Unravelling the pivotal role of Alix in MVB sorting and silencing of the activated EGFR
Open accessAbstract
Endosomal sorting complex required for transport (ESCRT)-III-mediated membrane invagination and scission are a critical step in multivesicular body (MVB) sorting of ubiquitinated membrane receptors, and generally thought to be required for degradation of these receptors in lysosomes. The adaptor protein Alix is critically involved in multiple ESCRT-III-mediated, membrane-remodelling processes in mammalian cells. However, Alix knockdown does not inhibit degradation of the activated epidermal growth factor receptor (EGFR) in mammalian cell lines, leading to a widely held notion that Alix is not critically involved in MVB sorting of ubiquitinated membrane receptors in mammalian cells. In the present study, we demonstrate that, despite its non-essential role in degradation of the activated EGFR, Alix plays a critical role in its MVB sorting and silencing Epidermal growth factor (EGF) stimulation of mammalian cell lines induces Alix's interaction with the ubiquitinated EGFR via the Alix V domain, and increases Alix's association with membrane-bound charged multivesicular body protein 4 (CHMP4) via the Alix Bro1 domain. Under both continuous and pulse-chase EGF stimulation conditions, inhibition of Alix's interaction with membrane-bound CHMP4, inhibition of Alix dimerization through the V domain or Alix knockdown dramatically inhibits MVB sorting of the activated EGFR and promotes sustained activation of extracellular-signal regulated kinase (ERK)1/2. Under the continuous EGF stimulation conditions, these cell treatments also retard degradation of the activated EGFR. These findings indicate that Alix is critically involved in MVB sorting of ubiquitinated membrane receptors in mammalian cells.
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?
Loss of Alix protein involved in ILV biogenesis in MVBs resulted in alteration of membrane budding, a decrease in the number of ELV released, and modifications of ELV-MT composition.
“In their study, loss of Alix protein involved in ILV biogenesis in MVBs (Sun et al., 2015) resulted in alteration of membrane budding, a decrease in the number of ELV released and a modifications of ELV-MT composition”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Sun et al., 2015
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
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
Henne, W. M., Buchkovich, N. J., & Emr, S. D. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.05.015 · Cited by 1,505 · see citing works
Receptor downregulation and multivesicular-body sorting
Katzmann, D. J., Odorizzi, G., & Emr, S. D. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm973 · Cited by 1,201 · 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
The Protein Network of HIV Budding
von Schwedler, U. K., Stuchell‐Brereton, M. D., Müller, B., Ward, D. M., Chung, H.-Y., Morita, E., Wang, H. E., Davis, T., He, G.-P., Cimbora, D. M., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00714-1 · Cited by 815 · 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
Membrane budding and scission by the ESCRT machinery: it's all in the neck
Hurley, J. H., & Hanson, P. I. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2937 · Cited by 757 · 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
The biogenesis of multivesicular endosomes
Gruenberg, J. E., & Stenmark, H. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1360 · Cited by 723 · see citing works
Wnt Signaling Requires Sequestration of Glycogen Synthase Kinase 3 inside Multivesicular Endosomes
Taelman, V. F., Dobrowolski, R., Plouhinec, J.-L., Fuentealba, L. C., Vorwald, P. P., Gumper, I., Sabatini, D. D., & Robertis, E. M. D. (2010) · Cell · doi:10.1016/j.cell.2010.11.034 · Cited by 715 · 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
ESCRT 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
Agonist-promoted Ubiquitination of the G Protein-coupled Receptor CXCR4 Mediates Lysosomal Sorting
Marchese, A., & Benovic, J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.c100527200 · Cited by 473 · see citing works
Molecular Mechanisms of the Membrane Sculpting ESCRT PathwayPreprint
Henne, W. M., Stenmark, H., & Emr, S. D. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016766 · Cited by 443 · see citing works
Aniento, F. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.123.6.1373 · Cited by 404 · see citing works
EGF stimulates annexin 1‐dependent inward vesiculation in a multivesicular endosome subpopulation
White, I. J., Bailey, L. M., Aghakhani, M. R., Moss, S. E., & Futter, C. E. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600759 · Cited by 367 · 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
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
Human VPS34 is required for internal vesicle formation within multivesicular endosomes
Futter, C. E., Collinson, L., Backer, J., & Hopkins, C. R. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200108152 · Cited by 248 · see citing works
Missotten, M., Nichols, A., Rieger, K., & Sadoul, R. (1999) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400456 · Cited by 239 · see citing works
Binding of Human Immunodeficiency Virus Type 1 Gag to Membrane: Role of the Matrix Amino Terminus
Ono, A., & Freed, E. O. (1999) · Journal of Virology · doi:10.1128/jvi.73.5.4136-4144.1999 · Cited by 238 · 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
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
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
Bro1 is an endosome-associated protein that functions in the MVB pathway in Saccharomyces cerevisiae
Odorizzi, G., Katzmann, D. J., Babst, M., Audhya, A., & Emr, S. D. (2003) · Journal of Cell Science · doi:10.1242/jcs.00395 · Cited by 213 · see citing works
Spearman, P. W., Horton, R., Ratner, L., & Kuli-zade, I. (1997) · Journal of Virology · doi:10.1128/jvi.71.9.6582-6592.1997 · Cited by 204 · 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
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
In Vitro Budding of Intralumenal Vesicles into Late Endosomes Is Regulated by Alix and Tsg101
Falguières, T., Luyet, P., Bissig, C., Scott, C. C., Velluz, M., & Gruenberg, J. E. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-03-0239 · Cited by 155 · 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
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
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
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
Malerød, L., Stuffers, S., Brech, A., & Stenmark, H. (2007) · Traffic · doi:10.1111/j.1600-0854.2007.00630.x · Cited by 120 · see citing works
UBAP1 Is a Component of an Endosome-Specific ESCRT-I Complex that Is Essential for MVB Sorting
Stefani, F., Zhang, L., Taylor, S., Donovan, J., Rollinson, S. J., Doyotte, A., Brownhill, K., Callister, J. B., Pickering-Brown, S. M., & Woodman, P. G. (2011) · Current Biology · doi:10.1016/j.cub.2011.06.028 · Cited by 119 · see citing works
Alix regulates cortical actin and the spatial distribution of endosomes
Cabezas, A., Bache, K. G., Brech, A., & Stenmark, H. (2005) · Journal of Cell Science · doi:10.1242/jcs.02382 · Cited by 113 · 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
Nikko, E., Marini, A., & André, B. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306953200 · Cited by 93 · 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
Structure and function of ESCRT-III
Lata, S., Schoehn, G., Solomons, J., Vieira-Pires, R. S., Göttlinger, H. G., & Weissenhorn, W. (2009) · Biochemical Society Transactions · doi:10.1042/bst0370156 · Cited by 77 · see citing works
Schmidt, M. H. H., Dikic, I., & Bögler, O. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m409839200 · Cited by 76 · see citing works
Down-regulation of epidermal growth factor receptor signalling within multivesicular bodies
Eden, E. R., White, I. J., & Futter, C. E. (2009) · Biochemical Society Transactions · doi:10.1042/bst0370173 · Cited by 71 · see citing works
Involvement of the Conserved Adaptor Protein Alix in Actin Cytoskeleton Assembly
Pan, S., Wang, R., Zhou, X., He, G., Koomen, J. M., Kobayashi, R., Sun, L., Corvera, J., Gallick, G. E., & Kuang, J. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m602263200 · Cited by 68 · see citing works
Self-citationKeren‐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
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
Yeast Npi3/Bro1 is involved in ubiquitin‐dependent control of permease trafficking
Springael, J., Nikko, E., André, B., & Marini, A. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)02586-3 · Cited by 60 · see citing works
ESCRT Proteins and Cell Signalling
Wegner, C. S., Rodahl, L. M., & Stenmark, H. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01210.x · Cited by 52 · see citing works
Multisite M-Phase Phosphorylation of Xenopus Wee1A
Kim, S. Y., Song, E. J., Lee, K., & Ferrell, J. E. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.23.10580-10590.2005 · Cited by 45 · see citing works
Overexpression of Hp95 induces G1 phase arrest in confluent HeLa cells
Wu, Y., Pan, S., Che, S., He, G., Nelman-Gonzalez, M. A., Weil, M. M., & Kuang, J. (2001) · Differentiation · doi:10.1046/j.1432-0436.2001.670406.x · Cited by 42 · see citing works
Self-citationXu, T., Lu, R.-F., Romano, D., Pitt, A. R., Houslay, M. D., Milligan, G., & Kölch, W. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.05770-11 · Cited by 38 · see citing works
The 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
Self-citationZhou, 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
Self-citationMPM‐2 epitope sequence is not sufficient for recognition and phosphorylation by ME kinase‐H
Che, S., Weil, M. M., Nelman-Gonzalez, M. A., Ashorn, C. L., & Kuang, J. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)00948-4 · Cited by 23 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Therapeutically harnessing extracellular vesicles
Cheng, L., & Hill, A. F. (2022) · Nature Reviews Drug Discovery · doi:10.1038/s41573-022-00410-w · Cited by 737 · see citing works
Extracellular Vesicles as Delivery Vehicles of Specific Cellular Cargo
Mir, B., & Goettsch, C. (2020) · Cells · doi:10.3390/cells9071601 · Cited by 137 · see citing works
Skeletal Muscle-Released Extracellular Vesicles: State of the Art
Rome, S., Forterre, A., Mizgier, M. L., & Bouzakri, K. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00929 · Cited by 139 · see citing works
Endocytic regulation of cytokine receptor signaling
Cendrowski, J., Mamińska, A., & Miączyńska, M. (2016) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2016.07.002 · Cited by 124 · see citing works
Small extracellular vesicle PD-L1 in cancer: the knowns and unknowns
Yu, Z., Liu, J., & Chen, G. (2022) · npj Precision Oncology · doi:10.1038/s41698-022-00287-3 · Cited by 64 · see citing works
Focus on the morphogenesis, fate and the role in tumor progression of multivesicular bodies
Peng, X., Yang, L., Ma, Y., Li, Y., & Li, H. (2020) · Cell Communication and Signaling · doi:10.1186/s12964-020-00619-5 · Cited by 60 · see citing works
Wang, J., Zou, J. X., Wang, H., Duan, Z.-J., Wang, H.-B., Chen, P., Liu, P.-Q., Xu, J., & Chen, H.-W. (2019) · Acta Pharmacologica Sinica · doi:10.1038/s41401-018-0199-z · Cited by 58 · see citing works
Multifaceted Roles of ALG-2 in Ca2+-Regulated Membrane Trafficking
Maki, M., Takahara, T., & Shibata, H. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17091401 · Cited by 50 · see citing works
Bardet-Biedl syndrome proteins modulate the release of bioactive extracellular vesicles
Volz, A., Frei, A., Kretschmer, V., Domingues, A. M. D. J., Ketting, R. F., Ueffing, M., Boldt, K., Krämer‐Albers, E., & May‐Simera, H. (2021) · Nature Communications · doi:10.1038/s41467-021-25929-1 · Cited by 45 · see citing works
The role of CHMP2BIntron5 in autophagy and frontotemporal dementia
Krasniak, C. S., & Ahmad, S. T. (2016) · Brain Research · doi:10.1016/j.brainres.2016.02.051 · Cited by 46 · see citing works
The role of ESCRT during development and functioning of the nervous system
Sadoul, R., Laporte, M. H., Chassefeyre, R., Il, K., Goldberg, Y., Chatellard, C., Hemming, F. J., & Fraboulet, S. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.08.013 · Cited by 43 · see citing works
ALG-2 interacting protein-X (Alix) is essential for clathrin-independent endocytosis and signaling
Mercier, V., Laporte, M. H., Destaing, O., Blot, B., Blouin, C. M., Pernet‐Gallay, K., Chatellard, C., Saoudi, Y., Albigès‐Rizo, C., Lamaze, C., et al. (2016) · Scientific Reports · doi:10.1038/srep26986 · Cited by 40 · see citing works
Sun, S., Sun, L., Zhou, X., Wu, C., Wang, R., Lin, S.-H., & Kuang, J. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.01.001 · Cited by 36 · see citing works
Self-citationALG-2 activates the MVB sorting function of ALIX through relieving its intramolecular interaction
Sun, S., Zhou, X., Corvera, J., Gallick, G. E., Lin, S.-H., & Kuang, J. (2015) · Cell Discovery · doi:10.1038/celldisc.2015.18 · Cited by 35 · see citing works
Self-citationTabernero, L., & Woodman, P. G. (2018) · Biochemical Society Transactions · doi:10.1042/bst20170443 · Cited by 30 · see citing works
Cooperation and Interplay between EGFR Signalling and Extracellular Vesicle Biogenesis in Cancer
Zanetti-Domingues, L. C., Bonner, S. E., Iyer, R. S., Martin-Fernandez, M. L., & Huber, V. (2020) · Cells · doi:10.3390/cells9122639 · Cited by 28 · see citing works
Gahloth, D., Heaven, G., Jowitt, T. A., Mould, A. P., Bella, J., Baldock, C., Woodman, P. G., & Tabernero, L. (2017) · Scientific Reports · doi:10.1038/s41598-017-09467-9 · Cited by 26 · see citing works
Structural Basis for Selective Interaction between the ESCRT Regulator HD-PTP and UBAP1
Gahloth, D., Levy, C., Heaven, G., Stefani, F., Wunderley, L., Mould, A. P., Cliff, M. J., Bella, J., Fielding, A. J., Woodman, P. G., et al. (2016) · Structure · doi:10.1016/j.str.2016.10.006 · Cited by 25 · see citing works
Lee, J., Oh, K., Lee, D., Kim, B. Y., Choi, J. S., Ku, B., & Kim, S. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0149113 · Cited by 21 · see citing works
Kaul, Z., & Chakrabarti, O. (2017) · Molecular Biology of the Cell · doi:10.1091/mbc.e16-12-0855 · Cited by 22 · see citing works
CCL2 mobilizes ALIX to facilitate Gag-p6 mediated HIV-1 virion release
Ajasin, D., Rao, V. R., Wu, X., Ramasamy, S., Pujato, M. A., Ruiz, A. P., Fiser, A., Bresnick, A. R., Kalpana, G. V., & Prasad, V. R. (2019) · eLife · doi:10.7554/elife.35546 · Cited by 18 · see citing works
Qiu, X., Campos, Y., van de Vlekkert, D., Gomero, E. M., Tanwar, A. S., Kalathur, R., Weesner, J. A., Bongiovanni, A., Demmers, J., & d’Azzo, A. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.102425 · Cited by 14 · see citing works
Parkinson, G. T., Roboti, P., Zhang, L., Taylor, S., & Woodman, P. G. (2021) · Journal of Cell Science · doi:10.1242/jcs.259192 · Cited by 13 · see citing works
ESCRT-III on endosomes: new functions, new activation pathway
Woodman, P. G. (2016) · Biochemical Journal · doi:10.1042/bj20151115 · Cited by 10 · see citing works
Desrochers, G., Kazan, J. M., & Pause, A. (2018) · Biochemistry and Cell Biology · doi:10.1139/bcb-2017-0322 · Cited by 9 · see citing works
The role of Alix in the proliferation of human glioma cells
Zhao, C., Ban, N., Dai, S., Zhang, X., Zhang, L., Xu, P., Chen, W., Sun, J., Bao, Z., Chang, H., et al. (2016) · Human Pathology · doi:10.1016/j.humpath.2015.09.046 · Cited by 8 · see citing works
Trubetckaia, O., Lane, A. E., Qian, L., Zhou, P., & Lane, D. (2019) · Communications Biology · doi:10.1038/s42003-019-0651-8 · Cited by 8 · see citing works
Pashkova, N., Yu, L., Schnicker, N., Tseng, C.-C., Gakhar, L., Katzmann, D. J., & Piper, R. C. (2021) · Molecular Biology of the Cell · doi:10.1091/mbc.e21-04-0219 · Cited by 7 · see citing works
Al-Abdallah, A., Jahanbani, I., Ali, R. H., Al-Brahim, N., Prasanth, J., Al-Shammary, B., & Al‐Bader, M. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1080008 · Cited by 6 · see citing works
Ayama-Canden, S., Tondo, R., Piñeros, L., Ninane, N., Demazy, C., Dieu, M., Fattaccioli, A., Sauvage, A., Tabarrant, T., Lucas, S., et al. (2023) · Cell Communication and Signaling · doi:10.1186/s12964-023-01340-9 · Cited by 5 · see citing works
Cheng, J., Ji, D., Ma, J., Zhang, Q., Zhang, W., & Yang, L. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1367159 · Cited by 2 · see citing works
Self-citationChang, J., Alenizi, S., Milioli, H. H., Lay, W., Pounraj, S., Li, Y., Shiferaw, M. S., Beheshti, E. H., & Kovačević, Ž. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.15.682724
Ayama-Canden, S., Tondo, R., Piñeros, L., Ninane, N., Demazy, C., Dieu, M., Fattaccioli, A., Sauvage, A., Tabarrant, T., Lucas, S., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26633928
Chang, J., Alenizi, S., Milioli, H. H., Lay, W., Pounraj, S., Li, Y., Sisay, M., Hosseini-Beheshti, E., & Kovačević, Ž. (2026) · Journal of Extracellular Vesicles · doi:10.1002/jev2.70334
Cytokinesis Arrest-induced Binucleation of Macrophages Produces Highly Efficient EfferocytesPreprint
Wu, X., Wang, Z., Xue, C., Li, F., Yue, J., Shern, T., Liu, W., Cui, J., Wu, C. W., Kissner, M., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.08.10.731793
- Authors
- Sun, S., Zhou, X., Zhang, W., Gallick, G. E., & Kuang, J.
- Affiliations
- The University of Texas MD Anderson Cancer Center (US)
- Beijing Normal University (CN)
- Corresponding author
- Sun, Sheng
- Zhou, Xi
- Kuang, Jian
- Venue
- Biochemical Journal
- Publisher
- Portland Press Ltd.
- Published
- 2015-03-06
- Volume
- 466
- Issue
- 3
- Pages
- 475-487
- ISSN
- 0264-6021 (ISSN-L)
- 1470-8728
- PMC
- PMC4495973
- OpenAlex
- W2043952539
- Cited by
- 37
- References
- 54
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 3 · 2023: 2 · 2022: 3 · 2021: 4 · 2020: 3 · 2019: 4 · 2018: 2 · 2017: 3 · 2016: 9 · 2015: 1
- FWCI
- 2.16
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biochemical Journal (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (CA-16672, 1 RO1 CA93941, R01CA093941, P30CA016672)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- Alix, ESCRT-III, epidermal growth factor receptor, receptor degradation, Bro1 domain, V domain, ERK1/2 activation, receptor internalization, lysosomal degradation
- MeSH terms
- Calcium-Binding Proteins, Epidermal Growth Factor, Humans, Cell Cycle Proteins, Ubiquitination, Endosomal Sorting Complexes Required for Transport, Multivesicular Bodies, HEK293 Cells, ErbB Receptors
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