Syntaxin 13 Mediates Cycling of Plasma Membrane Proteins via Tubulovesicular Recycling Endosomes
Open accessAbstract
Endocytosis-mediated recycling of plasma membrane is a critical vesicle trafficking step important in diverse biological processes. The membrane trafficking decisions and sorting events take place in a series of heterogeneous and highly dynamic organelles, the endosomes. Syntaxin 13, a recently discovered member of the syntaxin family, has been suggested to play a role in mediating endosomal trafficking. To better understand the function of syntaxin 13 we examined its intracellular distribution in nonpolarized cells. By confocal immunofluorescence and electron microscopy, syntaxin 13 is primarily found in tubular early and recycling endosomes, where it colocalizes with transferrin receptor. Additional labeling is also present in endosomal vacuoles, where it is often found in clathrin-coated membrane areas. Furthermore, anti-syntaxin 13 antibody inhibits transferrin receptor recycling in permeabilized PC12 cells. Immunoprecipitation of syntaxin 13 revealed that, in Triton X-100 extracts, syntaxin 13 is present in a complex(es) comprised of βSNAP, VAMP 2/3, and SNAP-25. This complex(es) binds exogenously added αSNAP and NSF and dissociates in the presence of ATP, but not ATPγS. These results support a role for syntaxin 13 in membrane fusion events during the recycling of plasma membrane proteins.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Syntaxin 13 resides in tubular structures that connect the early and recycling endosomes and have been suggested to mediate protein recycling via early/recycling tubulovesicular endosomes enriched in Rab11 endosomes.
“Syntaxin 13 resides in tubular structures that connect the early and recycling endosomes and have been suggested to mediate protein recycling via early/recycling tubulovesicular endosomes that are enriched in Rab11 endosomes [70], [71].”
From Sorting nexin 17 regulates ApoER2 recycling and reelin signaling (2014) · cites this paper as [70]
The Results and Discussion (pages not specified in our copy) place syntaxin 13 on a tubulovesicular recycling network that includes early- and recycling-endosome tubules, and the Discussion suggests a role in protein recycling through that network. The paper describes Rab11 as thought to be specific to recycling endosomes, but does not show that the syntaxin 13–positive structures are enriched in Rab11 or directly connect the two endosome types. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Rat hippocampal neurons in dispersed cell culture.
Banker, G. A., & Cowan, W. M. (1977) · Brain Research · doi:10.1016/0006-8993(77)90594-7 · Cited by 1,110 · see citing works
Flagged first, then by citations
Research works printed but not linked: 64
- [1]Advani RJ Bae HR Bock JB Chao DS Doung YC Prekeris R Yoo JS Scheller RH Seven novel mammalian SNARE proteins localize to distinct membrane compartments J Biol Chem 1998 273 10317 10324 9553086
- [2]Apodaca, G., M.H. Cardone, S.W. Whiteheart, B.R. dasGupta, and K.E. Mostov. 1996. Reconstitution of transcytosis in SLO-permeabilized MDCK cells: existence of an NSF-dependent fusion mechanism with the apical surface of MDCK cells. EMBO (Eur. Mol. Biol. Organ.) J. 15: 1471–1481. PMC450054 8612570
- [4]Bean AJ Seifer R Chen YA Sacks R Scheller RH Hrs-2 is an ATPase implicated in calcium-regulated secretion Nature 1998 385 826 829 9039916
- [5]Becherer KA Rieder SE Emr SD Jones EW Novel syntaxin homologue, Pep12p, required for the sorting of lumenal hydrolases to the lysosome-like vacuole in yeast Mol Biol Cell 1996 7 579 594 8730101 PMC275911
- [6]Bennett MK Scheller RH The molecular machinery for secretion is conserved from yeast to neurons Proc Natl Acad Sci USA 1993 90 2559 2563 8096639 PMC46134
- [7]Bennett MK Scheller RH A molecular description of synaptic vesicle membrane trafficking Annu Rev Biochem 1994 63 63 100 7979250
- [8]Binz T Blasi J Yamasaki S Baumeister A Link E Sudhof TC Jahn R Niemann H Proteolysis of SNAP-25 by types E and A botulinal neurotoxins J Biol Chem 1994 269 1617 1620 8294407
- [9]Bock JB Klumperman J Davanger S Scheller RH Syntaxin 6 functions in trans-Golgi network vesicle trafficking Mol Biol Cell 1997 8 1261 1271 9243506 PMC276151
- [10]Bock JB Lin RC Scheller RH A new syntaxin family member implicated in targeting of intracellular transport vesicles J Biol Chem 1996 271 17961 17965 8663448
- [11]Bucci C Parton RG Mather IH Stunnenberg H Simons K Hoflack B Zerial M The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway Cell 1992 70 715 728 1516130
- [12]Chang MP Mallet WG Mostov KE Brodsky FM Adaptor self-aggregation, adaptor-receptor recognition and binding of alpha-adaptin subunits to the plasma membrane contribute to recruitment of adaptor (AP2) components of clathrin-coated pits EMBO (Eur Mol Biol Organ) J 1993 12 169 180 PMC413438 8491205
- [14]Daro E van der Sliujis P Galli T Mellman I Rab4 and cellubrevin define distinct populations of endosomes on the pathway of transferrin recycling Proc Natl Acad Sci USA 1996 93 9559 9564 8790369 PMC38467
- [15]Darsow T Rieder SE Emr SD A multispecifisity syntaxin homologue, Vam3p, essential for autophagic and biosynthetic proteinm transport to the vacuole J Cell Biol 1997 138 517 529 9245783 PMC2141632
- [16]Dunn KW Mayor S Myers JN Application of ration fluorescence microscopy in the study of cell physiology FASEB (Fed Am Soc Exp Biol) J 1994 8 573 582 8005385
- [17]Galli T Chilcote T Mundigl O Binz T Niemann H de Camilli P Tetanus toxin-mediated cleavage of cellubrevin impairs exocytosis of transferrin receptor-containing vesicles in CHO cells J Cell Biol 1994 125 1015 1024 8195285 PMC2120045
- [18]Geuze HJ Slot JW Strous GJ Peppard J von Figura K Hasilik A Schwartz AL Intracellular receptor sorting during endocytosis: comparative immunoelectron microscopy of multiple receptors in rat liver Cell 1984 37 195 204 6327050
- [19]Gorvel JP Chavrier P Zerial M Gruenberg J rab5 controls early endosome fusion in vitro Cell 1991 64 915 925 1900457
- [20]Gosh RN Gelman DL Maxfield FR Quantification of low density lipoproteins and transferrin endocytic sorting in HEp2 cells using confocal microscopy J Cell Sci 1994 107 2177 2189 7983176
- [21]Gruenberg J Maxfield FR Membrane transport in the endocytic pathway Curr Opin Cell Biol 1995 7 552 563 7495576
- [22]Hanson PI Roth R Morisaki H Jahn R Heuser JE Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy Cell 1997 90 523 535 9267032
- [23]Hay J Martin TFJ Resolution of regulated secretion into sequential MgATP-dependent and Calcium-dependent stages mediated by distinct cytosolic factors J Cell Biol 1992 119 139 151 1527165 PMC2289634
- [24]Hay JC Chao DS Kuo CS Scheller RH Protein interactions regulating vesicle transport between the endoplasmic reticulum and Golgi apparatus in mammalian cells Cell 1997 89 149 158 9094723
- [25]Hay JC Hirling H Scheller RH Mammalian vesicle trafficking proteins of the endoplasmic reticulum and Golgi apparatus J Biol Chem 1996 271 5671 5679 8621431
- [27]Hopkins CR Intracellular routing of transferrin receptors in epidermoid carcinoma A431 cells Cell 1983 35 321 330 6313227
- [28]Hopkins CR Gibson A Shipman M Miller K Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum Nature 1990 346 335 339 2374607
- [29]Hopkins CR Trowbridge IS Internalization and processing of transferrin and transferrin receptor in human carcinoma A431 cells J Cell Biol 1983 97 508 521 6309862 PMC2112524
- [30]Inoue A Akagawa K Neuron specific expression of a membrane protein, HPC-1: tissue distribution, and cellular and subcellular localization of immunoreactivity and mRNA Brain Res Mol Brain Res 1993 19 121 128 8361334
- [31]Kee Y Lin RC Hsu SC Scheller RH Distinct domains of syntaxin are required for synaptic vesicle fusion complex formation and dissociation Neuron 1995 14 991 998 7748566
- [32]Leung, S.M., D. Chen, B.R. dasGupta, S.W. Whiteheart, and G. Apodaca. 1998. SNAP-23 requirement for transferrin recycling in streptolysin-O-permeabilized Madin-Darby canine kidney cells. J. Biol. Chem. 273: 17732–17741. 9651373
- [33]Lin RC Scheller RH Structural organization of the synaptic exocytosis core complex Neuron 1997 19 1087 1094 9390521
- [34]Link E McMahon H Fisher von Mollard G Yamasaki S Niemann H Sudhof TC Jahn R Cleavage of cellubrevin by tetanus toxin does not affect fusion of early endosomes J Biol Chem 1993 268 18423 18426 8360142
- [35]Lippincott-Schwartz J Yuan LC Tipper C Amherdt M Orci L Klausner R Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic Cell 1991 67 601 616 1682055
- [36]Low SH Chapin SJ Wimmer C Whiteheart SW Komuves LG Mostov KE Weimbs T The SNARE machinery is involved in apical plasma membrane trafficking in MDCK cells J Cell Biol 1998 141 1503 1513 9647644 PMC2133007
- [37]Mayor S Presley JF Maxfield FR Sorting of membrane components from endosomes and subsequent recycling to the cell surface J Cell Biol 1993 121 1257 1269 8509447 PMC2119709
- [38]Mellman I Endocytosis and molecular sorting Annu Rev Cell Dev Biol 1996 12 575 625 8970738
- [39]Miettinen JM Matter K Hunziker W Rose JK Mellman I Fc receptors contain a cytoplasmic domain determinant that actively regulates coated pit localization J Cell Biol 1992 118 875 888 PMC2289334 1734021
- [40]Nichols BJ Ungermann C Pelham HR Wickner WT Haas A Homotypic vacuolar fusion mediated by t- and v-SNAREs Nature 1997 387 199 202 9144293
- [41]Nicholson KL Munson M Miller RB Filip TJ Fairman R Hughson FM Regulation of SNARE complex assembly by an N-terminal domain of the t-SNARE Sso1p Nat Struct Biol 1998 5 793 802 9731774
- [42]Oyler GA Higgins GA Hart RA Battenberg E Billingsley M Bloom FE Wilson MC The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations J Cell Biol 1989 109 3039 3052 2592413 PMC2115928
- [43]Pearse BM Clathrin and coated vesicles EMBO (Eur Mol Biol Organ) J 1987 6 2507 2512 2890519 PMC553666
- [44]Pearse BM Robinson MS Clathrin, adaptors, and sorting Annu Rev Cell Biol 1990 6 151 171 2177341
- [45]Reaves B Banting G Perturbation of the morphology of the trans-Golgi network following brefeldin A treatment: redistribution of a TGN-specific integral membrane protein TGN38 J Cell Biol 1992 116 85 94 1730751 PMC2289270
- [46]Robinson MS Kreis TE Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: effect of brefeldin A and G protein activators Cell 1992 69 129 138 1555237
- [47]Robinson MS Watts C Zerial C Membrane dynamics in endocytosis Cell 1996 84 13 21 8548817
- [48]Rossetto O Gorza L Schiavo G Schiavo N Scheller RH Montecucco C VAMP/synaptobrevin usoforms 1 and 2 are widely and differentially expressed in nonneuronal tissues J Cell Biol 1996 132 167 179 8567721 PMC2120699
- [49]Schmid SL Two distinct subpopulations of endosomes involved in membrane recycling and transport to lysosomes Cell 1988 52 73 83 3345561
- [50]Schmid SL Smythe E Stage-specific assays for coated pit formation and coated vesicle budding in vitro J Cell Biol 1991 114 869 880 1908470 PMC2289107
- [51]Schmidt A Hannah MJ Huttner WB Synaptic-like microvesicles of neuroendocrine cells originate from novel compartment that is continuous with plasma membrane and devoid of transferrin receptor J Cell Biol 1997 137 445 458 9128254 PMC2139769
- [52]Simonsen A Lippe R Christoforidis S Gaullier JM Brech A Callaghan J Toh BH Murphy C Zerial M Stenmark H EEA1 links PI(3)K function to rab5 regulation of endosome fusion Nature 1998 394 494 498 9697774
- [53]Slot JW Geuze HJ Gigengack S Lienhard GE James DE Immunolocalization of the insulin regulatable glucose transporter in brown adipose tissue of the rat J Cell Biol 1991 113 123 135 2007617 PMC2288909
- [54]Sollner T Bennett MK Whiteheart SW Scheller RH Rothman JE A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion Cell 1993 75 409 418 8221884
- [55]Sollner T Whiteheart SW Brunner M Erdjument-Bromage H Geromanos S Tempst P Rothman JE SNAP receptors implicated in vesicle targeting and fusion [see Comments] Nature 1993 362 318 324 8455717
- [56]Tagaya M Toyonaga S Takahashi M Yamamoto A Fujiwara T Akagawa K Moriyama Y Mizushima S Syntaxin 1 (HPC-1) is associated with chromaffin granules J Biol Chem 1995 270 15930 15933 7608144
- [57]Tang BL Tan AEH Lim LK Lee SS Low DYH Hong W Syntaxin 12, a member of syntaxin family localized to the endosome J Biol Chem 1998 273 6944 6950 9507000
- [58]Tooze J Hollinshead H Tubular early endosomal networks in AtT20 and other cells J Cell Biol 1991 115 635 653 1918157 PMC2289185
- [59]Trowbridge IS Collawn JF Hopkins CR Signal-dependent membrane protein trafficking in the endocytic pathway Annu Rev Cell Biol 1993 9 129 161 8280459
- [60]Ulrich O Reinsch S Urbe S Zerial M Parton RG Rab11 regulates recycling through the pericentriolar recycling endosome J Cell Biol 1996 135 913 924 8922376 PMC2133374
- [61]van der Sluijs P Hull M Webster P Male P Goud B Mellman I The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway Cell 1992 70 729 740 1516131
- [62]Walch-Solimena C Blasi J Edelmann L Chapman ER von Mollard GF Jahn R The t-SNAREs syntaxin 1 and SNAP-25 are present on organelles that participate in synaptic vesicle recycling J Cell Biol 1995 128 637 645 7860636 PMC2199899
- [63]Wang H Frelin L Pevsner J Human syntaxin 7: a Pep12p/ Vps6p homologue implicated in vesicle trafficking to lysosomes Gene 1997 199 39 48 9358037
- [64]Wei ML Bonzelius F Scully RM Kelly RB Herman GA GLUT4 and transferrin receptor are differentially sorted along the endocytic pathway in CHO cells J Cell Biol 1998 140 565 575 9456317 PMC2140164
- [65]Whiteheart SW Griff IC Brunner M Clary DO Mayer T Buhrow SA Rothman JE SNAP family of NSF attachment proteins includes a brain-specific isoform [see Comments] Nature 1993 362 353 355 8455721
- [66]Wong SH Xu Y Zhang T Hong W Syntaxin 7, a novel syntaxin member associated with the early endosomal compartment J Biol Chem 1998 273 375 380 9417091
- [67]Yamashiro D Tycko B Fluss S Maxfield FR Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway Cell 1984 37 789 800 6204769
Cited by
Sorted by citations
Recycling Endosomes Supply AMPA Receptors for LTP
Park, M., Penick, E. C., Edwards, J. G., Kauer, J. A., & Ehlers, M. D. (2004) · Science · doi:10.1126/science.1102026 · Cited by 730 · see citing works
McBride, H. M., Rybin, V., Murphy, C., Giner, A., Teasdale, R., & Zerial, M. (1999) · Cell · doi:10.1016/s0092-8674(00)81966-2 · Cited by 520 · see citing works
Beyond the role of glutamate as a neurotransmitter
Nedergaard, M., Takano, T., & Hansen, A. J. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn916 · Cited by 450 · see citing works
Raposo, G., & Marks, M. S. (2002) · Traffic · doi:10.1034/j.1600-0854.2002.030401.x · Cited by 161 · see citing works
Wade, N., Bryant, N. J., Connolly, L. M., Simpson, R. J., Luzio, J. P., Piper, R. C., & James, D. E. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m010838200 · Cited by 89 · see citing works
Melanoregulin (MREG) modulates lysosome function in pigment epithelial cells
Damek-Poprawa, M., Diemer, T., Lopes, V. S., Lillo, C., Harper, D. C., Marks, M. S., Wu, Y., Sparrow, J. R., Rachel, R. A., Williams, D. S., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m808857200 · Cited by 50 · see citing works
Sorting nexin 17 regulates ApoER2 recycling and reelin signaling
Sotelo, P., Farfán, P., Benitez, M. L., Bu, G., & Marzolo, M.-P. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093672 · Cited by 47 · see citing works
- Authors
- Prekeris, R., Klumperman, J., Chen, Y. A., & Scheller, R. H.
- Affiliations
- Howard Hughes Medical Institute (US)
- Venue
- The Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 1998-11-16
- Volume
- 143
- Issue
- 4
- Pages
- 957-971
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC2132958
- OpenAlex
- W1979688230
- Cited by
- 286
- References
- 1
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 3 · 2023: 8 · 2022: 6 · 2021: 8 · 2020: 4 · 2019: 7 · 2018: 8 · 2017: 3 · 2016: 4 · 2015: 14 · 2014: 5 · 2013: 8 · 2012: 4
- FWCI
- 6.42
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Keywords
- recycling endosomes, endosomal trafficking, transferrin receptor recycling, membrane fusion, SNARE proteins, SNAP-25, NSF, vesicle trafficking
- MeSH terms
- Adenosine Triphosphate, Animals, Antineoplastic Agents, Biological Transport, Carrier Proteins, Cell Membrane, Cricetinae, Kidney, Ligands, Membrane Proteins, Microscopy, Electron, Nerve Tissue Proteins, Neurons, Protein Synthesis Inhibitors, Endosomes, RNA, Messenger, Synaptic Vesicles, Nocodazole, Gene Expression, CHO Cells, 3T3 Cells, PC12 Cells, Brefeldin A, Vesicular Transport Proteins, R-SNARE Proteins, Qa-SNARE Proteins, Mice, Rats, N-Ethylmaleimide-Sensitive Proteins, Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review