M. Krauss, G. Nagy, V. Haucke, R. Jahn, and E. Neher
Plasmalemmal Phosphatidylinositol-4,5-Bisphosphate Level Regulates the Releasable Vesicle Pool Size in Chromaffin Cells
J. Neurosci., March 9, 2005; 25(10): 2557 - 2565.
[Abstract] [Full Text] [PDF]
L. Puljak, M. J Pagliassotti, Y. Wei, I. Qadri, V. Parameswara, V. Esser, J. G. Fitz, and G. Kilic
Inhibition of cellular responses to insulin in a rat liver cell line. A role for PKC in insulin resistance
J. Physiol., March 1, 2005; 563(2): 471 - 482.
[Abstract] [Full Text] [PDF]
J. Fu, A. P. Naren, X. Gao, G. U. Ahmmed, and A. B. Malik
Protease-activated Receptor-1 Activation of Endothelial Cells Induces Protein Kinase C{alpha}-dependent Phosphorylation of Syntaxin 4 and Munc18c: ROLE IN SIGNALING P-SELECTIN EXPRESSION
J. Biol. Chem., February 4, 2005; 280(5): 3178 - 3184.
[Abstract] [Full Text] [PDF]
M. Elbert, G. Rossi, and P. Brennwald
The Yeast Par-1 Homologs Kin1 and Kin2 Show Genetic and Physical Interactions with Components of the Exocytic Machinery
Mol. Biol. Cell, February 1, 2005; 16(2): 532 - 549.
[Abstract] [Full Text] [PDF]
X. Ma, Y. Zhang, J. Gromada, S. Sewing, P.-O. Berggren, K. Buschard, A. Salehi, J. Vikman, P. Rorsman, and L. Eliasson
Glucagon Stimulates Exocytosis in Mouse and Rat Pancreatic {alpha}-Cells by Binding to Glucagon Receptors
Mol. Endocrinol., January 1, 2005; 19(1): 198 - 212.
[Abstract] [Full Text] [PDF]
T. Galli and V. Haucke
Cycling of Synaptic Vesicles: How Far? How Fast!
Sci. Signal., December 21, 2004; 2004(264): re19 - re19.
[Abstract] [Full Text] [PDF]
Q.-F. Wan, Y. Dong, H. Yang, X. Lou, J. Ding, and T. Xu
Protein Kinase Activation Increases Insulin Secretion by Sensitizing the Secretory Machinery to Ca2+
J. Gen. Physiol., November 29, 2004; 124(6): 653 - 662.
[Abstract] [Full Text] [PDF]
N.-J. Xu, Y.-X. Yu, J.-M. Zhu, H. Liu, L. Shen, R. Zeng, X. Zhang, and G. Pei
Inhibition of SNAP-25 Phosphorylation at Ser187 Is Involved in Chronic Morphine-induced Down-regulation of SNARE Complex Formation
J. Biol. Chem., September 24, 2004; 279(39): 40601 - 40608.
[Abstract] [Full Text] [PDF]
L. Polo-Parada, C. M. Bose, F. Plattner, and L. T. Landmesser
Distinct Roles of Different Neural Cell Adhesion Molecule (NCAM) Isoforms in Synaptic Maturation Revealed by Analysis of NCAM 180 kDa Isoform-Deficient Mice
J. Neurosci., February 25, 2004; 24(8): 1852 - 1864.
[Abstract] [Full Text] [PDF]
N. Brose and E. Neher
Specificity emerges in the dissection of diacylglycerol- and protein kinase C-mediated signalling pathways
PNAS, December 24, 2002; 99(26): 16522 - 16523.
[Full Text] [PDF]
|
|
|
|
 |
|