The Rab5 effector EEA1 is a core component of endosome docking
Abstract
Intracellular membrane docking and fusion requires the interplay between soluble factors and SNAREs. The SNARE hypothesis postulates that pairing between a vesicular v-SNARE and a target membrane z-SNARE is the primary molecular interaction underlying the specificity of vesicle targeting as well as lipid bilayer fusion. This proposal is supported by recent studies using a minimal artificial system. However, several observations demonstrate that SNAREs function at multiple transport steps and can pair promiscuously, questioning the role of SNAREs in conveying vesicle targeting. Moreover, other proteins have been shown to be important in membrane docking or tethering. Therefore, if the minimal machinery is defined as the set of proteins sufficient to reproduce in vitro the fidelity of vesicle targeting, docking and fusion as in vivo, then SNAREs are not sufficient to specify vesicle targeting. Endosome fusion also requires cytosolic factors and is regulated by the small GTPase Rab5. Here we show that Rab5-interacting soluble proteins can completely substitute for cytosol in an in vivo endosome-fusion assay, and that the Rab5 effector EEA1 is the only factor necessary to confer minimal fusion activity. Rab5 and other associated proteins seem to act upstream of EEA1, implying that Rab5 effectors comprise both regulatory molecules and mechanical components of the membrane transport machinery. We further show that EEA1 mediates endosome docking and, together with SNAREs, leads to membrane fusion.
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Rab5A is a marker of early phagosomes and facilitates downstream maturation by recruiting EEA1, which then binds NSF, Rabex5, and Rabaptin-5 and subsequently syntaxin13 to form a fusogenic complex with endosomes.
“The small GTPase Rab5A is a marker of early phagosomes and facilitates downstream maturation by recruiting early endosomal antigen 1 (EEA1), which then binds NSF, Rabex5, and Rabaptin-5 and subsequently syntaxin13 to form a fusogenic complex with endosomes (22–24).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [23]
Cites
SNAREpins: Minimal Machinery for Membrane Fusion
Weber, T., Zemelman, B. V., McNew, J. A., Westermann, B., Gmachl, M., Parlati, F., Söllner, T. H., & Rothman, J. E. (1998) · Cell · doi:10.1016/s0092-8674(00)81404-x · Cited by 2,481 · see citing works
Mechanisms of intracellular protein transport
Rothman, J. E. (1994) · Nature · doi:10.1038/372055a0 · Cited by 2,283 · see citing works
EEA1 links PI(3)K function to Rab5 regulation of endosome fusion
Simonsen, A., Lippe, R., Christoforidis, S., Gaullier, J.-M., Brech, A., Callaghan, J., Toh, B.-H., Murphy, C., Zerial, M., & Stenmark, H. (1998) · Nature · doi:10.1038/28879 · Cited by 1,133 · see citing works
Self-citationrab5 controls early endosome fusion in vitro
Gorvel, J., Chavrier, P., Zerial, M., & Gruenberg, J. E. (1991) · Cell · doi:10.1016/0092-8674(91)90316-q · Cited by 1,094 · see citing works
Self-citationThe diversity of Rab proteins in vesicle transport
Novick, P., & Zerial, M. (1997) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(97)80025-7 · Cited by 767 · see citing works
Self-citationEEA1, an Early Endosome-Associated Protein.
Mu, F., Callaghan, J. M., Steele‐Mortimer, O., Stenmark, H., Parton, R. G., Campbell, P. L., McCluskey, J., Yeo, J.-P., Tock, E. P. C., & Toh, B. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.22.13503 · Cited by 714 · see citing works
Horiuchi, H., Lippé, R., McBride, H. M., Rubino, M., Woodman, P. G., Stenmark, H., Rybin, V., Wilm, M. S., Ashman, K., Mann, M., et al. (1997) · Cell · doi:10.1016/s0092-8674(00)80380-3 · Cited by 595 · see citing works
Self-citationSec18p (NSF)-Driven Release of Sec17p (α-SNAP) Can Precede Docking and Fusion of Yeast Vacuoles
Mayer, A., Wickner, W. T., & Haas, A. (1996) · Cell · doi:10.1016/s0092-8674(00)81084-3 · Cited by 580 · see citing works
A rab protein is required for the assembly of SNARE complexes in the docking of transport vesicles
Søgaard, M., Tani, K., Ye, R. R., Geromanos, S. J., Tempst, P., Kirchhausen, T. L., Rothman, J. E., & Söllner, T. H. (1994) · Cell · doi:10.1016/0092-8674(94)90270-4 · Cited by 503 · see citing works
Endosomal Localization of the Autoantigen EEA1 Is Mediated by a Zinc-binding FYVE Finger
Stenmark, H., Aasland, R., Toh, B., & D’Arrigo, A. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.39.24048 · Cited by 483 · see citing works
Initial docking of ER‐derived vesicles requires Uso1p and Ypt1p but is independent of SNARE proteins
Cao, X., Ballew, N., & Barlowe, C. K. (1998) · The EMBO Journal · doi:10.1093/emboj/17.8.2156 · Cited by 366 · see citing works
A Role for Giantin in Docking COPI Vesicles to Golgi Membranes
Sönnichsen, B., Lowe, M., Levine, T. P., Jokitalo, E., Dirac-Svejstrup, A. B., & Warren, G. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.140.5.1013 · Cited by 284 · see citing works
Annexin II is a major component of fusogenic endosomal vesicles.
Emans, N., Gorvel, J., Walter, C., Gerke, V., Kellner, R., Griffiths, G. W., & Gruenberg, J. E. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.120.6.1357 · Cited by 269 · see citing works
Two syntaxin homologues in the TGN/endosomal system of yeast
Holthuis, J. C. M., Nichols, B. J., Dhruvakumar, S., & Pelham, H. R. B. (1998) · The EMBO Journal · doi:10.1093/emboj/17.1.113 · Cited by 255 · see citing works
Mayer, A., & Wickner, W. T. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.136.2.307 · Cited by 238 · see citing works
Identification of an early endosomal protein regulated by phosphatidylinositol 3-kinase
Patki, V., Virbasius, J., Lane, W. S., Toh, B., Shpetner, H. S., & Corvera, S. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.14.7326 · Cited by 228 · see citing works
von Mollard, G. F., Nothwehr, S. F., & Stevens, T. H. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.137.7.1511 · Cited by 216 · see citing works
t-SNARE Activation Through Transient Interaction with a Rab-Like Guanosine Triphosphatase
Lupashin, V. V., & Waters, M. G. (1997) · Science · doi:10.1126/science.276.5316.1255 · Cited by 212 · see citing works
Ypt1p implicated in v-SNARE activation
Lian, J. P., Stone, S., Jiang, Y., Lyons, P., & Ferro‐Novick, S. (1994) · Nature · doi:10.1038/372698a0 · Cited by 197 · see citing works
Assembly of the ER to Golgi SNARE complex requires Uso1p.
Sapperstein, S. K., Lupashin, V. V., Schmitt, H. D., & Waters, M. G. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.132.5.755 · Cited by 192 · see citing works
Barnard, R. J. O., Morgan, A., & Burgoyne, R. D. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.139.4.875 · Cited by 178 · see citing works
Self-citationCoupled ER to Golgi Transport Reconstituted with Purified Cytosolic Proteins
Barlowe, C. K. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.139.5.1097 · Cited by 173 · see citing works
Localization, Dynamics, and Protein Interactions Reveal Distinct Roles for ER and Golgi SNAREs
Hay, J., Klumperman, J., Oorschot, V. M. J., Steegmaier, M., Kuo, C. S., & Scheller, R. H. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.141.7.1489 · Cited by 157 · see citing works
Sec35p, a Novel Peripheral Membrane Protein, Is Required for ER to Golgi Vesicle Docking
VanRheenen, S. M., Cao, X., Lupashin, V. V., Barlowe, C. K., & Waters, M. G. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.141.5.1107 · Cited by 136 · see citing works
Calmodulin Regulates Endosome Fusion
Colombo, M. I., Berón, W., & Stahl, P. D. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.12.7707 · Cited by 135 · see citing works
Two distinct effectors of the small GTPase Rab5 cooperate in endocytic membrane fusion
Gournier, H., Stenmark, H., Rybin, V., Lippé, R., & Zerial, M. (1998) · The EMBO Journal · doi:10.1093/emboj/17.7.1930 · Cited by 97 · see citing works
Self-citationDocking and fusion in neurosecretion
Robinson, L. J., & Martin, T. F. J. (1998) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(98)80063-x · Cited by 88 · see citing works
Multiple N-ethylmaleimide-sensitive components are required for endosomal vesicle fusion.
Rodriguez, L., Stirling, C. J., & Woodman, P. G. (1994) · Molecular Biology of the Cell · doi:10.1091/mbc.5.7.773 · Cited by 85 · see citing works
A Possible Predocking Attachment Site for N-Ethylmaleimide-sensitive Fusion Protein
Colombo, M. I., Taddese, M., Whiteheart, S. W., & Stahl, P. D. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.31.18810 · Cited by 54 · see citing works
Wiedemann, C. G., & Cockcroft, S. (1998) · Nature · doi:10.1038/28752 · Cited by 54 · see citing works
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Stenmark, H. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2728 · Cited by 3,413 · see citing works
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Zerial, M., & McBride, H. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35052055 · Cited by 3,381 · see citing works
Self-citationTakai, Y., Sasaki, T., & Matozaki, T. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.1.153 · Cited by 2,481 · see citing works
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Bonifacino, J. S., & Glick, B. S. (2004) · Cell · doi:10.1016/s0092-8674(03)01079-1 · Cited by 1,863 · see citing works
Rab Conversion as a Mechanism of Progression from Early to Late Endosomes
Rink, J. C., Ghigo, É., Kalaidzidis, Y. L., & Zerial, M. (2005) · Cell · doi:10.1016/j.cell.2005.06.043 · Cited by 1,680 · see citing works
Self-citationRole of Rab GTPases in Membrane Traffic and Cell Physiology
Hutagalung, A. H., & Novick, P. (2011) · Physiological Reviews · doi:10.1152/physrev.00059.2009 · Cited by 1,514 · see citing works
Rab7: A Key to Lysosome Biogenesis
Bucci, C., Thomsen, P., Nicoziani, P., McCarthy, J., & van Deurs, B. (2000) · Molecular Biology of the Cell · doi:10.1091/mbc.11.2.467 · Cited by 1,084 · see citing works
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Flannagan, R. S., Jaumouillé, V., & Grinstein, S. (2011) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-011811-132445 · Cited by 1,016 · see citing works
Macrophage defense mechanisms against intracellular bacteria
Weiss, G., & Schaible, U. E. (2015) · Immunological Reviews · doi:10.1111/imr.12266 · Cited by 989 · see citing works
Sönnichsen, B., Renzis, S. D., Nielsen, E., Rietdorf, J., & Zerial, M. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.149.4.901 · Cited by 1,013 · see citing works
Self-citationBurgoyne, R. D., & Morgan, A. (2003) · Physiological Reviews · doi:10.1152/physrev.00031.2002 · Cited by 934 · see citing works
Self-citationHuman RAS Superfamily Proteins and Related GTPases
Colicelli, J. (2004) · Science s STKE · doi:10.1126/stke.2502004re13 · Cited by 837 · see citing works
Stenmark, H., & Olkkonen, V. M. (2001) · Genome biology · doi:10.1186/gb-2001-2-5-reviews3007 · Cited by 714 · see citing works
Mechanisms of membrane fusion: disparate players and common principles
Martens, S., & McMahon, H. (2008) · Nature reviews. Molecular cell biology · doi:10.1038/nrm2417 · Cited by 715 · see citing works
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Poteryaev, D., Datta, S., Ackema, K., Zerial, M., & Spang, A. (2010) · Cell · doi:10.1016/j.cell.2010.03.011 · Cited by 752 · see citing works
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Analysis of the Small GTPase Gene Superfamily of Arabidopsis
Vernoud, V., Horton, A. C., Yang, Z., & Nielsen, E. (2003) · PLANT PHYSIOLOGY · doi:10.1104/pp.013052 · Cited by 636 · see citing works
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Christoforidis, S., Miączyńska, M., Ashman, K., Wilm, M. S., Zhao, L., Yip, S.-C., Waterfield, M. D., Backer, J., & Zerial, M. (1999) · Nature Cell Biology · doi:10.1038/12075 · Cited by 633 · see citing works
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Wandinger-Ness, A., & Zerial, M. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a022616 · Cited by 586 · see citing works
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Lin, J., Ju, W. H., Foster, K. A., Lee, S. H., Ahmadian, G., Wyszynski, M. W., Wang, Y. T., & Sheng, M. (2000) · Nature Neuroscience · doi:10.1038/81814 · Cited by 557 · see citing works
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Rosales, C., & Uribe‐Querol, E. (2017) · BioMed Research International · doi:10.1155/2017/9042851 · Cited by 555 · see citing works
Rab‐interacting lysosomal protein (RILP): the Rab7 effector required for transport to lysosomes
Cantalupo, G., Alifano, P., Roberti, V., Bruni, C. B., & Bucci, C. (2001) · The EMBO Journal · doi:10.1093/emboj/20.4.683 · Cited by 542 · see citing works
Fratti, R. A., Backer, J., Gruenberg, J. E., Corvera, S., & Deretic, V. P. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200106049 · Cited by 535 · see citing works
APPL Proteins Link Rab5 to Nuclear Signal Transduction via an Endosomal Compartment
Miączyńska, M., Christoforidis, S., Giner, A., Shevchenko, A., Uttenweiler‐Joseph, S., Habermann, B. H., Wilm, M. S., Parton, R. G., & Zerial, M. (2004) · Cell · doi:10.1016/s0092-8674(04)00117-5 · Cited by 536 · see citing works
Self-citationMcBride, 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
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Balderhaar, H. J. K., & Ungermann, C. (2013) · Journal of Cell Science · doi:10.1242/jcs.107805 · Cited by 500 · see citing works
Rab5 regulates motility of early endosomes on microtubules
Nielsen, E., Severin, F. F., Backer, J., Hyman, A. A., & Zerial, M. (1999) · Nature Cell Biology · doi:10.1038/14075 · Cited by 510 · see citing works
Self-citationPhagosome maturation: going through the acid test
Kinchen, J. M., & Ravichandran, K. S. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2515 · Cited by 555 · see citing works
Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis
Belland, R. J., Zhong, G., Crane, D. D., Hogan, D. M., Sturdevant, D. E., Sharma, J., Beatty, W. L., & Caldwell, H. D. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1331135100 · Cited by 501 · see citing works
The role of ARF and Rab GTPases in membrane transport
Chavrier, P., & Goud, B. (1999) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(99)80067-2 · Cited by 496 · see citing works
Seals, D. F., Eitzen, G., Margolis, N., Wickner, W. T., & Price, A. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.17.9402 · Cited by 477 · see citing works
Rab family of small GTPases: an updated view on their regulation and functions
Homma, Y., Hiragi, S., & Fukuda, M. (2020) · FEBS Journal · doi:10.1111/febs.15453 · Cited by 468 · see citing works
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Allan, B. B., Moyer, B. D., & Balch, W. E. (2000) · Science · doi:10.1126/science.289.5478.444 · Cited by 458 · see citing works
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Rojas, R., van Vlijmen, T., Mardones, G. A., Prabhu, Y., Rojas, A. L., Mohammed, S., Heck, A. J. R., Raposo, G., van der Sluijs, P., & Bonifacino, J. S. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200804048 · Cited by 458 · see citing works
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Whyte, J. R. C., & Munro, S. (2002) · Journal of Cell Science · doi:10.1242/jcs.115.13.2627 · Cited by 457 · see citing works
G Protein–Coupled Receptor Sorting to Endosomes and Lysosomes
Marchese, A., Paing, M. M., Temple, B. R. S., & Trejo, J. (2007) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.48.113006.094646 · Cited by 456 · see citing works
Rab GTPases coordinate endocytosis
Rodman, J. S., & Wandinger‐Ness, A. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.2.183 · Cited by 450 · see citing works
Transport-vesicle targeting: tethers before SNAREs
Pfeffer, S. R. (1999) · Nature Cell Biology · doi:10.1038/8967 · Cited by 449 · see citing works
Wickner, W. T., & Schekman, R. W. (2008) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1451 · Cited by 447 · see citing works
CELL BIOLOGY OF MYCOBACTERIUM TUBERCULOSIS PHAGOSOME
Vergne, I., Chua, J., Singh, S., & Deretic, V. P. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.010403.114015 · Cited by 440 · see citing works
Vonderheit, A., & Helenius, A. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030233 · Cited by 437 · see citing works
Maturation of autophagosomes and endosomes: A key role for Rab7
Hyttinen, J. M. T., Niittykoski, M., Salminen, A., & Kaarniranta, K. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.11.018 · Cited by 424 · see citing works
Functions and mechanisms of retrograde neurotrophin signalling
Zweifel, L. S., Kuruvilla, R., & Ginty, D. D. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1727 · Cited by 413 · see citing works
Endocytic Traffic in Polarized Epithelial Cells: Role of the Actin and Microtubule Cytoskeleton
Apodaca, G. (2001) · Traffic · doi:10.1034/j.1600-0854.2001.020301.x · Cited by 408 · see citing works
Rab GTPase Function in Endosome and Lysosome Biogenesis
Langemeyer, L., Fröhlich, F., & Ungermann, C. (2018) · Trends in Cell Biology · doi:10.1016/j.tcb.2018.06.007 · Cited by 393 · see citing works
Multiple Roles of the Small GTPase Rab7
Guerra, F., & Bucci, C. (2016) · Cells · doi:10.3390/cells5030034 · Cited by 394 · see citing works
An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway
Shin, H., Hayashi, M., Christoforidis, S., Lacas‐Gervais, S., Hoepfner, S., Wenk, M. R., Modregger, J., Uttenweiler‐Joseph, S., Wilm, M. S., Nystuen, A., et al. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200505128 · Cited by 398 · see citing works
Self-citationNielsen, E., Christoforidis, S., Uttenweiler‐Joseph, S., Miączyńska, M., Dewitte, F., Wilm, M. S., Hoflack, B., & Zerial, M. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.3.601 · Cited by 383 · see citing works
Self-citationRab5 is necessary for the biogenesis of the endolysosomal system in vivo
Zeigerer, A., Gilleron, J., Bogorad, R. L., Marsico, G., Nonaka, H., Seifert, S., Epstein-Barash, H., Kuchimanchi, S., Peng, C. G., Ruda, V. M., et al. (2012) · Nature · doi:10.1038/nature11133 · Cited by 362 · see citing works
Self-citationVergne, I., Chua, J., & Deretic, V. P. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20030527 · Cited by 354 · see citing works
Berger, K. L., Cooper, J. D., Heaton, N. S., Yoon, R., Oakland, T. E., Jordan, T. X., Mateu, G., Grakoui, A., & Randall, G. C. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902693106 · Cited by 346 · see citing works
Intracellular routing of plasmid DNA during non-viral gene transfer.
Lechardeur, D., Verkman, A., & Lukács, G. (2005) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2004.12.008 · Cited by 339 · see citing works
Matteis, M. A. D., & Godi, A. (2004) · Nature Cell Biology · doi:10.1038/ncb0604-487 · Cited by 338 · see citing works
Sec1p Binds to SNARE Complexes and Concentrates at Sites of Secretion
Carr, C. M., Grote, E., Munson, M., Hughson, F. M., & Novick, P. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.146.2.333 · Cited by 329 · see citing works
Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes
Renzis, S. D., Sönnichsen, B., & Zerial, M. (2002) · Nature Cell Biology · doi:10.1038/ncb744 · Cited by 326 · see citing works
Self-citationBelenkaya, T. Y., Wu, Y., Tang, X., Zhou, B., Cheng, L., Sharma, Y. V., Yan, D., Selva, E. M., & Lin, X. (2007) · Developmental Cell · doi:10.1016/j.devcel.2007.12.003 · Cited by 323 · see citing works
Tethering Factors as Organizers of Intracellular Vesicular Traffic
Yu, I.-M., & Hughson, F. M. (2010) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.042308.113327 · Cited by 323 · see citing works
A post-docking role for active zone protein Rim
Koushika, S. P., Richmond, J. E., Hadwiger, G., Weimer, R. M., Jørgensen, E. M., & Nonet, M. L. (2001) · Nature Neuroscience · doi:10.1038/nn732 · Cited by 320 · see citing works
Focal Exocytosis of Vamp3-Containing Vesicles at Sites of Phagosome Formation
Bajno, L., Peng, X., Schreiber, A. D., Moore, H.-P. H., Trimble, W. S., & Grinstein, S. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.149.3.697 · Cited by 319 · see citing works
Gagescu, R., Demaurex, N., Parton, R. G., Hunziker, W., Huber, L. A., & Gruenberg, J. E. (2000) · Molecular Biology of the Cell · doi:10.1091/mbc.11.8.2775 · Cited by 316 · see citing works
The life cycle of phagosomes: formation, maturation, and resolution
Levin‐Konigsberg, R., Grinstein, S., & Canton, J. (2016) · Immunological Reviews · doi:10.1111/imr.12439 · Cited by 319 · see citing works
Almeida, C. G., Takahashi, R. H., & Gouras, G. K. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.5078-05.2006 · Cited by 316 · see citing works
Role of Phospholipids in Endocytosis, Phagocytosis, and Macropinocytosis
Bohdanowicz, M., & Grinstein, S. (2013) · Physiological Reviews · doi:10.1152/physrev.00002.2012 · Cited by 306 · see citing works
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Uribe‐Querol, E., & Rosales, C. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01368 · Cited by 310 · see citing works
How nascent phagosomes mature to become phagolysosomes
Fairn, G. D., & Grinstein, S. (2012) · Trends in Immunology · doi:10.1016/j.it.2012.03.003 · Cited by 303 · see citing works
Identification and Characterization of a Family of Rab11-interacting Proteins
Hales, C. M., Griner, R. D., Hobdy‐Henderson, K. C., Dorn, M. C., Hardy, D. M., Kumar, R., Navarre, J., Chan, E. K. L., Lapierre, L. A., & Goldenring, J. R. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104831200 · Cited by 297 · see citing works
Rab GTPases: master regulators that establish the secretory and endocytic pathways
Pfeffer, S. R. (2017) · Molecular Biology of the Cell · doi:10.1091/mbc.e16-10-0737 · Cited by 297 · see citing works
Phosphatidylinositol 3‐phosphates—at the interface between cell signalling and membrane traffic
Marat, A. L., & Haucke, V. (2016) · The EMBO Journal · doi:10.15252/embj.201593564 · Cited by 285 · see citing works
Ypt and Rab GTPases: insight into functions through novel interactions
Segev, N. (2001) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(00)00242-8 · Cited by 293 · see citing works
Conibear, E., & Stevens, T. H. (2000) · Molecular Biology of the Cell · doi:10.1091/mbc.11.1.305 · Cited by 290 · see citing works
The Stress-Induced MAP Kinase p38 Regulates Endocytic Trafficking via the GDI:Rab5 Complex
Cavalli, V., Vilbois, F., Felberbaum‐Corti, M., Marcote, M. J., Tamura, K., Karin, M., Arkinstall, S., & Gruenberg, J. E. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00189-7 · Cited by 288 · see citing works
Visualizing the site and dynamics of IgG salvage by the MHC class I-related receptor, FcRn
Ober, R. J., Martinez, C., Vaccaro, C., Zhou, J., & Ward, E. S. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.4.2021 · Cited by 314 · see citing works
Nanoescapology: progress toward understanding the endosomal escape of polymeric nanoparticles
FitzGerald, L. I., Cortez‐Jugo, C., Such, G. K., & Johnston, A. P. R. (2017) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1452 · Cited by 285 · see citing works
Toward a Comprehensive Map of the Effectors of Rab GTPases
Gillingham, A. K., Sinka, R., Torres, I. L., Lilley, K. S., & Munro, S. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.10.007 · Cited by 283 · see citing works
Rab proteins: The key regulators of intracellular vesicle transport
Bhuin, T., & Roy, J. K. (2014) · Experimental Cell Research · doi:10.1016/j.yexcr.2014.07.027 · Cited by 280 · see citing works
Vergne, I., Fratti, R. A., Hill, P. J., Chua, J., Belisle, J. T., & Deretic, V. P. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-05-0307 · Cited by 260 · see citing works
Misra, S., & Hurley, J. H. (1999) · Cell · doi:10.1016/s0092-8674(00)80776-x · Cited by 259 · see citing works
Whyte, J. R. C., & Munro, S. (2001) · Developmental Cell · doi:10.1016/s1534-5807(01)00063-6 · Cited by 253 · see citing works
Rab1 Interaction with a GM130 Effector Complex Regulates COPII Vesicle cis‐Golgi Tethering
Moyer, B. D., Allan, B. B., & Balch, W. E. (2001) · Traffic · doi:10.1034/j.1600-0854.2001.1o007.x · Cited by 251 · see citing works
Multivalent Endosome Targeting by Homodimeric EEA1
Dumas, J. J., Merithew, E., Sudharshan, E., Rajamani, D., Hayes, S., Lawe, D. C., Corvera, S., & Lambright, D. G. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00385-9 · Cited by 251 · see citing works
Otomo, A. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg184 · Cited by 250 · see citing works
Signal transduction during Fc receptor-mediated phagocytosis
García-García, E., & Rosales, C. (2002) · Journal of Leukocyte Biology · doi:10.1189/jlb.72.6.1092 · Cited by 249 · see citing works
The Rab5 Effector EEA1 Interacts Directly with Syntaxin-6
Simonsen, A., Gaullier, J., D’Arrigo, A., & Stenmark, H. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.41.28857 · Cited by 248 · see citing works
Pal, A., Severin, F. F., Lommer, B. S., Shevchenko, A., & Zerial, M. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200509091 · Cited by 244 · see citing works
Self-citationIntegrin endosomal signalling suppresses anoikis
Alanko, J., Mai, A., Jacquemet, G., Schauer, K., Kaukonen, R., Saari, M. A., Goud, B., & Ivaska, J. (2015) · Nature Cell Biology · doi:10.1038/ncb3250 · 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
Kim, D. H., Eu, Y.-J., Yoo, C. M., Kim, Y.-W., Pih, K. T., Jin, J. B., Kim, S. J., Stenmark, H., & Hwang, I. (2001) · The Plant Cell · doi:10.1105/tpc.13.2.287 · Cited by 241 · see citing works
Rab GTPases and membrane identity: Causal or inconsequential?
Barr, F. A. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201306010 · Cited by 240 · see citing works
Gandek, T. B., van der Koog, L., & Nagelkerke, A. (2023) · Advanced Healthcare Materials · doi:10.1002/adhm.202300319 · Cited by 242 · see citing works
Reconstitution of Rab- and SNARE-dependent membrane fusion by synthetic endosomes
Ohya, T., Miączyńska, M., Coskun, Ü., Lommer, B. S., Runge, A., Drechsel, D. N., Kalaidzidis, Y. L., & Zerial, M. (2009) · Nature · doi:10.1038/nature08107 · Cited by 235 · see citing works
Self-citationLawe, D. C., Patki, V., Heller-Harrison, R. A., Lambright, D. G., & Corvera, S. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.5.3699 · Cited by 233 · see citing works
Cellular functions of phosphatidylinositol 3-phosphate and FYVE domain proteins
Gillooly, D. J., Simonsen, A., & Stenmark, H. (2001) · Biochemical Journal · doi:10.1042/0264-6021:3550249 · Cited by 229 · see citing works
Multisubunit Tethering Complexes and Their Role in Membrane Fusion
Bröcker, C., Engelbrecht-Vandré, S., & Ungermann, C. (2010) · Current Biology · doi:10.1016/j.cub.2010.09.015 · Cited by 228 · see citing works
A GTPase-activating protein controls Rab5 function in endocytic trafficking
Haas, A. K., Fuchs, E., Kopajtich, R., & Barr, F. A. (2005) · Nature Cell Biology · doi:10.1038/ncb1290 · Cited by 228 · see citing works
Uptake of a Fluorescent Marker in Plant Cells Is Sensitive to Brefeldin A and Wortmannin
Emans, N., Zimmermann, S., & Fischer, R. (2002) · The Plant Cell · doi:10.1105/tpc.010339 · Cited by 227 · see citing works
When cell biology meets development: endocytic regulation of signaling pathwaysPreprint
Seto, E., Bellen, H. J., & Lloyd, T. E. (2002) · Genes & Development · doi:10.1101/gad.989602 · Cited by 224 · see citing works
RhoD regulates endosome dynamics through Diaphanous-related Formin and Src tyrosine kinase
Gasman, S., Kalaidzidis, Y. L., & Zerial, M. (2003) · Nature Cell Biology · doi:10.1038/ncb935 · Cited by 226 · see citing works
Self-citationBlumenthal, R., Clague, M. J., Durell, S. R., & Epand, R. M. (2002) · Chemical Reviews · doi:10.1021/cr000036+ · Cited by 226 · see citing works
The Rab5 Effector Rabankyrin-5 Regulates and Coordinates Different Endocytic Mechanisms
Schnatwinkel, C., Christoforidis, S., Lindsay, M. R., Uttenweiler‐Joseph, S., Wilm, M. S., Parton, R. G., & Zerial, M. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020261 · Cited by 225 · see citing works
Self-citationRab7: Role of its protein interaction cascades in endo-lysosomal traffic
Wang, T., Ming, Z., Xiaochun, W., & Hong, W. (2010) · Cellular Signalling · doi:10.1016/j.cellsig.2010.09.012 · Cited by 225 · see citing works
- Authors
- Christoforidis, S., McBride, H. M., Burgoyne, R. D., & Zerial, M.
- Affiliations
- European Molecular Biology Laboratory (DE)
- University of Liverpool (GB)
- Corresponding author
- Zerial, Marino
- Venue
- Nature
- Published
- 1999-02
- Volume
- 397
- Issue
- 6720
- Pages
- 621-625
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1595436183
- Cited by
- 854
- References
- 30
- Citations by year
- 2026: 7 · 2025: 14 · 2024: 32 · 2023: 23 · 2022: 21 · 2021: 39 · 2020: 25 · 2019: 32 · 2018: 26 · 2017: 25 · 2016: 26 · 2015: 20 · 2014: 27 · 2013: 36 · 2012: 27
- FWCI
- 21.53
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- 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 › Physiology › Calcium signaling and nucleotide metabolism
- Keywords
- EEA1, Rab5, membrane fusion, SNARE proteins, vesicle targeting, small GTPases, endosomal transport, lipid bilayer fusion
- MeSH terms
- Adenosine Triphosphate, Animals, Cattle, Chromatography, Affinity, Chromatography, Agarose, Cytosol, HeLa Cells, Humans, Intracellular Membranes, Membrane Fusion, Membrane Proteins, Protein Binding, Endosomes, Recombinant Fusion Proteins, GTP-Binding Proteins, rab5 GTP-Binding Proteins, Vesicular Transport Proteins, SNARE Proteins
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