![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
|
|
|
|
|
||
HY Gaisano, M Ghai, PN Malkus, L Sheu, A Bouquillon, MK Bennett and WS Trimble
Department of Medicine, University of Toronto, Ontario, Canada.
Syntaxins are cytoplasmically oriented integral membrane soluble NEM- sensitive factor receptors (SNAREs; soluble NEM-sensitive factor attachment protein receptors) thought to serve as targets for the assembly of protein complexes important in regulating membrane fusion. The SNARE hypothesis predicts that the fidelity of vesicle traffic is controlled in part by the correct recognition of vesicle SNAREs with their cognate target SNARE partner. Here, we show that in the exocrine acinar cell of the pancreas, multiple syntaxin isoforms are expressed and that they appear to reside in distinct membrane compartments. Syntaxin 2 is restricted to the apical plasma membrane whereas syntaxin 4 is found most abundantly on the basolateral membranes. Surprisingly, syntaxin 3 was found to be localized to a vesicular compartment, the zymogen granule membrane. In addition, we show that these proteins are capable of specific interaction with vesicle SNARE proteins. Their nonoverlapping locations support the general principle of the SNARE hypothesis and provide new insights into the mechanisms of polarized secretion in epithelial cells.
This article has been cited by other articles:
|
|
 |
|
  N. Weng, M. D. Baumler, D. D. H. Thomas, M. A. Falkowski, L. A. Swayne, J. E. A. Braun, and G. E. Groblewski Functional role of J domain of cysteine string protein in Ca2+-dependent secretion from acinar cells Am J Physiol Gastrointest Liver Physiol, May 1, 2009; 296(5): G1030 - G1039. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Procino, C. Barbieri, G. Tamma, L. De Benedictis, J. E. Pessin, M. Svelto, and G. Valenti AQP2 exocytosis in the renal collecting duct - involvement of SNARE isoforms and the regulatory role of Munc18b J. Cell Sci., June 15, 2008; 121(12): 2097 - 2106. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Best, D. A. Sahlender, N. Walther, A. A. Peden, and I. R. Adams Sdmg1 is a conserved transmembrane protein associated with germ cell sex determination and germline-soma interactions in mice Development, April 15, 2008; 135(8): 1415 - 1425. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. I. Cosen-Binker, P. P. L. Lam, M. G. Binker, J. Reeve, S. Pandol, and H. Y. Gaisano Alcohol/Cholecystokinin-evoked Pancreatic Acinar Basolateral Exocytosis Is Mediated by Protein Kinase C{alpha} Phosphorylation of Munc18c J. Biol. Chem., April 27, 2007; 282(17): 13047 - 13058. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Weng, D. D. H. Thomas, and G. E. Groblewski Pancreatic Acinar Cells Express Vesicle-associated Membrane Protein 2- and 8-Specific Populations of Zymogen Granules with Distinct and Overlapping Roles in Secretion J. Biol. Chem., March 30, 2007; 282(13): 9635 - 9645. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Sharma, S. H. Low, S. Misra, B. Pallavi, and T. Weimbs Apical targeting of syntaxin 3 is essential for epithelial cell polarity J. Cell Biol., June 19, 2006; 173(6): 937 - 948. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 X. Chen, A. K. Walker, J. R. Strahler, E. S. Simon, S. L. Tomanicek-Volk, B. B. Nelson, M. C. Hurley, S. A. Ernst, J. A. Williams, and P. C. Andrews Organellar Proteomics: Analysis of Pancreatic Zymogen Granule Membranes Mol. Cell. Proteomics, February 1, 2006; 5(2): 306 - 312. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. H. Low, A. Vasanji, J. Nanduri, M. He, N. Sharma, M. Koo, J. Drazba, and T. Weimbs Syntaxins 3 and 4 Are Concentrated in Separate Clusters on the Plasma Membrane before the Establishment of Cell Polarity Mol. Biol. Cell, February 1, 2006; 17(2): 977 - 989. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. B.A. t. Beest, S. J. Chapin, D. Avrahami, and K. E. Mostov The Role of Syntaxins in the Specificity of Vesicle Targeting in Polarized Epithelial Cells Mol. Biol. Cell, December 1, 2005; 16(12): 5784 - 5792. [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]
|
|
|
|
|
|
J. A. Pickett, P. Thorn, and J. M. Edwardson The Plasma Membrane Q-SNARE Syntaxin 2 Enters the Zymogen Granule Membrane during Exocytosis in the Pancreatic Acinar Cell J. Biol. Chem., January 14, 2005; 280(2): 1506 - 1511. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. L. TUMA and A. L. HUBBARD Transcytosis: Crossing Cellular Barriers Physiol Rev, July 1, 2003; 83(3): 871 - 932. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 X. Li, S. H. Low, M. Miura, and T. Weimbs SNARE expression and localization in renal epithelial cells suggest mechanism for variability of trafficking phenotypes Am J Physiol Renal Physiol, November 1, 2002; 283(5): F1111 - F1122. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Bhattacharya, B. A. Stewart, B. A. Niemeyer, R. W. Burgess, B. D. McCabe, P. Lin, G. Boulianne, C. J. O'Kane, and T. L. Schwarz From the Cover: Members of the synaptobrevin/vesicle-associated membrane protein (VAMP) family in Drosophila are functionally interchangeable in vivo for neurotransmitter release and cell viability PNAS, October 15, 2002; 99(21): 13867 - 13872. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. M. Castle, A. Y. Huang, and J. D. Castle The minor regulated pathway, a rapid component of salivary secretion, may provide docking/fusion sites for granule exocytosis at the apical surface of acinar cells J. Cell Sci., July 15, 2002; 115(14): 2963 - 2973. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Ji, S. Tsuk, A. M. F. Salapatek, X. Huang, D. Chikvashvili, E. A. Pasyk, Y. Kang, L. Sheu, R. Tsushima, N. Diamant, et al. The 25-kDa Synaptosome-associated Protein (SNAP-25) Binds and Inhibits Delayed Rectifier Potassium Channels in Secretory Cells J. Biol. Chem., May 31, 2002; 277(23): 20195 - 20204. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 W. Antonin, M. Wagner, D. Riedel, N. Brose, and R. Jahn Loss of the Zymogen Granule Protein Syncollin Affects Pancreatic Protein Synthesis and Transport but Not Secretion Mol. Cell. Biol., March 1, 2002; 22(5): 1545 - 1554. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. H. Low, L. Y. Marmorstein, M. Miura, X. Li, N. Kudo, A. D. Marmorstein, and T. Weimbs Retinal pigment epithelial cells exhibit unique expression and localization of plasma membrane syntaxins which may contribute to their trafficking phenotype J. Cell Sci., January 12, 2002; 115(23): 4545 - 4553. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Yeaman, K. K. Grindstaff, J. R. Wright, and W. J. Nelson Sec6/8 complexes on trans-Golgi network and plasma membrane regulate late stages of exocytosis in mammalian cells J. Cell Biol., November 12, 2001; 155(4): 593 - 604. [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]
|
|
|
|
|
|
K. Kasai and K. Akagawa Roles of the cytoplasmic and transmembrane domains of syntaxins in intracellular localization and trafficking J. Cell Sci., January 9, 2001; 114(17): 3115 - 3124. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. H. Low, M. Miura, P. A. Roche, A. C. Valdez, K. E. Mostov, and T. Weimbs Intracellular Redirection of Plasma Membrane Trafficking after Loss of Epithelial Cell Polarity Mol. Biol. Cell, September 1, 2000; 11(9): 3045 - 3060. [Abstract] [Full Text]
|
|
|
|
|
|
S. J. An, N. J. Hansen, A. Hodel, R. Jahn, and J. M. Edwardson Analysis of the Association of Syncollin with the Membrane of the Pancreatic Zymogen Granule J. Biol. Chem., April 6, 2000; 275(15): 11306 - 11311. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. T. Watson and J. E. Pessin Functional Cooperation of Two Independent Targeting Domains in Syntaxin 6 Is Required for Its Efficient Localization in the trans-Golgi Network of 3T3L1 Adipocytes J. Biol. Chem., January 14, 2000; 275(2): 1261 - 1268. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. J. Hansen, W. Antonin, and J. M. Edwardson Identification of SNAREs Involved in Regulated Exocytosis in the Pancreatic Acinar Cell J. Biol. Chem., August 6, 1999; 274(32): 22871 - 22876. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. B. Brimhall, K. A. Sikorski, J. Torday, A. Shahsafaei, K. J. Haley, and M. E. Sunday Syntaxin 1A is transiently expressed in fetal lung mesenchymal cells: potential developmental roles Am J Physiol Lung Cell Mol Physiol, August 1, 1999; 277(2): L401 - L411. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. A. Bertrand, C. L. Laboisse, and U. Hopfer Purinergic and cholinergic agonists induce exocytosis from the same granule pool in HT29-Cl.16E monolayers Am J Physiol Cell Physiol, April 1, 1999; 276(4): C907 - C914. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B Quinones, K Riento, V. Olkkonen, S Hardy, and M. Bennett Syntaxin 2 splice variants exhibit differential expression patterns, biochemical properties and subcellular localizations J. Cell Sci., January 12, 1999; 112(23): 4291 - 4304. [Abstract] [PDF]
|
|
|
|
 |
|
 E.L. Watson GTP-Binding Proteins and Regulated Exocytosis Critical Reviews in Oral Biology & Medicine, January 1, 1999; 10(3): 284 - 306. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. YEAMAN, K. K. GRINDSTAFF, and W. J. NELSON New Perspectives on Mechanisms Involved in Generating Epithelial Cell Polarity Physiol Rev, January 1, 1999; 79(1): 73 - 98. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. H. Wong, Y. Xu, T. Zhang, G. Griffiths, S. L. Lowe, V. N. Subramaniam, K. T. Seow, and W. Hong GS32, a Novel Golgi SNARE of 32 kDa, Interacts Preferentially with Syntaxin 6 Mol. Biol. Cell, January 1, 1999; 10(1): 119 - 134. [Abstract] [Full Text]
|
|
|
|
|
|
S. Urbe, L. J. Page, and S. A. Tooze Homotypic Fusion of Immature Secretory Granules during Maturation in a Cell-free Assay J. Cell Biol., December 28, 1998; 143(7): 1831 - 1844. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Tahara, J. R. Coorssen, K. Timmers, P. S. Blank, T. Whalley, R. Scheller, and J. Zimmerberg Calcium Can Disrupt the SNARE Protein Complex on Sea Urchin Egg Secretory Vesicles without Irreversibly Blocking Fusion J. Biol. Chem., December 11, 1998; 273(50): 33667 - 33673. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S.-M. Leung, D. Chen, B. R. DasGupta, S. W. Whiteheart, and G. Apodaca SNAP-23 Requirement for Transferrin Recycling in StreptolysinO-permeabilized Madin-Darby Canine Kidney Cells J. Biol. Chem., July 10, 1998; 273(28): 17732 - 17741. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 X. Huang, M. B. Wheeler, Y.-h. Kang, L. Sheu, G. L. Lukacs, W. S. Trimble, and H. Y. Gaisano Truncated SNAP-25 (1-197), Like Botulinum Neurotoxin A, Can Inhibit Insulin Secretion from HIT-T15 Insulinoma Cells Mol. Endocrinol., July 1, 1998; 12(7): 1060 - 1070. [Abstract] [Full Text]
|
|
|
|
|
|
A. Goyal, R. Singh, E. A. Swietlicki, M. S. Levin, and D. C. Rubin Characterization of rat epimorphin/syntaxin 2 expression suggests a role in crypt-villus morphogenesis Am J Physiol Gastrointest Liver Physiol, July 1, 1998; 275(1): G114 - G124. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. C. Calhoun, L. A. Lapierre, C. S. Chew, and J. R. Goldenring Rab11a redistributes to apical secretory canaliculus during stimulation of gastric parietal cells Am J Physiol Cell Physiol, July 1, 1998; 275(1): C163 - C170. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Galli, A. Zahraoui, V. V. Vaidyanathan, G. Raposo, J. M. Tian, M. Karin, H. Niemann, and D. Louvard A Novel Tetanus Neurotoxin-insensitive Vesicle-associated Membrane Protein in SNARE Complexes of the Apical Plasma Membrane of Epithelial Cells Mol. Biol. Cell, June 1, 1998; 9(6): 1437 - 1448. [Abstract] [Full Text]
|
|
|
|
|
|
M. Plateroti, D. C. Rubin, I. Duluc, R. Singh, C. Foltzer-Jourdainne, J.-N. Freund, and M. Kedinger Subepithelial fibroblast cell lines from different levels of gut axis display regional characteristics Am J Physiol Gastrointest Liver Physiol, May 1, 1998; 274(5): G945 - G954. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Klumperman, R. Kuliawat, J. M. Griffith, H. J. Geuze, and P. Arvan Mannose 6-Phosphate Receptors Are Sorted from Immature Secretory Granules via Adaptor Protein AP-1, Clathrin, and Syntaxin 6-positive Vesicles J. Cell Biol., April 20, 1998; 141(2): 359 - 371. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Ihrke, G. V. Martin, M. R. Shanks, M. Schrader, T. A. Schroer, and A. L. Hubbard Apical Plasma Membrane Proteins and Endolyn-78 Travel through a Subapical Compartment in Polarized WIF-B Hepatocytes J. Cell Biol., April 6, 1998; 141(1): 115 - 133. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. L. Tang, A. E. H. Tan, L. K. Lim, S. S. Lee, D. Y. H. Low, and W. Hong Syntaxin 12, a Member of the Syntaxin Family Localized to the Endosome J. Biol. Chem., March 20, 1998; 273(12): 6944 - 6950. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D Massey-Harroche, N Mayran, and S Maroux Polarized localizations of annexins I, II, VI and XIII in epithelial cells of intestinal, hepatic and pancreatic tissues J. Cell Sci., January 10, 1998; 111(20): 3007 - 3015. [Abstract] [PDF]
|
|
|
|
|
|
K Riento, T Galli, S Jansson, C Ehnholm, E Lehtonen, and V. Olkkonen Interaction of Munc-18-2 with syntaxin 3 controls the association of apical SNAREs in epithelial cells J. Cell Sci., January 9, 1998; 111(17): 2681 - 2688. [Abstract] [PDF]
|
|
|
|
|
|
S. H. Wong, Y. Xu, T. Zhang, and W. Hong Syntaxin 7, a Novel Syntaxin Member Associated with the Early Endosomal Compartment J. Biol. Chem., January 2, 1998; 273(1): 375 - 380. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Mandon, S. Nielsen, B. K. Kishore, and M. A. Knepper Expression of syntaxins in rat kidney Am J Physiol Renal Physiol, November 1, 1997; 273(5): F718 - F730. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Weimbs, S. H. Low, S. J. Chapin, K. E. Mostov, P. Bucher, and K. Hofmann A conserved domain is present in different families of vesicular fusion proteins: A new superfamily PNAS, April 1, 1997; 94(7): 3046 - 3051. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Delgrossi, L Breuza, C Mirre, P Chavrier, and A Le Bivic Human syntaxin 3 is localized apically in human intestinal cells J. Cell Sci., January 9, 1997; 110(18): 2207 - 2214. [Abstract] [PDF]
|
|
|
|
|
|
M Pilon and D. Weisblat A nanos homolog in leech Development, January 5, 1997; 124(9): 1771 - 1780. [Abstract] [PDF]
|
|
