ALIX- and ESCRT-III–dependent sorting of tetraspanins to exosomes
Open accessAbstract
The intraluminal vesicles (ILVs) of endosomes mediate the delivery of activated signaling receptors and other proteins to lysosomes for degradation, but they also modulate intercellular communication when secreted as exosomes. The formation of ILVs requires four complexes, ESCRT-0, -I, -II, and -III, with ESCRT-0, -I, and -II presumably involved in cargo sorting and ESCRT-III in membrane deformation and fission. Here, we report that an active form of the ESCRT-associated protein ALIX efficiently recruits ESCRT-III proteins to endosomes. This recruitment occurs independently of other ESCRTs but requires lysobisphosphatidic acid (LBPA) in vivo, and can be reconstituted on supported bilayers in vitro. Our data indicate that this ALIX- and ESCRT-III–dependent pathway promotes the sorting and delivery of tetraspanins to exosomes. We conclude that ALIX provides an additional pathway of ILV formation, secondary to the canonical pathway, and that this pathway controls the targeting of exosomal proteins.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Vps4 and ALIX participate in cargo sorting and exosome formation.
“In addition, Vps4 and ALIX also participate in cargo sorting and exosome formation [15,16].”
From The Therapeutic Potential and Clinical Significance of Exosomes as Carriers of Drug Delivery System (2022) · cites this paper as [16]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Shedding light on the cell biology of extracellular vesicles
van Niel, G., D'Angelo, G., & Raposo, G. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.125 · Cited by 8,369 · see citing works
Isolation and Characterization of Exosomes from Cell Culture Supernatants and Biological Fluids
Théry, C., Amigorena, S., Raposo, G., & Clayton, A. (2006) · Current Protocols in Cell Biology · doi:10.1002/0471143030.cb0322s30 · Cited by 5,766 · see citing works
Membrane vesicles as conveyors of immune responses
Théry, C., Ostrowski, M., & Segura, É. (2009) · Nature reviews. Immunology · doi:10.1038/nri2567 · Cited by 3,869 · see citing works
Ceramide Triggers Budding of Exosome Vesicles into Multivesicular Endosomes
Trajković, K., Hsu, C., Chiantia, S., Rajendran, L., Wenzel, D., Wieland, F., Schwille, P., Brügger, B., & Simons, M. (2008) · Science · doi:10.1126/science.1153124 · Cited by 3,639 · see citing works
Communication by Extracellular Vesicles: Where We Are and Where We Need to Go
Tkach, M., & Théry, C. (2016) · Cell · doi:10.1016/j.cell.2016.01.043 · Cited by 3,444 · see citing works
Exosomes – vesicular carriers for intercellular communication
Simons, M., & Raposo, G. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.03.007 · Cited by 2,351 · see citing works
Syndecan–syntenin–ALIX regulates the biogenesis of exosomes
Baietti, M. F., Zhang, Z., Mortier, E., Melchior, A., Degeest, G., Geeraerts, A., Ivarsson, Y., Depoortere, F., Coomans, C., Vermeiren, E., et al. (2012) · Nature Cell Biology · doi:10.1038/ncb2502 · Cited by 1,899 · see citing works
Biogenesis and secretion of exosomes
Kowal, J., Tkach, M., & Théry, C. (2014) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2014.05.004 · Cited by 1,781 · see citing works
Colombo, M., Moita, C. F., van Niel, G., Kowal, J., Vigneron, J., Benaroch, P., Manel, N., Moita, L. F., Théry, C., & Raposo, G. (2013) · Journal of Cell Science · doi:10.1242/jcs.128868 · Cited by 1,472 · see citing works
Katzmann, D. J., Babst, M., & Emr, S. D. (2001) · Cell · doi:10.1016/s0092-8674(01)00434-2 · Cited by 1,430 · see citing works
The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins
Raiborg, C., & Stenmark, H. (2009) · Nature · doi:10.1038/nature07961 · Cited by 1,408 · see citing works
Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding
Garrus, J. E., von Schwedler, U. K., Pornillos, O. W., Morham, S. G., Zavitz, K. H., Wang, H. E., Wettstein, D. A., Stray, K. M., Côté, M., Rich, R. L., et al. (2001) · Cell · doi:10.1016/s0092-8674(01)00506-2 · Cited by 1,369 · see citing works
Vesiclepedia: A Compendium for Extracellular Vesicles with Continuous Community Annotation
Kalra, H., Simpson, R. J., Ji, H., Aikawa, E., Altevogt, P., Askenase, P., Bond, V. C., Borràs, F. E., Breakefield, X., Budnik, V., et al. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001450 · Cited by 1,367 · see citing works
Nuclear envelope rupture and repair during cancer cell migration
Denais, C. M., Gilbert, R. M., Isermann, P., McGregor, A. L., te Lindert, M., Weigelin, B., Davidson, P. M., Friedl, P., Wolf, K., & Lammerding, J. (2016) · Science · doi:10.1126/science.aad7297 · Cited by 1,318 · see citing works
Kamentsky, L. D., Jones, T. R., Fraser, A. N., Bray, M., Logan, D. J., Madden, K. L., Ljosa, V., Rueden, C., Eliceiri, K. W., & Carpenter, A. E. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr095 · Cited by 1,002 · see citing works
van Niel, G., Charrin, S., Simoes, S., Romao, M., Rochin, L., Säftig, P., Marks, M. S., Rubinstein, E., & Raposo, G. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.08.019 · Cited by 955 · see citing works
ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death
Raab, M., Gentili, M., Belly, H. D., Thiam, H. R., Vargas, P., Jiménez, A. J., Lautenschläger, F., Voituriez, R., Lennon‐Duménil, A., Manel, N., et al. (2016) · Science · doi:10.1126/science.aad7611 · Cited by 946 · see citing works
Babst, M., Katzmann, D. J., Estepa, E. J., Meerloo, T., & Emr, S. D. (2002) · Developmental Cell · doi:10.1016/s1534-5807(02)00220-4 · Cited by 875 · see citing works
Breaking the chains: deubiquitylating enzyme specificity begets function
Clague, M. J., Urbé, S., & Komander, D. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0099-1 · Cited by 839 · see citing works
AIP1/ALIX Is a Binding Partner for HIV-1 p6 and EIAV p9 Functioning in Virus Budding
Strack, B., Calistri, A., Craig, S., Popova, E., & Göttlinger, H. G. (2003) · Cell · doi:10.1016/s0092-8674(03)00653-6 · Cited by 825 · see citing works
A lipid associated with the antiphospholipid syndrome regulates endosome structure and function
Kobayashi, T., Stang, E., Fang, K. S., de Moerloose, P., Parton, R. G., & Gruenberg, J. (1998) · Nature · doi:10.1038/32440 · Cited by 787 · see citing works
Self-citationUbiquitination of a Yeast Plasma Membrane Receptor Signals Its Ligand-Stimulated Endocytosis
Hicke, L., & Riezman, H. (1996) · Cell · doi:10.1016/s0092-8674(00)80982-4 · Cited by 783 · see citing works
Parallels Between Cytokinesis and Retroviral Budding: A Role for the ESCRT Machinery
Carlton, J. G., & Martin-Serrano, J. (2007) · Science · doi:10.1126/science.1143422 · Cited by 764 · see citing works
The emerging shape of the ESCRT machinery
Williams, R. L., & Urbé, S. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2162 · Cited by 747 · see citing works
Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis
Morita, E., Sandrin, V., Chung, H., Morham, S. G., Gygi, S. P., Rodesch, C. K., & Sundquist, W. I. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601850 · Cited by 724 · see citing works
Martin-Serrano, J., Zang, T., & Bieniasz, P. D. (2001) · Nature Medicine · doi:10.1038/nm1201-1313 · Cited by 710 · see citing works
Role of LBPA and Alix in Multivesicular Liposome Formation and Endosome Organization
Matsuo, H., Chevallier, J., Mayran, N., Le Blanc, I., Ferguson, C., Fauré, J., Blanc, N. S., Matile, S., Dubochet, J., Sadoul, R., et al. (2004) · Science · doi:10.1126/science.1092425 · Cited by 705 · see citing works
Self-citationESCRT Machinery Is Required for Plasma Membrane Repair
Jiménez, A. J., Maiuri, P., Lafaurie-Janvore, J., Divoux, S., Piel, M., & Perez, F. (2014) · Science · doi:10.1126/science.1247136 · Cited by 670 · see citing works
Babst, M., Katzmann, D. J., Snyder, W. B., Wendland, B., & Emr, S. D. (2002) · Developmental Cell · doi:10.1016/s1534-5807(02)00219-8 · Cited by 662 · see citing works
Peters, P. J., Neefjes, J., Oorschot, V. M. J., Ploegh, H. L., & Geuze, H. J. (1991) · Nature · doi:10.1038/349669a0 · Cited by 658 · see citing works
Membrane scission by the ESCRT-III complex
Wollert, T., Wunder, C., Lippincott‐Schwartz, J., & Hurley, J. H. (2009) · Nature · doi:10.1038/nature07836 · Cited by 634 · see citing works
Filimonenko, M., Stuffers, S., Raiborg, C., Yamamoto, A., Malerød, L., Fisher, E. M. C., Isaacs, A., Brech, A., Stenmark, H., & Simonsen, A. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200702115 · Cited by 626 · see citing works
BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals
Poser, I., Sarov, M., Hutchins, J. R. A., Hèriché, J.-K., Toyoda, Y., Pozniakovsky, A., Weigl, D., Nitzsche, A., Hegemann, B., Bird, A. W., et al. (2008) · Nature Methods · doi:10.1038/nmeth.1199 · Cited by 597 · see citing works
Endosome maturation, transport and functions
Scott, C. C., Vacca, F., & Gruenberg, J. E. (2014) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2014.03.034 · Cited by 581 · see citing works
Self-citationRab‐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
Triggered recruitment of ESCRT machinery promotes endolysosomal repair
Skowyra, M. L., Schlesinger, P. H., Naismith, T. V., & Hanson, P. I. (2018) · Science · doi:10.1126/science.aar5078 · Cited by 537 · see citing works
Pérez-Hernández, D., Gutiérrez‐Vázquez, C., Jorge, I., López‐Martín, S., Ursa, Á., Sánchez‐Madrid, F., Vázquez, J., & Yáñez‐Mó, M. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.445304 · Cited by 534 · see citing works
CD81 (TAPA-1): A MOLECULE INVOLVED IN SIGNAL TRANSDUCTION AND CELL ADHESION IN THE IMMUNE SYSTEM
Levy, S., Todd, S. C., & Maecker, H. T. (1998) · Annual Review of Immunology · doi:10.1146/annurev.immunol.16.1.89 · Cited by 514 · see citing works
Cortical Constriction During Abscission Involves Helices of ESCRT-III–Dependent Filaments
Guizetti, J., Schermelleh, L., Mäntler, J., Maar, S., Poser, I., Leonhardt, H., Müller-Reichert, T., & Gerlich, D. (2011) · Science · doi:10.1126/science.1201847 · Cited by 496 · see citing works
ESCRT-III Dysfunction Causes Autophagosome Accumulation and Neurodegeneration
Lee, J., Beigneux, A. P., Ahmad, S. T., Young, S. G., & Gao, F. (2007) · Current Biology · doi:10.1016/j.cub.2007.07.029 · Cited by 490 · see citing works
Interfering with Apoptosis: Ca 2+ -Binding Protein ALG-2 and Alzheimer's Disease Gene ALG-3
Vito, P., Lacaná, E., & D'adamio, L. (1996) · Science · doi:10.1126/science.271.5248.521 · Cited by 468 · see citing works
Vps27 recruits ESCRT machinery to endosomes during MVB sorting
Katzmann, D. J., Stefan, C. J., Babst, M., & Emr, S. D. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200302136 · Cited by 455 · see citing works
ESCRT-mediated lysosome repair precedes lysophagy and promotes cell survival
Radulovic, M., Bongiovanni, A., Schink, K., Nähse, V., Wenzel, E. M., Lafont, F., & Stenmark, H. (2018) · bioRxiv · doi:10.15252/embj.201899753 · Cited by 423 · see citing works
Separation and Characterization of Late Endosomal Membrane Domains
Kobayashi, T., Beuchat, M.-H., Chevallier, J., Makino, A., Mayran, N., Escola, J.-M., Lebrand, C., Cosson, P., Kobayashi, T., & Gruenberg, J. E. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m202838200 · Cited by 409 · see citing works
Self-citationElia, N., Sougrat, R., Spurlin, T. A., Hurley, J. H., & Lippincott‐Schwartz, J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102714108 · Cited by 389 · see citing works
Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing
Vietri, M., Schink, K. O., Campsteijn, C., Wegner, C. S., Schultz, S. W., Christ, L., Thoresen, S. B., Brech, A., Raiborg, C., & Stenmark, H. (2015) · Nature · doi:10.1038/nature14408 · Cited by 378 · see citing works
Mechanisms of pathogen entry through the endosomal compartments
Gruenberg, J., & van der Goot, F. G. (2006) · Nature reviews. Molecular cell biology · doi:10.1038/nrm1959 · Cited by 360 · see citing works
Self-citationMechanism of Ca2+-triggered ESCRT assembly and regulation of cell membrane repair
Scheffer, L., Sreetama, S. C., Sharma, N., Medikayala, S., Brown, K. J., Defour, A., & Jaiswal, J. K. (2014) · Nature Communications · doi:10.1038/ncomms6646 · Cited by 358 · see citing works
ESCRT-III controls nuclear envelope reformation
Olmos, Y., Hodgson, L. R., Mantell, J., Verkade, P., & Carlton, J. G. (2015) · Nature · doi:10.1038/nature14503 · Cited by 355 · see citing works
Helical Structures of ESCRT-III Are Disassembled by VPS4
Lata, S., Schoehn, G., Jain, A., Vieira-Pires, R. S., Piehler, J., Göttlinger, H. G., & Weissenhorn, W. (2008) · Science · doi:10.1126/science.1161070 · Cited by 352 · see citing works
Late endosome motility depends on lipids via the small GTPase Rab7
Lebrand, C., Felberbaum‐Corti, M., Goodson, H. V., Cosson, P., Cavalli, V., Mayran, N., Fauré, J., & Gruenberg, J. E. (2002) · The EMBO Journal · doi:10.1093/emboj/21.6.1289 · Cited by 338 · see citing works
Self-citationTeis, D., Saksena, S., & Emr, S. D. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.08.013 · Cited by 338 · see citing works
Relaxation of Loaded ESCRT-III Spiral Springs Drives Membrane Deformation
Chiaruttini, N., Redondo‐Morata, L., Colom, A., Humbert, F., Lenz, M., Simon Scheuring, A., & Roux, A. (2015) · Cell · doi:10.1016/j.cell.2015.10.017 · Cited by 331 · see citing works
Self-citationPmel17 initiates premelanosome morphogenesis within multivesicular bodies
Berson, J. F., Harper, D. C., Tenza, D., Raposo, G., & Marks, M. S. (2001) · Molecular Biology of the Cell · doi:10.1091/mbc.12.11.3451 · Cited by 326 · see citing works
ALIX and the multivesicular endosome: ALIX in Wonderland
Bissig, C., & Gruenberg, J. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2013.10.009 · Cited by 323 · see citing works
Self-citationKölling, R., & Hollenberg, C. P. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06627.x · Cited by 320 · see citing works
Structural and Biochemical Studies of ALIX/AIP1 and Its Role in Retrovirus Budding
Fisher, R. D., Chung, H.-Y., Zhai, Q., Robinson, H., Sundquist, W. I., & Hill, C. P. (2007) · Cell · doi:10.1016/j.cell.2007.01.035 · Cited by 315 · see citing works
Tetraspanins as Regulators of Protein Trafficking
Berditchevski, F., & Odintsova, E. (2006) · Traffic · doi:10.1111/j.1600-0854.2006.00515.x · Cited by 296 · see citing works
Functional Reconstitution of ESCRT-III Assembly and Disassembly
Saksena, S., Wahlman, J., Teis, D., Johnson, A. E., & Emr, S. D. (2009) · Cell · doi:10.1016/j.cell.2008.11.013 · Cited by 296 · see citing works
Theos, A. C., Truschel, S. T., Tenza, D., Hurbain, I., Harper, D. C., Berson, J. F., Thomas, P. C., Raposo, G., & Marks, M. S. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.01.012 · Cited by 289 · see citing works
Kleijmeer, M. J., Ramm, G., Schuurhuis, D. H., Griffith, J. M., Rescigno, M., Ricciardi‐Castagnoli, P., Rudensky, A. Y., OSSENDORP, F. A., Melief, C. J. M., Stoorvogel, W., et al. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200103071 · Cited by 288 · see citing works
Berditchevski, F., Zutter, M. M., & Hemler, M. E. (1996) · Molecular Biology of the Cell · doi:10.1091/mbc.7.2.193 · Cited by 274 · see citing works
Lysosome-related organelles: unusual compartments become mainstream
Marks, M. S., Heijnen, H. F. G., & Raposo, G. (2013) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2013.04.008 · Cited by 266 · see citing works
Bishop, N. E., Horman, A., & Woodman, P. G. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200112080 · Cited by 266 · see citing works
Mierzwa, B. E., Chiaruttini, N., Redondo‐Morata, L., von Filseck, J. M., König, J., Larios, J., Poser, I., Müller‐Reichert, T., Simon Scheuring, A., Roux, A., et al. (2017) · Nature Cell Biology · doi:10.1038/ncb3559 · Cited by 252 · see citing works
Self-citationMissotten, M., Nichols, A., Rieger, K., & Sadoul, R. (1999) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400456 · Cited by 239 · see citing works
Vito, P., Pellegrini, L., Guiet, C., & D'adamio, L. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.3.1533 · Cited by 235 · see citing works
Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release
Carlton, J. G., Agromayor, M., & Martin‐Serrano, J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802008105 · Cited by 233 · see citing works
ALIX-CHMP4 interactions in the human ESCRT pathway
McCullough, J., Fisher, R. D., Whitby, F. G., Sundquist, W. I., & Hill, C. P. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801567105 · Cited by 233 · see citing works
Hrs‐ and CD63 ‐Dependent Competing Mechanisms Make Different Sized Endosomal Intraluminal Vesicles
Edgar, J. R., Eden, E. R., & Futter, C. E. (2013) · Traffic · doi:10.1111/tra.12139 · Cited by 224 · see citing works
Abrami, L., Brandi, L., Moayeri, M., Brown, M. J., Krantz, B. A., Leppla, S. H., & van der Goot, F. G. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.10.019 · Cited by 216 · see citing works
Katoh, K., Shibata, H., Suzuki, H., Nara, A., Ishidoh, K., Kominami, E., Yoshimori, T., & Maki, M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301604200 · Cited by 213 · see citing works
Ubiquitin-Dependent Sorting in EndocytosisPreprint
Piper, R. C., Đikić, I., & Lukács, G. L. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016808 · Cited by 209 · see citing works
Exosomes in developmental signalling
McGough, I. J., & Vincent, J. (2016) · Development · doi:10.1242/dev.126516 · Cited by 207 · see citing works
LEM2 recruits CHMP7 for ESCRT-mediated nuclear envelope closure in fission yeast and human cells
Gu, M., LaJoie, D., Chen, O. S., von Appen, A., Ladinsky, M. S., Redd, M. J., Nikolova, L. S., Björkman, P. J., Sundquist, W. I., Ullman, K. S., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1613916114 · Cited by 196 · see citing works
Bowers, K., Piper, S. C., Edeling, M. A., Gray, S. R., Owen, D. J., Lehner, P. J., & Luzio, J. P. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m508632200 · Cited by 187 · see citing works
Exosomes contain ubiquitinated proteins
Buschow, S. I., Liefhebber, J. M. P., Wubbolts, R., & Stoorvogel, W. (2005) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2005.08.005 · Cited by 185 · see citing works
Adell, M. A. Y., Vogel, G. F., Pakdel, M., Müller, M., Lindner, H. H., Hess, M. W., & Teis, D. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201310114 · Cited by 182 · see citing works
How Ubiquitin Functions with ESCRTs
Shields, S. B., & Piper, R. C. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01242.x · Cited by 175 · see citing works
Structural Basis for Endosomal Targeting by the Bro1 Domain
Kim, J., Sitaraman, S., Hierro, A., Beach, B. M., Odorizzi, G., & Hurley, J. H. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.04.001 · Cited by 174 · see citing works
ALIX binds a YPX3L motif of the GPCR PAR1 and mediates ubiquitin-independent ESCRT-III/MVB sorting
Dores, M. R., Chen, B., Lin, H., Soh, U. J. K., Paing, M. M., Montagne, W. A., Meerloo, T., & Trejo, J. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201110031 · Cited by 163 · see citing works
ALIX and ESCRT-I/II function as parallel ESCRT-III recruiters in cytokinetic abscission
Christ, L., Wenzel, E. M., Liestøl, K., Raiborg, C., Campsteijn, C., & Stenmark, H. (2016) · Journal of Cell Biology · doi:10.1083/jcb.201507009 · Cited by 163 · see citing works
Teis, D., Saksena, S., Judson, B. L., & Emr, S. D. (2010) · The EMBO Journal · doi:10.1038/emboj.2009.408 · Cited by 162 · see citing works
Hurbain, I., Geerts, W. J. C., Boudier, T., Marco, S., Verkleij, A. J., Marks, M. S., & Raposo, G. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803488105 · Cited by 160 · see citing works
Structural basis for activation, assembly and membrane binding of ESCRT-III Snf7 filaments
Tang, S., Henne, W. M., Borbat, P. P., Buchkovich, N. J., Freed, J. H., Mao, Y., Fromme, J. C., & Emr, S. D. (2015) · eLife · doi:10.7554/elife.12548 · Cited by 156 · see citing works
Doyotte, A., Mironov, A., McKenzie, E., & Woodman, P. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707601105 · Cited by 154 · see citing works
Adell, M. A. Y., Migliano, S. M., Upadhyayula, S., Bykov, Y. S., Sprenger, S., Pakdel, M., Vogel, G. F., Jih, G. T., Skillern, W., Behrouzi, R., et al. (2017) · eLife · doi:10.7554/elife.31652 · Cited by 154 · see citing works
Lysosome-related organelles as functional adaptations of the endolysosomal system
Delevoye, C., Marks, M. S., & Raposo, G. (2019) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2019.05.003 · Cited by 147 · see citing works
Usami, Y., Popov, S., & Göttlinger, H. G. (2007) · Journal of Virology · doi:10.1128/jvi.00314-07 · Cited by 143 · see citing works
Apolipoprotein E Regulates Amyloid Formation within Endosomes of Pigment Cells
van Niel, G., Bergam, P., Cicco, A. D., Hurbain, I., Cicero, A. L., Dingli, F., Palmulli, R., Fort, C., Potier, M., Schurgers, L. J., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.08.057 · Cited by 143 · see citing works
A Crescent-Shaped ALIX Dimer Targets ESCRT-III CHMP4 Filaments
Vieira-Pires, R. S., Hartlieb, B., Signor, L., Schoehn, G., Lata, S., Roessle, M. W., Moriscot, C., Popov, S., Hinz, A., Jamin, M., et al. (2009) · Structure · doi:10.1016/j.str.2009.04.007 · Cited by 138 · see citing works
Higginbotham, J. N., Zhang, Q., Jeppesen, D. K., Scott, A. M., Manning, H. C., Ochieng, J., Franklin, J. L., & Coffey, R. J. (2016) · Journal of Extracellular Vesicles · doi:10.3402/jev.v5.29254 · Cited by 133 · see citing works
Membrane Binding by CHMP7 Coordinates ESCRT-III-Dependent Nuclear Envelope Reformation
Olmos, Y., Perdrix-Rosell, A., & Carlton, J. G. (2016) · Current Biology · doi:10.1016/j.cub.2016.07.039 · Cited by 132 · see citing works
López-Jiménez, A. T., Cardenal‐Muñoz, E., Leuba, F., Gerstenmaier, L., Barisch, C., Hagedorn, M., King, J., & Soldati, T. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1007501 · Cited by 132 · see citing works
Structural analysis and modeling reveals new mechanisms governing ESCRT-III spiral filament assembly
Shen, Q.-T., Schuh, A. L., Zheng, Y., Quinney, K., Wang, L., Hanna, M., Mitchell, J. C., Otegui, M. S., Ahlquist, P., Cui, Q., et al. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201403108 · Cited by 129 · see citing works
Post-translational add-ons mark the path in exosomal protein sorting
Moreno-Gonzalo, O., Fernández‐Delgado, I., & Sánchez‐Madrid, F. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2690-y · Cited by 128 · see citing works
Viral Infection Controlled by a Calcium-Dependent Lipid-Binding Module in ALIX
Bissig, C., Lenoir, M., Velluz, M., Kufareva, I., Abagyan, R. A., Overduin, M., & Gruenberg, J. E. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.04.003 · Cited by 126 · see citing works
Self-citationMolecular interactions shaping the tetraspanin web
van Deventer, S. J., Dunlock, V.-M. E., & van Spriel, A. B. (2017) · Biochemical Society Transactions · doi:10.1042/bst20160284 · Cited by 126 · see citing works
Recruitment of UBPY and ESCRT Exchange Drive HD-PTP-Dependent Sorting of EGFR to the MVB
Ali, N., Zhang, L., Taylor, S., Mironov, A., Urbé, S., & Woodman, P. G. (2013) · Current Biology · doi:10.1016/j.cub.2013.02.033 · Cited by 121 · see citing works
Alix/AIP1 Antagonizes Epidermal Growth Factor Receptor Downregulation by the Cbl-SETA/CIN85 Complex
Schmidt, M. H. H., Hoeller, D., Yu, J., Furnari, F. B., Cavenee, W. K., Đikić, I., & Bögler, O. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.20.8981-8993.2004 · Cited by 121 · see citing works
Spatial Separation of HLA-DM/HLA-DR Interactions within MIIC and Phagosome-Induced Immune Escape
Zwart, W. T., Griekspoor, A., Kuijl, C. P., Marsman, M., van Rheenen, J., Janssen, H., Calafat, J., van Ham, S. M., Janssen, L., van Lith, M., et al. (2005) · Immunity · doi:10.1016/j.immuni.2005.01.006 · Cited by 117 · see citing works
Guix, F. X., Sannerud, R., Berditchevski, F., Arranz, A. M., Horré, K., Snellinx, A., Thathiah, A., Saido, T. C., Saito, T., Rajesh, S., et al. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-017-0165-0 · Cited by 98 · see citing works
Pashkova, N., Gakhar, L., Winistorfer, S. C., Sunshine, A. B., Rich, M. S., Dunham, M. J., Yu, L. P., & Piper, R. C. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.04.007 · Cited by 94 · see citing works
Alix, a Protein Regulating Endosomal Trafficking, Is Involved in Neuronal Death
Trioulier, Y., Torch, S., Blot, B., Cristina, N., Chatellard, C., Verna, J., & Sadoul, R. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m309243200 · Cited by 94 · see citing works
ALIX Is a Lys63-Specific Polyubiquitin Binding Protein that Functions in Retrovirus Budding
Dowlatshahi, D. P., Sandrin, V., Vivona, S., Shaler, T. A., Kaiser, S. E., Melandri, F. D., Sundquist, W. I., & Kopito, R. R. (2012) · Developmental Cell · doi:10.1016/j.devcel.2012.10.023 · Cited by 86 · see citing works
ESCRT-III activation by parallel action of ESCRT-I/II and ESCRT-0/Bro1 during MVB biogenesis
Tang, S., Buchkovich, N. J., Henne, W. M., Banjade, S., Kim, Y. J., & Emr, S. D. (2016) · eLife · doi:10.7554/elife.15507 · Cited by 84 · see citing works
Shi, Y., Zhou, W., Cheng, L., Chen, C., Huang, Z., Fang, X., Wu, Q., He, Z., Xu, S., Lathia, J. D., et al. (2016) · Cell Death and Differentiation · doi:10.1038/cdd.2016.110 · Cited by 82 · see citing works
Endosomal vesicles as vehicles for viral genomes
Nour, A. M., & Modis, Y. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2014.03.006 · Cited by 70 · see citing works
Keren‐Kaplan, T., Attali, I., Estrin, M., Kuo, L. S., Farkash, E., Jerabek‐Willemsen, M., Wertheimer, N. B., Artzi, S., Peri, A., Freed, E. O., et al. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.4 · Cited by 67 · see citing works
Odintsova, E., van Niel, G., Conjeaud, H., Raposo, G., Iwamoto, R., Mekada, E., & Berditchevski, F. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.439380 · Cited by 66 · see citing works
Functional Replacement of a Retroviral Late Domain by Ubiquitin Fusion
Joshi, A., Munshi, U. M., Ablan, S. D., Nagashima, K., & Freed, E. O. (2008) · Traffic · doi:10.1111/j.1600-0854.2008.00817.x · Cited by 66 · see citing works
Meng, B., Ip, N. C. Y., Prestwood, L. J., Abbink, T. E. M., & Lever, A. M. L. (2015) · Retrovirology · doi:10.1186/s12977-015-0197-x · Cited by 65 · see citing works
The ESCRT‐I Subunit TSG101 Controls Endosome‐to‐Cytosol Release of Viral RNA
Luyet, P., Falguières, T., Pons, V., Pattnaik, A. K., & Gruenberg, J. E. (2008) · Traffic · doi:10.1111/j.1600-0854.2008.00820.x · Cited by 63 · see citing works
Self-citationIchioka, F., Takaya, E., SUZUKI, H., Kajigaya, S., Buchman, V. L., Shibata, H., & Maki, M. (2006) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2006.11.008 · Cited by 61 · see citing works
Dores, M. R., Grimsey, N. J., Mendez, F., & Trejo, J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0157587 · Cited by 58 · see citing works
ATG12–ATG3 connects basal autophagy and late endosome function
Murrow, L. M., & Debnath, J. (2015) · Autophagy · doi:10.1080/15548627.2015.1040976 · Cited by 55 · see citing works
Activation of the Retroviral Budding Factor ALIX
Zhai, Q., Landesman, M. B., Chung, H.-Y., Dierkers, A., Jeffries, C. M., Trewhella, J., Hill, C. P., & Sundquist, W. I. (2011) · Journal of Virology · doi:10.1128/jvi.02653-10 · Cited by 52 · see citing works
Dynamic and elastic shape transitions in curved ESCRT-III filaments
Chiaruttini, N., & Roux, A. (2017) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2017.07.002 · Cited by 51 · see citing works
Self-citationIchioka, F., Kobayashi, R., Katoh, K., Shibata, H., & Maki, M. (2008) · The FEBS Journal · doi:10.1111/j.1742-4658.2007.06230.x · Cited by 41 · see citing works
Hp95 promotes anoikis and inhibits tumorigenicity of HeLa cells
Wu, Y., Pan, S., Luo, W., Lin, S.-H., & Kuang, J. (2002) · Oncogene · doi:10.1038/sj.onc.1205849 · Cited by 41 · see citing works
Decoding the intrinsic mechanism that prohibits ALIX interaction with ESCRT and viral proteins
Zhou, X., Si, J., Corvera, J., Gallick, G. E., & Kuang, J. (2010) · Biochemical Journal · doi:10.1042/bj20100862 · Cited by 38 · see citing works
Wang, Y., Tong, X., Omoregie, E. S., Liu, W., Meng, S., & Ye, X. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.390401 · Cited by 35 · see citing works
The CD9, CD81, and CD151 EC2 domains bind to the classical RGD-binding site of integrin αvβ3
Yu, F., Lee, C.-Y., Changou, C. A., Cedano-Prieto, D. M., Takada, Y. K., & Takada, Y. (2016) · Biochemical Journal · doi:10.1042/bcj20160998 · Cited by 32 · see citing works
Role of SNX16 in the Dynamics of Tubulo-Cisternal Membrane Domains of Late Endosomes
Brankatschk, B., Pons, V., Parton, R. G., & Gruenberg, J. E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021771 · Cited by 30 · see citing works
Self-citationThe CHMP4b- and Src-docking sites in the Bro1 domain are autoinhibited in the native state of Alix
Zhou, X., Pan, S., Sun, L., Corvera, J., Lee, Y.-C., Lin, S.-H., & Kuang, J. (2008) · Biochemical Journal · doi:10.1042/bj20081388 · Cited by 28 · see citing works
Zhou, X., Pan, S., Sun, L., Corvera, J., Lin, S.-H., & Kuang, J. (2008) · Biochemical Journal · doi:10.1042/bj20080642 · Cited by 24 · see citing works
Tetraspan cargo adaptors usher GPI-anchored proteins into multivesicular bodies
MacDonald, C., Stamnes, M. A., Katzmann, D. J., & Piper, R. C. (2015) · Cell Cycle · doi:10.1080/15384101.2015.1100773 · Cited by 15 · see citing works
In Vitro Polymerization of F-actin on Early Endosomes
Muriel, O., Scott, C. C., Larios, J., et al. (2017) · Journal of Visualized Experiments · doi:10.3791/55829 · Cited by 3 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Current Knowledge on Exosome Biogenesis, Cargo-Sorting Mechanism and Therapeutic Implications
Xie, S., Zhang, Q., & Jiang, L. (2022) · Membranes · doi:10.3390/membranes12050498 · Cited by 262 · see citing works
The Therapeutic Potential and Clinical Significance of Exosomes as Carriers of Drug Delivery System
Li, T., Li, X., Han, G., Liang, M., Yang, Z., Zhang, C., Huang, S., Tai, S., & Yu, S. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics15010021 · Cited by 110 · see citing works
- Authors
- Larios, J., Mercier, V., Roux, A., & Gruenberg, J.
- Affiliations
- University of Geneva (CH)
- Corresponding author
- Roux, Aurélien
- Gruenberg, Jean
- Venue
- Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 2020-02-12
- Volume
- 219
- Issue
- 3
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC7054990
- OpenAlex
- W3005622563
- Cited by
- 422
- References
- 128
- Citations by year
- 2026: 51 · 2025: 83 · 2024: 84 · 2023: 74 · 2022: 57 · 2021: 54 · 2020: 19
- FWCI
- 25.43
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- The Journal of Cell Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- 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
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- Alix, ESCRT-III, tetraspanins, exosomes, intraluminal vesicles, endosomes, exosome biogenesis, lysobisphosphatidic acid, cargo sorting, membrane deformation, membrane fission, ESCRT
- MeSH terms
- Calcium-Binding Proteins, HeLa Cells, Humans, Lysophospholipids, Endosomes, Time Factors, Cell Cycle Proteins, Protein Transport, Monoglycerides, Exosomes, Endosomal Sorting Complexes Required for Transport, Tetraspanins, Tetraspanin 30, Tetraspanin 28, Tetraspanin 29
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