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The t-SNARE Syntaxin 4 Is Regulated during Macrophage Activation to Function in Membrane Traffic and Cytokine Secretion
Open accessAbstract
Activation of macrophages with lipopolysaccharide (LPS) induces the rapid synthesis and secretion of proinflammatory cytokines, such as tumor necrosis factor (TNFalpha), for priming the immune response. TNFalpha plays a key role in inflammatory disease; yet, little is known of the intracellular trafficking events leading to its secretion. In order to identify molecules involved in this secretory pathway, we asked whether any of the known trafficking proteins are regulated by LPS. We found that the levels of SNARE proteins were rapidly and significantly up- or downregulated during macrophage activation. A subset of t-SNAREs (Syntaxin 4/SNAP23/Munc18c) known to control regulated exocytosis in other cell types was substantially increased by LPS in a temporal pattern coinciding with peak TNFalpha secretion. Syntaxin 4 formed a complex with Munc18c at the cell surface of macrophages. Functional studies involving the introduction of Syntaxin 4 cDNA or peptides into macrophages implicate this t-SNARE in a rate-limiting step of TNFalpha secretion and in membrane ruffling during macrophage activation. We conclude that, in macrophages, SNAREs are regulated in order to accommodate the rapid onset of cytokine secretion and for membrane traffic associated with the phenotypic changes of immune activation. This represents a novel regulatory role for SNAREs in regulated secretion and in macrophage-mediated host defense.
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“In macrophages, TNF is released to the extracellular milieu via the constitutive secretion pathway, and its trafficking is the best understood of all cytokines (9, 17, 18).”
From Macrophage Cytokines: Involvement in Immunity and Infectious Diseases (2014) · cites this paper as [18]
In the citing paper
“Thence, the Stx4/SNAP23/VAMP3 complex facilitates the passage of TNF from recycling endosomes to the cell membrane (17, 18).”
From Macrophage Cytokines: Involvement in Immunity and Infectious Diseases (2014) · cites this paper as [18]
In the citing paper
“Moreover, LPS was found to increase the expression of vesicle trafficking proteins that regulate TNF trafficking (17, 18).”
From Macrophage Cytokines: Involvement in Immunity and Infectious Diseases (2014) · cites this paper as [18]
In the citing paper
“The post-Golgi trafficking of IL-6 follows a route that is also dependent on Stx6 and Vti1b, which form a complex with cognate SNARE VAMP3 at recycling endosomes (17, 18).”
From Macrophage Cytokines: Involvement in Immunity and Infectious Diseases (2014) · cites this paper as [18]
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Sorted by citations
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“Thence, the Stx4/SNAP23/VAMP3 complex facilitates the passage of TNF from recycling endosomes to the cell membrane (17, 18).”
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Self-citationThe macrophage response towards LPS and its control through the p38MAPK–STAT3 axis
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“LPS and IFN- , which both regulate gpnmb mRNA, also cause profound changes in post-Golgi trafficking (31, 32).”
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Self-citationPathways for Cytokine Secretion
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“Indeed, several candidate SNARE and Munc18 proteins have already been identified in platelets (Chen et al., 2000), macophages (Pagan et al., 2003), and mast cells (Paumet et al., 2000; Martion-Verdeaux et al., 2002; Puri et al., 2003) and have been shown to be involved in lysosomal secretion.”
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“SNARE proteins have emerged as functional mediators and as particularly useful markers of cytokine secretory pathways (Huse et al., 2006; Moqbel and Coughlin, 2006; Murray et al., 2005b; Pagan et al., 2003; Stow et al., 2006).”
BackgroundInfluentialSelf-citationCytokine Secretion in Macrophages: SNAREs, Rabs, and Membrane Trafficking
Murray, R. Z., & Stow, J. L. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00538 · Cited by 200
“This step of the constitutive pathway, like earlier stages, is also enhanced in activated macrophages by upregulation and increased levels of the cell surface SNAREs (11, 22).”
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“The size, appearance, and kinetics of these carriers are consistent with carriers seen previously in macrophages labeled with TNFα as cargo, and they are also similar to post-Golgi carriers visualized in other cell types (Polishchuk et al., 2000, 2006; Lock et al., 2005; Murray et al., 2005a).”
Self-citationShouts, whispers and the kiss of death: directional secretion in T cells
Huse, M., Quann, E. J., & Davis, M. M. (2008) · Nature Immunology · doi:10.1038/ni.f.215 · Cited by 183
Clinical Uses of Botulinum Neurotoxins: Current Indications, Limitations and Future Developments
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Rab8a interacts directly with PI3Kγ to modulate TLR4-driven PI3K and mTOR signalling
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Self-citationLatham, C. F., Bernal, J. L., Hu, S., Gee, C. L., Westbury, E., Blair, D. H., Armishaw, C. J., Alewood, P. F., Bryant, N. J., James, D. E., et al. (2006) · Traffic · doi:10.1111/j.1600-0854.2006.00474.x · Cited by 133
“They have been shown to regulate a variety of exocytic trafficking steps including the insulin-dependent trafficking of Glucose Transporter 4 (GLUT4) in muscle and fat cells (19,20), the regulated transport of cytokines in macrophages (21) and regulated exocytosis in pancreatic acinar cells (22).”
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“trafficking during TNF- secretion (38).”
Intracellular trafficking and secretion of inflammatory cytokines
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“Instead, they synthesize and transport a sequence of newly made cytokines to the cell surface after activation [50,51,75].”
BackgroundInfluentialSelf-citationVesicular Trafficking and Signaling for Cytokine and Chemokine Secretion in Mast Cells
Blank, U., Madera-Salcedo, I. K., Danelli, L., Claver, J., Tiwari, N., Sánchez-Miranda, E., Vázquez‐Victorio, G., Ramírez‐Valadez, K. A., Macías‐Silva, M., & González‐Espinosa, C. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00453 · Cited by 127
“generally increases their expression, which could be a means to enhance the cytokine trafficking (171, 178).”
BackgroundEndosomal and Phagosomal SNAREs
Dingjan, I., Linders, P. T. A., Verboogen, D. R. J., Revelo, N. H., ter Beest, M., & van den Bogaart, G. (2018) · Physiological Reviews · doi:10.1152/physrev.00037.2017 · Cited by 114
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“Recently, a series of studies, using high-resolution microscopy and live cell imaging, have identified some exocytosis pathways responsible for TNF-a and IL-6 trafficking and secretion (16, 17, 29, 30).”
BackgroundCytokine Secretion via Cholesterol-rich Lipid Raft-associated SNAREs at the Phagocytic Cup
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Self-citationThe SNARE Machinery in Mast Cell Secretion
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“…STX6-STX7-Vti1b with the R-SNARE VAMP3, and second, the membrane fusion of the recycling endosome and the plasma membrane is mediated by the R-SNARE VAMP3 on the recycling endosome by pairing with the STX4–SNAP-23 Q-SNARE complex on the plasma membrane (Pagan et al., 2003; Murray et al., 2005a,b).”
MethodInhibition of the PtdIns(5) kinase PIKfyve disrupts intracellular replication of Salmonella
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Self-citationThe Recruitment of Neutrophils to the Tumor Microenvironment Is Regulated by Multiple Mediators
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“A SNAP23-specific BoNT may also be targeted for other therapeutic applications that include diabetes and inflammatory and immune disorders which include a hypersecretory component (27, 28).”
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“The SNARE proteins syntaxin 4 is implicated in regulated secretion from haematopoetic cells and at the IS [49,50,82,83] and we have demonstrated that syntaxin 4 also contributes to HIV-1 egress at the VS.”
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Rab6a/a’ Are Important Golgi Regulators of Pro-Inflammatory TNF Secretion in Macrophages
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“membrane fusion proteins [5,6,7] and increases the budding of”
BackgroundMethodSelf-citationSyntaxin 11 Binds Vti1b and Regulates Late Endosome to Lysosome Fusion in Macrophages
Offenhäuser, C., Lei, N., Roy, S., Collins, B. M., Stow, J. L., & Murray, R. Z. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01189.x · Cited by 68
“LPS was purchased from Salmonella minosota Re595 and NEM were purchased from Sigma.”
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“Upon activation, macrophages have been found to increase the level of a number of key SNARE proteins including Stx4 and VAMP3 (13,19,20).”
BackgroundMethodSNAP-23 and syntaxin-3 are required for chemokine release by mature human mast cells
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“Data concerning TNF secretion after TLR4 receptor activation have been mainly generated in macrophages, where it is known to require the association of syntaxin-6 and -7 with VAMP3 (20) and the association of SNAP23 with syntaxin-4 (21), among other events (22).”
BackgroundSympathetic excitotoxicity in sepsis: pro-inflammatory priming of macrophages by norepinephrine
Miksa, M. (2005) · Frontiers in bioscience · doi:10.2741/1691 · Cited by 62
“Members of the soluble Nethylmaleimide sensitive factor attachment protein receptor (SNARE) family have been shown to be involved in the intracellular vesicle transport in neurons and immune cells (38-42).”
BackgroundDrosophila14-3-3ε has a crucial role in anti-microbial peptide secretion and innate immunity
Shandala, T., Woodcock, J. M., Ng, Y., Biggs, L., Skoulakis, E. M. C., Brooks, D. A., & Lopez, A. F. (2011) · Journal of Cell Science · doi:10.1242/jcs.080598 · Cited by 62
“Given the function of Syx1a as a component of the exocytic machinery (Gladycheva et al., 2007; Murray et al., 2005; Pagan et al., 2003), the similarity between the 14-3-3 and the Syx1aRNAi phenotypes suggests that 14-3-3 has a role in regulating exocytosis.”
BackgroundLow, P. C., Misaki, R., Schroder, K., Stanley, A. C., Sweet, M. J., Teasdale, R. D., Vanhaesebroeck, B., Meunier, F. A., Taguchi, T., & Stow, J. L. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201001028 · Cited by 64
“Fluorescence microscopy, live cell imaging, and flow cytometry Immunofluorescence staining was performed as previously described (Pagan et al., 2003) on coverslip-adherent macrophages fixed for 1 h at room temperature in 4% paraformaldehyde.”
InfluentialSelf-citationAlpha synuclein in hematopoiesis and immunity
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“In one IL-2 and IFN-γ are secreted directly into the synapse while in the other TNF-α can be multidirectional.”
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Regulation of exocytotic protein expression and Ca2+‐dependent peptide secretion in astrocytes
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Syntaxin7 Is Required for Lytic Granule Release from Cytotoxic T Lymphocytes
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“Immunofluorescence staining was performed as described previously [19]”
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“Our results are in agreement with previously reported changes in murine SNARE protein levels in response to LPS, accommodating the rapid onset of cytokine secretion and membrane traffic associated with the phenotypic changes of immune activation [42].”
ResultOxidized phagosomal NOX2 complex is replenished from lysosomes
Dingjan, I., Linders, P. T. A., van den Bekerom, L., Baranov, M. V., Halder, P., ter Beest, M., & van den Bogaart, G. (2017) · Journal of Cell Science · doi:10.1242/jcs.196931 · Cited by 46
“Although SNAP23 has long been considered to be a plasma membrane SNARE (Chamberlain and Gould, 2002; Hong, 2005; Kawanishi et al., 2000; Pagan et al., 2003; Paumet et al., 2000; Tellam et al., 1997; Volchuk et al., 1996; Wang et al., 2004), it is increasingly clear that it also has intracellular functions in many diff…”
BackgroundOxidized LDL immune complexes induce release of sphingosine kinase in human U937 monocytic cells
Hammad, S. M., Taha, T. A., Nareika, A., Johnson, K. R., Lopes-Virella, M. F., & Obeid, L. M. (2006) · Prostaglandins & Other Lipid Mediators · doi:10.1016/j.prostaglandins.2005.12.004 · Cited by 45
The SNARE VAMP7 Regulates Exocytic Trafficking of Interleukin-12 in Dendritic Cells
Chiaruttini, G., Piperno, G. M., Jouve, M. J., Nardi, F. D., Larghi, P., Peden, A. A., Baj, G., Müller, S., Valitutti, S., Galli, T., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.02.055 · Cited by 45
“Surface delivery of secretory proteins via vesicular SNARE requires a cognate PM acceptor complex constituted by the R-SNAREs SNAP23 and Syntaxin 4 in immune cells (Murray et al., 2005b; Pagan et al., 2003).”
BackgroundRab31 and APPL2 enhance FcγR-mediated phagocytosis through PI3K/Akt signaling in macrophages
Yeo, J. C., Wall, A. A., Luo, L., & Stow, J. L. (2015) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-10-1457 · Cited by 44
“Immunofluorescence, fluorescence microscopy, and live-cell imaging Immunofluorescence staining was performed as previously described (Pagan et al., 2003).”
MethodSelf-citationThe Exocytosis Regulator Synaptotagmin V Controls Phagocytosis in Macrophages
Vinet, A. F., Fukuda, M., & Descoteaux, A. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.8.5289 · Cited by 42
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“…fusion events have been implicated in the process of phagosome formation and maturation during phagocytosis (Hackam et al, 1996; Ward et al, 2000; Braun et al, 2004), as well as the regulation of macrophage secretion of cytokines (Pagan et al, 2003; Murray et al, 2005; Kay et al, 2006).”
BackgroundThe structural and functional evidence for vesicular release from astrocytes in situ
Bohmbach, K., Schwarz, M. K., Schoch, S., & Henneberger, C. (2017) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.01.015 · Cited by 47
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Self-citationSequential recruitment of Rab GTPases during early stages of phagocytosis
Yeo, J. C., Wall, A. A., Luo, L., & Stow, J. L. (2016) · Cellular Logistics · doi:10.1080/21592799.2016.1140615 · Cited by 37
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“Although the reason for their depletion by K5 is unclear, many members of the SNARE family are involved in cytokine (Collins et al., 2015; Naegelen et al., 2015; Pagan et al., 2003) and tumor necrosis factor alpha (TNF-a) secretion (STX7) (Murray et al., 2005).”
BackgroundRobust syntaxin-4 immunoreactivity in mammalian horizontal cell processes
Hirano, A. A., Brandstätter, J. H., VILA, A., & Brecha, N. C. (2007) · Visual Neuroscience · doi:10.1017/s0952523807070198 · Cited by 37
“…from cells in the immune system ~Stow et al., 2006!, such as crystalloid granules from eosinophils ~Logan et al., 2003!, several types of granules from neutrophils ~Logan et al., 2003!, degranulation of mast cells ~Blank et al., 2001!, and cytokine secretion from macrophages ~Pagan et al., 2003!.”
BackgroundNaegelen, I., Plançon, S., Nicot, N., Kaoma, T., Muller, A., Vallar, L., Tschirhart, E. J., & ́chard, S. B. (2014) · Journal of Leukocyte Biology · doi:10.1189/jlb.3a0514-254rr · Cited by 34
“For example, STX4 acts with VAMP3 in TNF secretion and phagocytosis in macrophages [37, 38], whereas these 2 proteins are involved in degranulation in mast cells [41–44].”
BackgroundSikorra, S., Litschko, C., Müller, C., Thiel, N., Galli, T., Eichner, T., & Binz, T. (2015) · Journal of Molecular Biology · doi:10.1016/j.jmb.2015.10.024 · Cited by 32
Verboogen, D. R. J., Mancha, N. G., ter Beest, M., & van den Bogaart, G. (2017) · eLife · doi:10.7554/elife.23525 · Cited by 32
“…muscle cells (Tellam et al., 1997; Hong, 2005), and are also implied in insulin secretion from pancreatic beta cells (Zhu et al., 2015), secretion of dense-core granules, a-granules and lysosomes from human platelets (Schraw et al., 2003) and TNFa secretion from macrophages (Pagan et al., 2003).”
BackgroundBoddul, S. V., Meng, J., Dolly, J. O., & Wang, J. (2013) · FEBS Journal · doi:10.1111/febs.12620 · Cited by 29
Haney, D., Quigley, M. F., Asher, T. E., Ambrozak, D. R., Emma Gostick, D., Price, D. A., Douek, D. C., & Betts, M. R. (2011) · Journal of Immunological Methods · doi:10.1016/j.jim.2011.04.003 · Cited by 26
“Importantly, the TNF-α Processing Inhibitor 0 (TAPI-0) can directly prevent TNF release from the cell surface (Crowe et al., 1995; Pagan et al., 2003; Huse et al., 2006), effectively trapping TNF on the surface of the producing cell.”
BackgroundMeng, J., Zou, X., Wu, R., Zhong, R., Zhu, D., & Zhang, Y. (2014) · Protein & Cell · doi:10.1007/s13238-014-0025-4 · Cited by 28
“In addition, a subset of t-SNAREs (syntaxin 4/SNAP23/Munc18c) performs a regulatory function in cytokine secretion in macrophages (Pagan, 2003).”
BackgroundLipopolysaccharides and Plant Innate Immunity
Erbs, G., Molinaro, A., Dow, J. M., & Newman, M. (2010) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-90-481-9078-2_17 · Cited by 26
Yu, C., Micaroni, M., Puyskens, A., Schultz, T. E., Yeo, J. C., Stanley, A. C., Lucas, M., Kurihara, J. N., Dobos, K. M., Stow, J. L., et al. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1500017 · Cited by 25
“RP105 macrophages by utilizing immunolabeling of surface TNF in cells treated with the TACE inhibitor, TAPI, followed by permeabilization and staining of intracellular TNF with a second round of immunolabeling using a different fluorophore (38) (Fig.”
MethodSelf-citationMedina‐Tamayo, J., Ibarra-Sánchez, A., Padilla-Trejo, A., & González‐Espinosa, C. (2010) · Inflammation Research · doi:10.1007/s00011-010-0230-4 · Cited by 25
“The second fusion process involves the VAMP3-containing recycling endosome and the t-SNARE complex at the plasma membrane comprising syntaxin 4 and SNAP-23 [28, 29].”
BackgroundA role for host cell exocytosis in InlB-mediated internalisation ofListeria monocytogenes
Ngo, H. V., Bhalla, M., Chen, D. W., & Ireton, K. (2017) · Cellular Microbiology · doi:10.1111/cmi.12768 · Cited by 28
“Exofacial VAMP3‐GFP co‐localised with SNAP23 or Munc18‐1 around InlB‐coated beads (Figure S1b), consistent with the roles of these exocytic proteins in InlB‐mediated entry (Figures 1 and 2aii).”
BackgroundInfluentialInvolvement of Cathepsins in Innate and Adaptive Immune Responses in Periodontitis
Yan, X., Wu, Z., Wang, B., Yu, T., Hu, Y., Wang, S., Deng, C., Zhao, B., Nakanishi, H., & Zhang, X. (2020) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2020/4517587 · Cited by 25
The effect of natural products on inflammatory cytokines production and secretion
Barakat, M. M., Syed, N. K., Hasen, E., Abdulrazzaq, S. B., Thiab, S. H., Al‐Najjar, M. A. A., Omar, A., Lucy, T. T., Mamun-Or-Rashid, A. N. M., Yagi, M., et al. (2023) · Phytomedicine Plus · doi:10.1016/j.phyplu.2023.100488 · Cited by 27
Wild-type huntingtin regulates human macrophage function
O’Regan, G. C., Farag, S. H., Ostroff, G. R., Tabrizi, S. J., & André, R. (2020) · Scientific Reports · doi:10.1038/s41598-020-74042-8 · Cited by 22
An Emerging Role for SNARE Proteins in Dendritic Cell Function
Collins, L. E., DeCourcey, J., Luca, M. D., Rochfort, K. D., & Loscher, C. E. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00133 · Cited by 22
Membrane trafficking as an active regulator of constitutively secreted cytokines
Revelo, N. H., ter Beest, M., & van den Bogaart, G. (2019) · Journal of Cell Science · doi:10.1242/jcs.234781 · Cited by 24
“Interestingly, not only does their downregulation by RNAi or the overexpression of dominant-negative mutants lead to reduced secretion of TNF-α – but their overexpression has the opposite effect (Mori et al., 2011;Murray et al., 2005a,b; Pagan et al., 2003), indicating that the levels of these trafficking proteins can…”
BackgroundInfluentialLiaw, K., Gök, Ö., DeRidder, L. B., Kannan, S., & Kannan, R. M. (2018) · Journal of Nanoparticle Research · doi:10.1007/s11051-018-4219-1 · Cited by 20
“This was expected, as LPS activation has been shown to upregulate a variety of internalization pathways, including t-SNARE membrane trafficking, TLR4 endocytosis via clathrin and caveolae pathways, and fluid-phase pinocytosis in macrophages and astrocytes (Peppelenbosch et al. 1999; Pagan et al. 2003; Zanoni et al. 20…”
BackgroundRöhl, J., West, Z. E., Rudolph, M., Zaharia, A., Lonkhuyzen, D. R. V., Hickey, D. K., Semmler, A., & Murray, R. Z. (2019) · Traffic · doi:10.1111/tra.12675 · Cited by 20
“Knockdown of VAMP7 and VAMP8 using siRNA showed both R-SNAREs regulate transport of MT1-MMP and immunoprecipitation experiments show both R-SNAREs can bind to the surface Q-SNARE complex Stx4/SNAP23.”
BackgroundInfluentialThe Rho GTPase Rac1 is required for recycling endosome-mediated secretion of TNF in macrophages
Stanley, A. C., Wong, C. X., Micaroni, M., Venturato, J., Khromykh, T., Stow, J. L., & Lacy, P. (2014) · Immunology & Cell Biology · doi:10.1038/icb.2013.90 · Cited by 21
Self-citationDistinct Roles for APPL1 and APPL2 in Regulating Toll‐like Receptor 4 Signaling in Macrophages
Yeo, J. C., Wall, A. A., Luo, L., Condon, N. D., & Stow, J. L. (2016) · Traffic · doi:10.1111/tra.12415 · Cited by 18
“Immunofluorescence, fluorescence microscopy and live cell imaging Immunofluorescence staining was performed as previously described (34).”
MethodSelf-citationExpression and transcriptional regulation of Munc18 isoforms in mast cells
Nigam, R., Sepulveda, J. L., Tuvim, M. J., Petrova, Y., Adachi, R., Dickey, B. F., & Agrawal, A. (2005) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/j.bbaexp.2005.01.018 · Cited by 17
Dyer, R. P., Isoda, H. M., Salcedo, G. S., Speciale, G., Fletcher, M. H., Le, L. Q., Liu, Y., Brami‐Cherrier, K., Malik, S. Z., Vazquez-Cintron, E. J., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-13617-z · Cited by 15
West, Z. E., Aitcheson, S. M., Semmler, A., & Murray, R. Z. (2021) · Traffic · doi:10.1111/tra.12813 · Cited by 15
“5-fold by 12 hours post LPS stimulation (Figure 3F and Figure S3).(14) Together these results suggest that the VAMP4/Stx6/Stx7/Vti1b trans-SNARE complex regulates transport of MT1-MMP from the Golgi complex to late endosomes/lysosomes and that VAMP4, Vti1b and Stx6 are up-regulated to increase formation of this comple…”
BackgroundHuman monocytes store and secrete preformed CCL5, independent of de novo protein synthesis
Persaud, A. T., Bennett, S. A., Thaya, L., Burnie, J., & Guzzo, C. (2021) · Journal of Leukocyte Biology · doi:10.1002/jlb.3a0820-522rr · Cited by 15
Functions of the Plant Qbc SNARE SNAP25 in Cytokinesis and Biotic and Abiotic Stress Responses.
Won, K., & Kim, H. (2020) · PubMed Central · doi:10.14348/molcells.2020.2245 · Cited by 14
“SNAP23 proteins play a pivotal role in immune cells by mediating the secretion of cytokines, antibodies, and granules (Pagan et al., 2003; Reales et al., 2005; Mollinedo et al., 2006).”
BackgroundChai, Y., Huang, X., Cong, B., Liu, S., Chen, K., Li, G., & Gaisano, H. Y. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.01.138 · Cited by 14
The role of the recycling endosome in regulating lamellipodia formation and macrophage migration
Veale, K. J., Offenhäuser, C., & Murray, R. Z. (2011) · Communicative & Integrative Biology · doi:10.4161/cib.13569 · Cited by 14
Platelet granule secretion mechanisms: Are they modified in sepsis?
Xu, X., & Sun, B. (2015) · Thrombosis Research · doi:10.1016/j.thromres.2015.09.008 · Cited by 13
Duque, G. A., Dion, R., Matte, C., Fabié, A., Descoteaux, J., Stäger, S., & Descoteaux, A. (2021) · The Journal of Immunology · doi:10.4049/jimmunol.2100258 · Cited by 13
Salinas, E., Quintanar‐Stephano, A., Córdova-Dávalos, L. E., & Ouintanar, J. L. (2008) · PubMed · Cited by 11
Weimershaus, M., Carvalho, C., Rignault‐Bricard, R., Waeckel-Énée, E., Dussiot, M., Endert, P. V., Maciel, T. T., & Hermine, O. (2023) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2023.01.014 · Cited by 10
Syntaxin-4 is essential for IgE secretion by plasma cells
Rahman, A., DeCourcey, J., Larbi, N. B., Loughran, S. T., Walls, D., & Loscher, C. E. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.09.058 · Cited by 10
Patients and mice with deficiency in the SNARE protein SYNTAXIN-11 have a secondary B cell defect
Kögl, T., Chang, H., Staniek, J., Chiang, S. C. C., Thoulass, G., Lao, J., Weißert, K., Dettmer‐Monaco, V., Geiger, K., Manna, P. T., et al. (2024) · The Journal of Experimental Medicine · doi:10.1084/jem.20221122 · Cited by 9
“The involvement of STX11 in the transport of cytokines is likely, since other SNARE proteins like STX4 regulate TNF α secretion by macrophages and STX3 is important for IL-6 secretion by DCs (Pagan et al., 2003; Collins et al., 2015; Stanley and Lacy, 2010; Murray and Stow, 2014).”
BackgroundRecombinant expression of Munc18c in a baculovirus system and interaction with syntaxin4
Hu, S., Gee, C. L., Latham, C. F., Rowlinson, S. W., Rova, U., Jones, A., Halliday, J. A., Bryant, N. J., James, D. E., & Martin, J. L. (2003) · Protein Expression and Purification · doi:10.1016/s1046-5928(03)00197-9 · Cited by 9
Self-citationCastañeda-Ramírez, A., González-Rodríguez, D., Ja, H.-P., & Verdugo-Rodríguez, A. (2015) · PubMed Central · Cited by 9
Syntaxin-2 balances phagocytic uptake and phagolysosomal clearance in macrophages
Samanta, S., Nandi, A., Datta, R., & Dolai, S. (2025) · Journal of Cell Science · doi:10.1242/jcs.263855 · Cited by 8
Engineering an Effective Human SNAP-23 Cleaving Botulinum Neurotoxin A Variant
Sikorra, S., Donald, S., Elliott, M. A., Schwede, S., Coker, S.-F., Kupinski, A. P., Tripathi, V., Keith, F., Beard, M., & Binz, T. (2020) · Toxins · doi:10.3390/toxins12120804 · Cited by 8
Metadata
- Authors
- Pagan, J. K., Wylie, F. G., Joseph, S., Widberg, C., Bryant, N. J., James, D. E., & Stow, J. L.
- Affiliations
- The University of Queensland (AU)
- Institute for Molecular Bioscience (AU)
- Garvan Institute of Medical Research (AU)
- Corresponding author
- Stow, Jennifer L
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2003-01
- Volume
- 13
- Issue
- 2
- Pages
- 156-160
- ISSN
- 0960-9822 (ISSN-L)
- OpenAlex
- W2155132039
- Cited by
- 130
- References
- 28
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 11 · 2023: 3 · 2022: 2 · 2021: 5 · 2020: 6 · 2019: 3 · 2018: 3 · 2017: 5 · 2016: 4 · 2015: 9 · 2014: 8 · 2013: 7 · 2012: 7
- FWCI
- 2.10
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 3850 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Health and Medical Research Council
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Keywords
- syntaxin 4, macrophage activation, lipopolysaccharide, TNF-alpha secretion, regulated exocytosis, membrane traffic, Munc18c, SNAP23, cytokine production, ruffles
- MeSH terms
- Animals, Cell Line, Cell Membrane, Lipopolysaccharides, Macrophage Activation, Membrane Proteins, Tumor Necrosis Factor-alpha, Cytokines, Vesicular Transport Proteins, SNARE Proteins, Qa-SNARE Proteins, Mice
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