Oligomeric Complexes Link Rab5 Effectors with NSF and Drive Membrane Fusion via Interactions between EEA1 and Syntaxin 13
Open accessAbstract
SNAREs and Rab GTPases cooperate in vesicle transport through a mechanism yet poorly understood. We now demonstrate that the Rab5 effectors EEA1 and Rabaptin-5/Rabex-5 exist on the membrane in high molecular weight oligomers, which also contain NSF. Oligomeric assembly is modulated by the ATPase activity of NSF. Syntaxin 13, the t-SNARE required for endosome fusion, is transiently incorporated into the large oligomers via direct interactions with EEA1. This interaction is required to drive fusion, since both dominant-negative EEA1 and synthetic peptides encoding the FYVE Zn2+ finger hinder the interaction and block fusion. We propose a novel mechanism whereby oligomeric EEA1 and NSF mediate the local activation of syntaxin 13 upon membrane tethering and, by analogy with viral fusion proteins, coordinate the assembly of a fusion pore.
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?
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 [22]
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
Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution
Sutton, R. B., Fasshauer, D., Jahn, R., & Brunger, A. T. (1998) · Nature · doi:10.1038/26412 · Cited by 2,417 · 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-citationThe Rab5 effector EEA1 is a core component of endosome docking
Christoforidis, S., McBride, H. M., Burgoyne, R. D., & Zerial, M. (1999) · Nature · doi:10.1038/17618 · Cited by 854 · see citing works
Self-citationHanson, P. I., Roth, R. A., Morisaki, H., Jahn, R., & Heuser, J. E. (1997) · Cell · doi:10.1016/s0092-8674(00)80512-7 · Cited by 797 · see citing works
The 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
The syntaxin family of vesicular transport receptors
Bennett, M. K., Garcia-Arrarás, J., Elferink, L. A., Peterson, K., Fleming, A. M., Hazuka, C. D., & Scheller, R. H. (1993) · Cell · doi:10.1016/0092-8674(93)90466-4 · Cited by 649 · see citing works
The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis
Guo, W., Roth, D., Walch-Solimena, C., & Novick, P. (1999) · The EMBO Journal · doi:10.1093/emboj/18.4.1071 · Cited by 627 · 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-citationGaullier, J.-M., Simonsen, A., D'Arrigo, A., Bremnes, B., Stenmark, H., & Aasland, R. (1998) · Nature · doi:10.1038/28767 · Cited by 553 · see citing works
NSF Binding to GluR2 Regulates Synaptic Transmission
Nishimune, A., Isaac, J. T. R., Molnár, E., Noël, J., Nash, S. R., Tagaya, M., Collingridge, G. L., Nakanishi, S., & Henley, J. M. (1998) · Neuron · doi:10.1016/s0896-6273(00)80517-6 · Cited by 544 · see citing works
The synaptic SNARE complex is a parallel four-stranded helical bundle
Poirier, M. A., Xiao, W., Macosko, J. C., Chan, C. K. F., Shin, Y., & Bennett, M. K. (1998) · Nature Structural Biology · doi:10.1038/1799 · Cited by 510 · 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
Phosphatidylinositol(3)-Phosphate Signaling Mediated by Specific Binding to RING FYVE Domains
Burd, C. G., & Emr, S. D. (1998) · Molecular Cell · doi:10.1016/s1097-2765(00)80125-2 · Cited by 499 · see citing works
Rabaptin-5 is a direct effector of the small GTPase Rab5 in endocytic membrane fusion
Stenmark, H., Vitale, G., Ullrich, O., & Zerial, M. (1995) · Cell · doi:10.1016/0092-8674(95)90120-5 · Cited by 474 · see citing works
Self-citationTransport-vesicle targeting: tethers before SNAREs
Pfeffer, S. R. (1999) · Nature Cell Biology · doi:10.1038/8967 · Cited by 449 · see citing works
Nakamura, N., Lowe, M., Levine, T. P., Rabouille, C., & Warren, G. (1997) · Cell · doi:10.1016/s0092-8674(00)80225-1 · Cited by 415 · see citing works
Protein-Protein Interactions Contributing to the Specificity of Intracellular Vesicular Trafficking
Calakos, N., Bennett, M. K., Peterson, K. E., & Scheller, R. H. (1994) · Science · doi:10.1126/science.8108733 · Cited by 399 · see citing works
Interaction of the N-Ethylmaleimide–Sensitive Factor with AMPA Receptors
Song, I., Kamboj, S. K., Xia, J., Dong, H., Liao, D., & Huganir, R. L. (1998) · Neuron · doi:10.1016/s0896-6273(00)80548-6 · Cited by 398 · see citing works
Ca2+/calmodulin signals the completion of docking and triggers a late step of vacuole fusion
Peters, C., & Mayer, A. (1998) · Nature · doi:10.1038/25133 · Cited by 386 · see citing works
Sec3p Is a Spatial Landmark for Polarized Secretion in Budding Yeast
Finger, F. P., Hughes, T. E., & Novick, P. (1998) · Cell · doi:10.1016/s0092-8674(00)80948-4 · Cited by 384 · 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
Osten, P., Srivastava, S., Inman, G. J., Vilim, F. S., Khatri, L., Lee, L. M., States, B. A., Einheber, S., Milner, T. A., Hanson, P. I., et al. (1998) · Neuron · doi:10.1016/s0896-6273(00)80518-8 · Cited by 358 · see citing works
Defining the functions of trans-SNARE pairs
Ungermann, C., Sato, K., & Wickner, W. T. (1998) · Nature · doi:10.1038/25069 · Cited by 336 · see citing works
Danieli, T., Pelletier, S. L., Henis, Y. I., & White, J. M. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.133.3.559 · Cited by 334 · see citing works
Rab GTPases, Directors of Vesicle Docking*
Schimmoller, F., Simon, I., & Pfeffer, S. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.35.22161 · Cited by 330 · see citing works
GTPase activity of Rab5 acts as a timer for endocytic membrane fusion
Rybin, V., Ullrich, O., Rubino, M., Alexandrov, K. A., Simón, I., Seabra, M. C., Goody, R. S., & Zerial, M. (1996) · Nature · doi:10.1038/383266a0 · Cited by 326 · see citing works
Self-citationSNARE Interactions Are Not Selective
Yang, B., Gonzalez, L. C., Prekeris, R., Steegmaier, M., Advani, R. J., & Scheller, R. H. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.9.5649 · Cited by 315 · see citing works
SNAREs and NSF in targeted membrane fusion
Hay, J., & Scheller, R. H. (1997) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(97)80026-9 · Cited by 297 · see citing works
Fujita, Y., Shirataki, H., Sakisaka, T., Asakura, T., Ohya, T., Kotani, H., Yokoyama, S., Nishioka, H., Matsuura, Y., Mizoguchi, A., et al. (1998) · Neuron · doi:10.1016/s0896-6273(00)80472-9 · Cited by 291 · see citing works
Syntaxin 6 functions in trans-Golgi network vesicle trafficking.
Bock, J. B., Klumperman, J., Davanger, S., & Scheller, R. H. (1997) · Molecular Biology of the Cell · doi:10.1091/mbc.8.7.1261 · Cited by 288 · see citing works
A functional PtdIns(3)P-binding motif
Patki, V., Lawe, D. C., Corvera, S., Virbasius, J. V., & Chawla, A. (1998) · Nature · doi:10.1038/28771 · Cited by 287 · see citing works
Klumperman, J., Kuliawat, R., Griffith, J. M., Geuze, H. J., & Arvan, P. R. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.141.2.359 · Cited by 287 · see citing works
Syntaxin 13 Mediates Cycling of Plasma Membrane Proteins via Tubulovesicular Recycling Endosomes
Prekeris, R., Klumperman, J., Chen, Y. A., & Scheller, R. H. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.143.4.957 · Cited by 286 · see citing works
Seven Novel Mammalian SNARE Proteins Localize to Distinct Membrane Compartments
Advani, R. J., Bae, H.-R., Bock, J. B., Chao, D. S., Doung, Y.-C., Prekeris, R., Yoo, J.-S., & Scheller, R. H. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.17.10317 · Cited by 263 · 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
Intermediates in influenza induced membrane fusion.
Stegmann, T., White, J. M., & Helenius, A. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb07871.x · Cited by 247 · 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
Involvement of the endosomal autoantigen EEA1 in homotypic fusion of early endosomes
Mills, I. G., Jones, A. T., & Clague, M. J. (1998) · Current Biology · doi:10.1016/s0960-9822(07)00351-x · Cited by 224 · see citing works
Endosome dynamics regulated by a Rho protein
Murphy, C., Saffrich, R., Grummt, M., Gournier, H., Rybin, V., Rubino, M., Auvinen, P., Lütcke, A., Parton, R. G., & Zerial, M. (1996) · Nature · doi:10.1038/384427a0 · Cited by 224 · see citing works
Self-citationvon 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
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
Peterson, M. R., Burd, C. G., & Emr, S. D. (1999) · Current Biology · doi:10.1016/s0960-9822(99)80071-2 · Cited by 177 · 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
A novel Sec18p/NSF-dependent complex required for Golgi-to-endosome transport in yeast.
Burd, C. G., Peterson, M. R., Cowles, C. R., & Emr, S. D. (1997) · Molecular Biology of the Cell · doi:10.1091/mbc.8.6.1089 · Cited by 151 · see citing works
Regulation of Membrane Trafficking
Gonzalez, L. C., & Scheller, R. H. (1999) · Cell · doi:10.1016/s0092-8674(00)80585-1 · Cited by 150 · see citing works
Coorssen, J. R., Blank, P. S., Tahara, M., & Zimmerberg, J. J. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.143.7.1845 · Cited by 138 · see citing works
Quaternary structure of influenza virus hemagglutinin after acid treatment
Doms, R. W., & Helenius, A. (1986) · Journal of Virology · doi:10.1128/jvi.60.3.833-839.1986 · Cited by 138 · see citing works
The endosome fusion regulator early-endosomal autoantigen 1 (EEA1) is a dimer
Callaghan, J. M., Simonsen, A., Gaullier, J., Toh, B., & Stenmark, H. (1999) · Biochemical Journal · doi:10.1042/0264-6021:3380539 · Cited by 137 · 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
Arrangement of Subunits in 20 S Particles Consisting of NSF, SNAPs, and SNARE Complexes
Hohl, T. M., Parlati, F., Wimmer, C., Rothman, J. E., Söllner, T. H., & Engelhardt, H. (1998) · Molecular Cell · doi:10.1016/s1097-2765(00)80153-7 · Cited by 130 · see citing works
Markovic, I., Pulyaeva, H., Sokoloff, A., & Chernomordik, L. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.143.5.1155 · Cited by 101 · 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-citationAn architecture for the fusion site of Influenza hemagglutinin
Bentz, J., Ellens, H. M., & Alford, D. R. (1990) · FEBS Letters · doi:10.1016/0014-5793(90)80492-2 · Cited by 93 · see citing works
Syntaxin 12, a Member of the Syntaxin Family Localized to the Endosome
Tang, B. L., Tan, A. E. H., Lim, L. K., Lee, S. S., Low, D. Y. H., & Hong, W. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.12.6944 · Cited by 91 · see citing works
Syntaxin 7, a Novel Syntaxin Member Associated with the Early Endosomal Compartment
Wong, S. H., Xu, Y., Zhang, T., & Hong, W. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.1.375 · Cited by 85 · see citing works
Xu, Z., Sato, K., & Wickner, W. T. (1998) · Cell · doi:10.1016/s0092-8674(00)81457-9 · Cited by 85 · see citing works
SNARE Membrane Trafficking Dynamics In Vivo
Chao, D. S., Hay, J., Winnick, S., Prekeris, R., Klumperman, J., & Scheller, R. H. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.144.5.869 · Cited by 67 · see citing works
NSF and AMPA Receptors Get Physical
Lin, J., & Sheng, M. (1998) · Neuron · doi:10.1016/s0896-6273(00)80534-6 · Cited by 58 · see citing works
Better Late Than Never: A Role for Rabs Late in Exocytosis
Bean, A. J., & Scheller, R. H. (1997) · Neuron · doi:10.1016/s0896-6273(00)80957-5 · Cited by 41 · see citing works
Flagged first, then by citations
1 of the 65 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Rab GTPases as coordinators of vesicle traffic
Stenmark, H. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2728 · Cited by 3,413 · see citing works
Rab proteins as membrane organizers
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 2,466 · see citing works
Maxfield, F. R., & McGraw, T. E. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1315 · Cited by 1,716 · 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-citationLocalization of phosphatidylinositol 3‐phosphate in yeast and mammalian cells
Gillooly, D. J., Morrow, I. C., Lindsay, M. R., Gould, R., Bryant, N. J., Gaullier, J., Parton, R. G., & Stenmark, H. (2000) · The EMBO Journal · doi:10.1093/emboj/19.17.4577 · Cited by 1,125 · see citing works
The Cell Biology of Phagocytosis
Flannagan, R. S., Jaumouillé, V., & Grinstein, S. (2011) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-011811-132445 · Cited by 1,018 · 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-citationRabs and their effectors: achieving specificity in membrane traffic
Grosshans, B. L., Ortiz, D., & Novick, P. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601617103 · Cited by 1,005 · see citing works
Antimicrobial mechanisms of phagocytes and bacterial evasion strategies
Flannagan, R. S., Cosío, G., & Grinstein, S. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2128 · Cited by 947 · 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
The endocytic pathway: a mosaic of domains
Gruenberg, J. E. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35096054 · Cited by 703 · see citing works
Transcytosis: Crossing Cellular Barriers
TUMA, P. L., & HUBBARD, A. L. (2003) · Physiological Reviews · doi:10.1152/physrev.00001.2003 · Cited by 681 · see citing works
Phagosome maturation: aging gracefully
Vieira, O. V., Botelho, R. J., & Grinstein, S. (2002) · Biochemical Journal · doi:10.1042/bj20020691 · Cited by 675 · see citing works
The regulation and function of Class III PI3Ks: novel roles for Vps34
Backer, J. (2008) · Biochemical Journal · doi:10.1042/bj20071427 · Cited by 659 · see citing works
Hong, W. (2005) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2005.03.014 · Cited by 629 · see citing works
Rab Proteins and the Compartmentalization of the Endosomal System
Wandinger-Ness, A., & Zerial, M. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a022616 · Cited by 586 · see citing works
Self-citationDistinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization
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 554 · see citing works
Phagocytosis: A Fundamental Process in Immunity
Rosales, C., & Uribe‐Querol, E. (2017) · BioMed Research International · doi:10.1155/2017/9042851 · Cited by 562 · 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
Pelkmans, L., Bürli, T., Zerial, M., & Helenius, A. (2004) · Cell · doi:10.1016/j.cell.2004.09.003 · Cited by 537 · see citing works
Self-citationVieira, O. V., Botelho, R. J., Rameh, L. E., Brachmann, S. M., Matsuo, T., Davidson, H. W., Schreiber, A. D., Backer, J., Cantley, L. C., & Grinstein, S. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200107069 · Cited by 530 · see citing works
Mechanisms of Synaptic Vesicle Exocytosis
Lin, R. C.-S., & Scheller, R. H. (2000) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.16.1.19 · Cited by 512 · see citing works
Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest
Fratti, R. A., Chua, J., Vergne, I., & Deretic, V. P. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0737613100 · Cited by 509 · 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
Rab1 Recruitment of p115 into a cis-SNARE Complex: Programming Budding COPII Vesicles for Fusion
Allan, B. B., Moyer, B. D., & Balch, W. E. (2000) · Science · doi:10.1126/science.289.5478.444 · Cited by 458 · see citing works
The melanosome: membrane dynamics in black and white
Marks, M. S., & Seabra, M. C. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35096009 · Cited by 452 · 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
Nitric Oxide Regulates Exocytosis by S-Nitrosylation of N-ethylmaleimide-Sensitive Factor
Matsushita, K., Morrell, C. N., Cambien, B., Yang, S.-X., Yamakuchi, M., Bao, C., Hara, M. R., Quick, R. A., Cao, W., O'Rourke, B. P., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00803-1 · Cited by 446 · 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
Regulation of membrane traffic by phosphoinositide 3-kinases
Lindmo, K., & Stenmark, H. (2006) · Journal of Cell Science · doi:10.1242/jcs.02855 · Cited by 425 · see citing works
Wurmser, A. E., Sato, T. K., & Emr, S. D. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.3.551 · Cited by 425 · 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
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-citationHrs recruits clathrin to early endosomes
Raiborg, C., Bache, K. G., Mehlum, A., Stang, E., & Stenmark, H. (2001) · The EMBO Journal · doi:10.1093/emboj/20.17.5008 · Cited by 389 · see citing works
Nielsen, 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-citationThe early endosome: a busy sorting station for proteins at the crossroads.
Jović, M., Sharma, M., Rahajeng, J., & Caplan, S. (2010) · PubMed · doi:10.14670/hh-25.99 · Cited by 377 · see citing works
Bruewer, M., Utech, M., Ivanov, A. I., Hopkins, A. M., Parkos, C. A., & Nusrat, A. (2005) · The FASEB Journal · doi:10.1096/fj.04-3260com · Cited by 364 · see citing works
A comprehensive map of the toll‐like receptor signaling network
Oda, K., & Kitano, H. (2006) · Molecular Systems Biology · doi:10.1038/msb4100057 · Cited by 354 · see citing works
The enigmatic endosome – sorting the ins and outs of endocytic trafficking
Naslavsky, N., & Caplan, S. (2018) · Journal of Cell Science · doi:10.1242/jcs.216499 · Cited by 338 · see citing works
Modulation of Rab5 and Rab7 Recruitment to Phagosomes by Phosphatidylinositol 3-Kinase
Vieira, O. V., Bucci, C., Harrison, R. E., Trimble, W. S., Lanzetti, L., Gruenberg, J. E., Schreiber, A. D., Stahl, P. D., & Grinstein, S. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.7.2501-2514.2003 · Cited by 347 · see citing works
Targeting of Host Rab GTPase Function by the Intravacuolar Pathogen Legionella pneumophila
Machner, M. P., & Isberg, R. R. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.05.013 · Cited by 340 · see citing works
Rab27a Regulates the Peripheral Distribution of Melanosomes in Melanocytes
Hume, A. N., Collinson, L., Rapak, A., Gomes, A. Q., Hopkins, C. R., & Seabra, M. C. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.152.4.795 · Cited by 333 · 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-citationThe 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 307 · 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
SNARE Protein Structure and Function
Ungár, D., & Hughson, F. M. (2003) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.19.110701.155609 · Cited by 311 · see citing works
Flotillin-1-enriched Lipid Raft Domains Accumulate on Maturing Phagosomes
Dermine, J.-F., Duclos, S., Garin, J., St-Louis, F., Rea, S. L., Parton, R. G., & Desjardins, M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m101113200 · Cited by 305 · 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
Phosphoinositides in Constitutive Membrane Traffic
Roth, M. G. (2004) · Physiological Reviews · doi:10.1152/physrev.00033.2003 · Cited by 297 · 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
Lysosome-endosome fusion and lysosome biogenesis
Luzio, J. P., Rous, B., Bright, N. A., Pryor, P. R., Mullock, B. M., & Piper, R. C. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.9.1515 · Cited by 292 · see citing works
Antonin, W., Holroyd, C., Fasshauer, D., Pabst, S., von Mollard, G. F., & Jahn, R. (2000) · The EMBO Journal · doi:10.1093/emboj/19.23.6453 · 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
Marshall, J. G., Booth, J. W., Stambolic, V., Mak, T. W., Balla, T., Schreiber, A. D., Meyer, T., & Grinstein, S. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.153.7.1369 · Cited by 281 · 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
Naslavsky, N., Weigert, R., & Donaldson, J. G. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.02-04-0053 · Cited by 278 · see citing works
Sato, T. K., Rehling, P., Peterson, M. R., & Emr, S. D. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)00064-2 · Cited by 278 · 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
The intracellular redox state is a core determinant of mitochondrial fusion
Shutt, T. E., Geoffrion, M., Milne, R. W., & McBride, H. M. (2012) · EMBO Reports · doi:10.1038/embor.2012.128 · Cited by 243 · see citing works
Self-citationKim, 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
Epidermal Growth Factor and Membrane Trafficking
Barbieri, M. A., Roberts, R. L., Gumusboga, A., Highfield, H. A., Alvarez-Domı́nguez, C., Wells, A. H., & Stahl, P. D. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.3.539 · Cited by 240 · 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
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-citationER-mediated phagocytosis: a new membrane for new functions
Desjardins, M. (2003) · Nature reviews. Immunology · doi:10.1038/nri1053 · Cited by 230 · 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
The Rab27a/Granuphilin Complex Regulates the Exocytosis of Insulin-Containing Dense-Core Granules
Yi, Z., Yokota, H., Torii, S., Aoki, T., Hosaka, M., Zhao, S., Takata, K., Takeuchi, T., & Izumi, T. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.6.1858-1867.2002 · 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
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-citationMunc13-4 Is a GTP-Rab27-binding Protein Regulating Dense Core Granule Secretion in Platelets
Shirakawa, R., Higashi, T., Tabuchi, A., Yoshioka, A., Nishioka, H., Fukuda, M., Kita, T., & Horiuchi, H. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m309426200 · Cited by 220 · see citing works
Protein complexes in transport vesicle targeting
Guo, W., Sacher, M. G., Barrowman, J., Ferro‐Novick, S., & Novick, P. (2000) · Trends in Cell Biology · doi:10.1016/s0962-8924(00)01754-2 · Cited by 219 · see citing works
Omori, Y., Zhao, C., Saras, A., Mukhopadhyay, S., Kim, W., Furukawa, T., Sengupta, P., Veraksa, A. N., & Malicki, J. J. (2008) · Nature Cell Biology · doi:10.1038/ncb1706 · Cited by 218 · see citing works
Fratti, R. A., Jun, Y., Merz, A. J., Margolis, N., & Wickner, W. T. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200409068 · Cited by 217 · see citing works
Paumet, F., Mao, J. L., Martin, S., Galli, T., David, B., Blank, U., & Roa, M. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.11.5850 · Cited by 217 · see citing works
Lippé, R., Miączyńska, M., Rybin, V., Runge, A., & Zerial, M. (2001) · Molecular Biology of the Cell · doi:10.1091/mbc.12.7.2219 · Cited by 216 · see citing works
Self-citationStructural basis for ubiquitin recognition and autoubiquitination by Rabex-5
Lee, S., Tsai, Y. C., Mattera, R., Smith, W. J., Kostelansky, M. S., Weissman, A. M., Bonifacino, J. S., & Hurley, J. H. (2006) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1064 · Cited by 215 · see citing works
Role of Rab5 in the Recruitment of hVps34/p150 to the Early Endosome
Murray, J. T., Panaretou, C., Stenmark, H., Miączyńska, M., & Backer, J. (2002) · Traffic · doi:10.1034/j.1600-0854.2002.30605.x · Cited by 212 · see citing works
Direct Interaction of the Rab3 Effector RIM with Ca2+Channels, SNAP-25, and Synaptotagmin
Coppola, T., Magnin, S., Perret-Menoud, V., Gattesco, S., Schiavo, G., & Regazzi, R. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m100929200 · Cited by 211 · see citing works
Sorting in the endosomal system in yeast and animal cells
Lemmon, S. K., & Traub, L. M. (2000) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(00)00117-4 · Cited by 210 · see citing works
Membrane traffic in the secretory pathway
Malsam, J., Kreye, S., & Söllner, T. H. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8352-3 · Cited by 208 · see citing works
Long coiled-coil proteins and membrane traffic
Gillingham, A. K., & Munro, S. (2003) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/s0167-4889(03)00088-0 · Cited by 208 · see citing works
Price, A., Seals, D. F., Wickner, W. T., & Ungermann, C. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.148.6.1231 · Cited by 206 · see citing works
Hattula, K., Furuhjelm, J., Arffman, A., & Peränen, J. (2002) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-03-0143 · Cited by 205 · see citing works
Shorter, J., Beard, M., Seemann, J., Dirac-Svejstrup, A. B., & Warren, G. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200112127 · Cited by 203 · see citing works
Siniossoglou, S., & Pelham, H. R. B. (2001) · The EMBO Journal · doi:10.1093/emboj/20.21.5991 · Cited by 202 · see citing works
Yoo, J.-S., Moyer, B. D., Bannykh, S. I., Yoo, H.-M., Riordan, J. R., & Balch, W. E. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m110263200 · Cited by 200 · see citing works
FYVE-finger proteins – effectors of an inositol lipid
Stenmark, H., & Aasland, R. (1999) · Journal of Cell Science · doi:10.1242/jcs.112.23.4175 · Cited by 198 · see citing works
The phosphatidylinositol 3‐phosphate‐binding FYVE finger
Stenmark, H., Aasland, R., & Driscoll, P. C. (2002) · FEBS Letters · doi:10.1016/s0014-5793(01)03308-7 · Cited by 224 · see citing works
RIN3: a novel Rab5 GEF interacting with amphiphysin II involved in the early endocytic pathway
Kajiho, H., Saito, K., Tsujita, K., Kontani, K., Araki, Y., Kurosu, H., & Katada, T. (2003) · Journal of Cell Science · doi:10.1242/jcs.00718 · Cited by 191 · see citing works
Regulation of endocytic recycling by C. elegans Rab35 and its regulator RME‐4, a coated‐pit protein
Sato, M., Sato, K., Liou, W., Pant, S., Harada, A., & Grant, B. D. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.54 · Cited by 185 · see citing works
Sorting of Golgi resident proteins into different subpopulations of COPI vesicles
Lanoix, J., Ouwendijk, J., Stark, A., Szafer‐Glusman, E., Cassel, D., Dejgaard, K., Weiß, M., & Nilsson, T. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200108017 · Cited by 183 · see citing works
Delprato, A., Merithew, E., & Lambright, D. G. (2004) · Cell · doi:10.1016/j.cell.2004.08.009 · Cited by 182 · see citing works
McDermott, R., Ziylan, U., Spehner, D., Bausinger, H., Lipsker, D. M., Mommaas, M., Cazenave, J., Raposo, G., Goud, B., de la Salle, H., et al. (2002) · Molecular Biology of the Cell · doi:10.1091/mbc.01-06-0300 · Cited by 182 · see citing works
Puchner, E. M., Walter, J. M., Kasper, R. T., Huang, B., & Lim, W. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1309676110 · Cited by 172 · see citing works
Duclos, S., Diez, R., Garin, J., Papadopoulou, B., Descoteaux, A., Stenmark, H., & Desjardins, M. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.19.3531 · Cited by 175 · see citing works
- Authors
- McBride, H. M., Rybin, V., Murphy, C., Giner, A., Teasdale, R., & Zerial, M.
- Affiliations
- European Molecular Biology Laboratory (DE)
- University of Ioannina (GR)
- Corresponding author
- Zerial, Marino
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 1999-08
- Volume
- 98
- Issue
- 3
- Pages
- 377-386
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2126162952
- Cited by
- 520
- References
- 65
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 8 · 2023: 6 · 2022: 3 · 2021: 17 · 2020: 17 · 2019: 10 · 2018: 7 · 2017: 11 · 2016: 12 · 2015: 8 · 2014: 14 · 2013: 21 · 2012: 23
- FWCI
- 18.39
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- University of Birmingham Research Portal (University of Birmingham) (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, Rabaptin-5, NSF, t-SNARE, membrane fusion, endosome fusion, oligomeric complexes, snares, Rab GTPases, vesicle trafficking, ATPase activity
- MeSH terms
- Adenosine Triphosphatases, Amino Acid Sequence, Autoantigens, Carrier Proteins, HeLa Cells, Humans, Intracellular Membranes, Membrane Fusion, Membrane Proteins, Models, Biological, Molecular Sequence Data, Oligopeptides, Peptide Fragments, Endosomes, Biosensing Techniques, Zinc Fingers, GTP-Binding Proteins, GTP Phosphohydrolases, rab5 GTP-Binding Proteins, Vesicular Transport Proteins, SNARE Proteins, Qa-SNARE Proteins, N-Ethylmaleimide-Sensitive 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