Retinal pigment epithelial cells exhibit unique expression and localization of plasma membrane syntaxins which may contribute to their trafficking phenotype
Abstract
The SNARE membrane fusion machinery controls the fusion of transport vesicles with the apical and basolateral plasma-membrane domains of epithelial cells and is implicated in the specificity of polarized trafficking. To test the hypothesis that differential expression and localization of SNAREs may be a mechanism that contributes to cell-type-specific polarity of different proteins, we studied the expression and distribution of plasma-membrane SNAREs in the retinal pigment epithelium (RPE), an epithelium in which the targeting and steady-state polarity of several plasma membrane proteins differs from most other epithelia. We show here that retinal pigment epithelial cells both in vitro and in vivo differ significantly from MDCK cells and other epithelial cells in their complement of expressed t-SNAREs that are known - or suggested - to be involved in plasma membrane trafficking. Retinal pigment epithelial cells lack expression of the normally apical-specific syntaxin 3. Instead, they express syntaxins 1A and 1B, which are normally restricted to neurons and neuroendocrine cells, on their apical plasma membrane. The polarity of syntaxin 2 is reversed in retinal pigment epithelial cells, and it localizes to a narrow band on the lateral plasma membrane adjacent to the tight junctions. In addition, syntaxin 4 and the v-SNARE endobrevin/VAMP-8 localize to this sub-tight junctional domain, which suggests that this is a region of preferred vesicle exocytosis. Altogether, these data suggest that the unique polarity of many retinal pigment epithelial proteins results from differential expression and distribution of SNAREs at the plasma membrane. We propose that regulation of the expression and subcellular localization of plasma membrane SNAREs may be a general mechanism that contributes to the establishment of distinct sorting phenotypes among epithelial cell types.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
In polarized RPE, calcium ionophores induce exocytosis at both the apical and basolateral domains because syntaxin 4 is non-polar; in MDCK cells, basolateral localization of syntaxin 4 restricts lysosome exocytosis to the basolateral domain.
“In polarized RPE, calcium ionophores induce exocytosis at both the apical and basolateral domains (Xu et al., 2012), because syntaxin 4 is non-polar in the RPE (Low et al., 2002). This is in contrast to Madin-Darby canine kidney (MDCK) cells where basolateral localization of syntaxin 4 (Low et al., 1996) restricts lysosome exocytosis to the basolateral domain (Xu et al., 2012).”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Low et al., 2002
Cites
Membrane fusion and exocytosis.
Jahn, R., & Südhof, T. (1999) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.68.1.863 · Cited by 1,253 · see citing works
SNARE-mediated membrane fusion
Chen, Y. A., & Scheller, R. H. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35052017 · Cited by 1,133 · see citing works
Compartmental specificity of cellular membrane fusion encoded in SNARE proteins
McNew, J. A., Parlati, F., Fukuda, R., Johnston, R. J., Paz, K., Paumet, F., Söllner, T. H., & Rothman, J. E. (2000) · Nature · doi:10.1038/35025000 · Cited by 691 · see citing works
Grindstaff, K. K., Yeaman, C. A., Anandasabapathy, N., Hsu, S.-C., Rodriguez-Boulan, E. J., Scheller, R. H., & Nelson, W. J. (1998) · Cell · doi:10.1016/s0092-8674(00)81435-x · Cited by 527 · see citing works
A Novel Clathrin Adaptor Complex Mediates Basolateral Targeting in Polarized Epithelial Cells
Fölsch, H., Ohno, H., Bonifacino, J. S., & Mellman, I. (1999) · Cell · doi:10.1016/s0092-8674(00)81650-5 · Cited by 515 · see citing works
New Perspectives on Mechanisms Involved in Generating Epithelial Cell Polarity
Yeaman, C. A., Grindstaff, K. K., & Nelson, W. J. (1999) · Physiological Reviews · doi:10.1152/physrev.1999.79.1.73 · Cited by 515 · see citing works
(2011) · SpringerReference · doi:10.1007/springerreference_36603 · Cited by 486 · see citing works
Huber, L. A., Pimplikar, S. W., Parton, R. G., Virta, H., Zerial, M., & Simons, K. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.123.1.35 · Cited by 466 · see citing works
Finnemann, S. C., Bonilha, V. L., Marmorstein, A. D., & Rodriguez-Boulan, E. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.24.12932 · Cited by 382 · see citing works
Membrane traffic in polarized epithelial cells
Mostov, K. E., Vergés, M., & Altschuler, Y. (2000) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(00)00120-4 · Cited by 381 · see citing works
A conserved domain is present in different families of vesicular fusion proteins: A new superfamily
Weimbs, T., Low, S. H., Chapin, S. J., Mostov, K. E., Bücher, P., & Hofmann, K. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.7.3046 · Cited by 315 · see citing works
Galli, T., Zahraoui, A., Vaidyanathan, V. V., Raposo, G., Tian, J. M., Karin, M., Niemann, H., & Louvard, D. (1998) · Molecular Biology of the Cell · doi:10.1091/mbc.9.6.1437 · Cited by 313 · see citing works
Matlin, K. S., & Simons, K. (1984) · The Journal of cell biology · doi:10.1083/jcb.99.6.2131 · Cited by 253 · see citing works
Distribution and Function of Ap-1 Clathrin Adaptor Complexes in Polarized Epithelial Cells
Fölsch, H., Pypaert, M., Schu, P. V., & Mellman, I. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.152.3.595 · Cited by 243 · see citing works
Raft association of SNAP receptors acting in apical trafficking in Madin–Darby canine kidney cells
Lafont, F., Verkade, P., Galli, T., Wimmer, C., Louvard, D., & Simons, K. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.7.3734 · Cited by 242 · see citing works
Olson, A. L., Knight, J. B., & Pessin, J. E. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.5.2425 · Cited by 233 · see citing works
Differential localization of syntaxin isoforms in polarized Madin-Darby canine kidney cells.
Low, S. H. H., Chapin, S. J., Weimbs, T., Kömüves, L. G., Bennett, M. K., & Mostov, K. E. (1996) · Molecular Biology of the Cell · doi:10.1091/mbc.7.12.2007 · Cited by 230 · see citing works
Zahraoui, A., Joberty, G., Arpin, M., Fontaine, J., Hellio, R., Tavitian, A., & Louvard, D. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.124.1.101 · Cited by 228 · see citing works
Characterization of Munc-18c and Syntaxin-4 in 3T3-L1 Adipocytes
Tellam, J., Macaulay, S. L., McIntosh, S. R., Hewish, D. R., Ward, C. W., & James, D. E. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.10.6179 · Cited by 210 · see citing works
SNAREs Contribute to the Specificity of Membrane Fusion
Scales, S. J., Chen, Y. A., Yoo, B. Y., Patel, S. M., Doung, Y.-C., & Scheller, R. H. (2000) · Neuron · doi:10.1016/s0896-6273(00)81177-0 · Cited by 197 · see citing works
The epithelial-specific adaptor AP1B mediates post-endocytic recycling to the basolateral membrane
Gan, Y., McGraw, T. E., & Rodriguez-Boulan, E. J. (2002) · Nature Cell Biology · doi:10.1038/ncb827 · Cited by 195 · see citing works
Distinct cellular locations of the syntaxin family of proteins in rat pancreatic acinar cells.
Gaisano, H. Y., Ghai, M., Malkus, P. N., Sheu, L., Bouquillon, A., Bennett, M. K., & Trimble, W. S. (1996) · Molecular Biology of the Cell · doi:10.1091/mbc.7.12.2019 · Cited by 183 · see citing works
The SNARE Machinery Is Involved in Apical Plasma Membrane Trafficking in MDCK Cells
Low, S. H., Chapin, S. J., Wimmer, C., Whiteheart, S. W., Kömüves, L. G., Mostov, K. E., & Weimbs, T. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.141.7.1503 · Cited by 183 · see citing works
Expression and polarized targeting of a rab3 isoform in epithelial cells.
Weber, E., Berta, G., Tousson, A., John, P. A. S., Green, M. W., Gopalokrishnan, U., Jilling, T., Sorscher, E. J., Elton, T. S., & Abrahamson, D. R. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.125.3.583 · Cited by 178 · see citing works
Zurzolo, C., Lisanti, M. P., Caras, I. W., Nitsch, L., & Rodriguez-Boulan, E. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.121.5.1031 · Cited by 169 · see citing works
Misek, D. E., Bard, E., & Rodriguez-Boulan, E. J. (1984) · Cell · doi:10.1016/0092-8674(84)90460-4 · Cited by 156 · see citing works
The R-SNARE Endobrevin/VAMP-8 Mediates Homotypic Fusion of Early Endosomes and Late Endosomes
Antonin, W., Holroyd, C., Tikkanen, R., Höning, S., & Jahn, R. (2000) · Molecular Biology of the Cell · doi:10.1091/mbc.11.10.3289 · Cited by 156 · see citing works
A model for structural similarity between different SNARE complexes based on sequence relationships
Weimbs, T., Mostov, K. E., Low, S. H., & Hofmann, K. (1998) · Trends in Cell Biology · doi:10.1016/s0962-8924(98)01285-9 · Cited by 153 · see citing works
Immortalization of polarized rat retinal pigment epithelium
Nabi, I. R., Mathews, A. P., Cohen-Gould, L., Gundersen, D., & Rodriguez-Boulan, E. (1993) · Journal of Cell Science · doi:10.1242/jcs.104.1.37 · Cited by 153 · see citing works
The polarity of the retinal pigment epithelium
Marmorstein, A. D. (2001) · Traffic · doi:10.1034/j.1600-0854.2001.21202.x · Cited by 139 · see citing works
Marrs, J. A., Andersson-Fisone, C., Jeong, M. C., Cohen‐Gould, L., Zurzolo, C., Nabi, I. R., Rodriguez-Boulan, E. J., & Nelson, W. J. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.129.2.507 · Cited by 137 · see citing works
Identification of SNAREs Involved in Regulated Exocytosis in the Pancreatic Acinar Cell
Hansen, N. J., Antonin, W., & Edwardson, J. M. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.32.22871 · Cited by 108 · see citing works
Targeting of SNAP-23 and SNAP-25 in Polarized Epithelial Cells
Low, S. H., Roche, P. A., Anderson, H. A., van IJzendoorn, S. C. D., Zhang, M., Mostov, K. E., & Weimbs, T. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.6.3422 · Cited by 108 · see citing works
VAP-33 localizes to both an intracellular vesicle population and with occludin at the tight junction
Lapierre, L. A., Tuma, P. L., Navarre, J., Goldenring, J. R., & Anderson, J. M. (1999) · Journal of Cell Science · doi:10.1242/jcs.112.21.3723 · Cited by 106 · see citing works
Riento, K., Galli, T., Jansson, S., Ehnholm, C., Lehtonen, E., & Olkkonen, V. M. (1998) · Journal of Cell Science · doi:10.1242/jcs.111.17.2681 · Cited by 85 · see citing works
Fujita, H., TUMA, L. P., FINNEGAN, M. C., Locco, L., & HUBBARD, L. A. (1998) · Biochemical Journal · doi:10.1042/bj3290527 · Cited by 83 · see citing works
Peng, X., Yao, X., Chow, D. C., Forte, J. G., & Bennett, M. K. (1997) · Molecular Biology of the Cell · doi:10.1091/mbc.8.3.399 · Cited by 83 · see citing works
Li, X., Low, S. H., Miura, M., & Weimbs, T. (2002) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00185.2002 · Cited by 79 · see citing works
Human syntaxin 3 is localized apically in human intestinal cells
Delgrossi, M.-H., Breuza, L., Mirre, C., Chavrier, P., & Bivic, A. L. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.18.2207 · Cited by 67 · see citing works
Localization of a syntaxin isoform, syntaxin 2, to the acrosomal region of rodent spermatozoa
Katafuchi, K., Mōri, T., Toshimori, K., & Iida, H. (2000) · Molecular Reproduction and Development · doi:10.1002/1098-2795(200012)57:4 · Cited by 66 · see citing works
Quiñones, B., Riento, K., Olkkonen, V. M., Hardy, S. F., & Bennett, M. K. (1999) · Journal of Cell Science · doi:10.1242/jcs.112.23.4291 · Cited by 66 · see citing works
Intracellular Redirection of Plasma Membrane Trafficking after Loss of Epithelial Cell Polarity
Low, S. H., Miura, M., Roche, P. A., Valdez, A. C., Mostov, K. E., & Weimbs, T. (2000) · Molecular Biology of the Cell · doi:10.1091/mbc.11.9.3045 · Cited by 61 · see citing works
Marmorstein, A. D., Gan, Y., Bonilha, V. L., Finnemann, S. C., Csaky, K. G., & Rodriguez-Boulan, E. J. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.3.697 · Cited by 60 · see citing works
SNARE Protein Trafficking in Polarized MDCK Cells
Steegmaier, M., Lee, K. C., Prekeris, R., & Scheller, R. H. (2000) · Traffic · doi:10.1034/j.1600-0854.2000.010705.x · Cited by 60 · see citing works
Saturation of, and competition for entry into, the apical secretory pathway
Marmorstein, A. D., Csaky, K. G., Baffi, J., Lam, L., Rahaal, F., & Rodriguez-Boulan, E. J. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.7.3248 · Cited by 57 · see citing works
Macaulay, S. L., Hewish, D. R., Gough, K. H., Stoichevska, V., MACPHERSON, S. F., Jagadish, M. N., & Ward, C. W. (1997) · Biochemical Journal · doi:10.1042/bj3240217 · Cited by 48 · see citing works
Kuliawat, R., Lisanti, M. P., & Arvan, P. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.6.2478 · Cited by 47 · see citing works
Apical sorting of influenza hemagglutinin by transcytosis in retinal pigment epithelium
Bonilha, V. L., Marmorstein, A. D., Cohen‐Gould, L., & Rodriguez-Boulan, E. J. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.15.1717 · Cited by 39 · see citing works
Protein synthesis and secretion by cultured retinal pigment epithelia
Jaworowski, A., Fang, Z., Khong, T. F., & Augusteyn, R. C. (1995) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(95)00079-q · Cited by 32 · see citing works
Phenotypic plasticity in the intercalated cell: the hensin pathway
Al‐Awqati, Q., Vijayakumar, S., Hikita, C., Chen, J., & Takito, J. (1998) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.1998.275.2.f183 · Cited by 30 · see citing works
Syntaxin 3 and Munc-18-2 in epithelial cells during kidney development
Lehtonen, S. H., Riento, K., Olkkonen, V. M., & Lehtonen, E. (1999) · Kidney International · doi:10.1046/j.1523-1755.1999.00625.x · Cited by 20 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The cell biology of neurogenesis
Götz, M., & Huttner, W. B. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1739 · Cited by 2,130 · see citing works
The cell biology of the retinal pigment epithelium
Lakkaraju, A., Umapathy, A., Tan, L. X., Daniele, L., Philp, N. J., Boesze-Battaglia, K., & Williams, D. S. (2020) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100846 · Cited by 422 · see citing works
Apical trafficking in epithelial cells: signals, clusters and motors
Weisz, O. A., & Rodriguez-Boulan, E. J. (2009) · Journal of Cell Science · doi:10.1242/jcs.032615 · Cited by 299 · see citing works
Polarized epithelial membrane traffic: conservation and plasticity
Mostov, K. E., Su, T., & ter Beest, M. (2003) · Nature Cell Biology · doi:10.1038/ncb0403-287 · Cited by 296 · see citing works
Syntaxin 2 and Endobrevin Are Required for the Terminal Step of Cytokinesis in Mammalian Cells
Low, S. H., Li, X., Miura, M., Kudo, N., Quiñones, B., & Weimbs, T. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00122-9 · Cited by 184 · see citing works
Protein trafficking in the exocytic pathway of polarized epithelial cells
Nelson, W. J., & Yeaman, C. A. (2001) · Trends in Cell Biology · doi:10.1016/s0962-8924(01)02145-6 · Cited by 150 · see citing works
Mazelova, J., Ransom, N. L., Astuto-Gribble, L. M., Wilson, M. C., & Deretic, D. (2009) · Journal of Cell Science · doi:10.1242/jcs.039982 · Cited by 126 · see citing works
Epithelial phenotype and the RPE: Is the answer blowing in the Wnt?
Burke, J. M. (2008) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2008.08.002 · Cited by 124 · see citing works
Apical targeting of syntaxin 3 is essential for epithelial cell polarity
Sharma, N., Low, S. H., Misra, S., Bhattaram, P., & Weimbs, T. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200603132 · Cited by 93 · see citing works
Sherry, D. M., Mitchell, R., Standifer, K. M., & du Plessis, B. (2006) · BMC Neuroscience · doi:10.1186/1471-2202-7-54 · Cited by 87 · see citing works
Iron alters glutamate secretion by regulating cytosolic aconitase activity
McGahan, M. C., Harned, J., Mukunnemkeril, M., Goralska, M., Fleisher, L. N., & Ferrell, J. (2004) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00444.2004 · Cited by 85 · see citing works
Low, S. H., Vasanji, A., Nanduri, J., He, M. Y., Sharma, N., Koo, M., Drazba, J. A., & Weimbs, T. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-05-0462 · Cited by 77 · see citing works
Delivering the message: epimorphin and mammary epithelial morphogenesis
Radisky, D. C., Hirai, Y., & Bissell, M. J. (2003) · Trends in Cell Biology · doi:10.1016/s0962-8924(03)00146-6 · Cited by 75 · see citing works
Deora, A. A., Gravotta, D., Kreitzer, G. E., Hu, J. G., Bok, D., & Rodriguez-Boulan, E. J. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-01-0058 · Cited by 73 · see citing works
Distinct v-SNAREs regulate direct and indirect apical delivery in polarized epithelial cells
Pocard, T., Bivic, A. L., Galli, T., & Zurzolo, C. (2007) · Journal of Cell Science · doi:10.1242/jcs.007948 · Cited by 69 · see citing works
Global gene expression profiling and cluster analysis in Xenopus laevis
Baldessari, D., Shin, Y., Krebs, O., König, R., Koide, T., Vinayagam, A., Fenger, U., Mochii, M., Terasaka, C., Kitayama, A., et al. (2005) · Mechanisms of Development · doi:10.1016/j.mod.2004.11.007 · Cited by 62 · see citing works
Bragina, L., Giovedı̀, S., Barbaresi, P., Benfenati, F., & Conti, F. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.11.009 · Cited by 43 · see citing works
The SNARE Protein Syntaxin 3 Confers Specificity for Polarized Axonal Trafficking in Neurons
Hoo, L. S., Banna, C. D., Radeke, C. M., Sharma, N., Albertolle, M. E., Low, S. H., Weimbs, T., & Vandenberg, C. A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0163671 · Cited by 27 · see citing works
Lee, C., Fishman, H. A., & Bent, S. F. (2007) · Biomaterials · doi:10.1016/j.biomaterials.2007.01.018 · Cited by 22 · see citing works
Weimbs, T., Low, S. H., Li, X., & Kreitzer, G. E. (2003) · Methods · doi:10.1016/s1046-2023(03)00025-2 · Cited by 22 · see citing works
Trafficking mechanisms of synaptogenic cell adhesion molecules
Ribeiro, L. F., Verpoort, B., & de Wit, J. (2018) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.04.003 · Cited by 20 · see citing works
Karvar, S., Zhu, L., Crothers, J. M., Wong, W., Turkoz, M., & Forte, J. G. (2005) · Traffic · doi:10.1111/j.1600-0854.2005.00306.x · Cited by 19 · see citing works
Soluble syntaxin 3 functions as a transcriptional regulator
Giovannone, A. J., Winterstein, C., Bhattaram, P., Reales, E., Low, S. H., Baggs, J. E., Xu, M., Lalli, M. A., Hogenesch, J. B., & Weimbs, T. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra117.000874 · Cited by 18 · see citing works
A platform for assessing outer segment fate in primary human fetal RPE cultures
Zhang, Q., Presswalla, F., Feathers, K. L., Cao, X., Hughes, B. A., Zacks, D. N., Thompson, D. A., & Miller, J. M. L. (2018) · Experimental Eye Research · doi:10.1016/j.exer.2018.10.008 · Cited by 14 · see citing works
The role of syntaxins in retinal function and health
Tebbe, L., Kakakhel, M., Al‐Ubaidi, M. R., & Naash, M. I. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1380064 · Cited by 9 · see citing works
Levetiracetam Affects Differentially Presynaptic Proteins in Rat Cerebral Cortex
Marcotulli, D., Fattorini, G., Bragina, L., Perugini, J., & Conti, F. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00389 · Cited by 9 · see citing works
Kuznetsova, A. V. (2014) · Biology Bulletin Reviews · doi:10.1134/s2079086414020030 · Cited by 2 · see citing works
Protein Trafficking in the Exocytic Pathway of Polarized Epithelial Cells
Yeaman, C. A. (2007) · Elsevier eBooks · doi:10.1016/b978-012369437-9/50020-7 · Cited by 1 · see citing works
Puzzella, C., & Sebastian, P. (2014)
Investigating intracellular SNARE-mediated trafficking of the kidney slit diaphragm protein nephrin
McNeilly, R. E. (2016) · The Atrium (University of Guelph)
Syntaxin‐3 Regulates Tight Junction Assembly in Human Retinal Pigment Epithelium
Ramesh, A., Sivagurunathan, S., Baburajan, N. V., & Chidambaram, S. (2026) · Cell Biochemistry and Function · doi:10.1002/cbf.70294
Guo, H., Yan, R., Han, X., & Yu, W. (2026) · Journal of Inflammation Research · doi:10.2147/jir.s612984
- Authors
- Low, S. H., Marmorstein, L. Y., Miura, M., Li, X., Kudo, N., Marmorstein, A. D., & Weimbs, T.
- Affiliations
- Cleveland Clinic Research (US)
- Cleveland Clinic (US)
- Corresponding author
- Weimbs, Thomas
- Venue
- Journal of Cell Science
- Publisher
- The Company of Biologists
- Published
- 2002-12-01
- Volume
- 115
- Issue
- 23
- Pages
- 4545-4553
- ISSN
- 0021-9533 (ISSN-L)
- 1477-9137
- OpenAlex
- W2148786460
- Cited by
- 32
- References
- 51
- Citations by year
- 2026: 2 · 2024: 1 · 2020: 1 · 2018: 3 · 2017: 1 · 2016: 2 · 2014: 2
- FWCI
- 1.22
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Cell Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Eye Institute (EY13847, R01EY013847, EY 13160)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-62338, R01DK062338)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Keywords
- retinal pigment epithelium, syntaxin, SNARE proteins, plasma membrane trafficking, epithelial polarity, syntaxin 3, syntaxin 1A, syntaxin 1B, syntaxin 2, syntaxin 4, tight junctions, subcellular localization, vesicle exocytosis, MDCK cells
- MeSH terms
- Animals, Cell Line, Cell Membrane, Membrane Proteins, Pigment Epithelium of Eye, Rats, Sprague-Dawley, Protein Transport, Vesicular Transport Proteins, SNARE Proteins, Qa-SNARE Proteins, Rats
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