The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.
Rab10 regulates tubular endosome formation through KIF13A and KIF13B motors
Abstract
Recycling endosomes are stations that sort endocytic cargoes to their appropriate destinations. Tubular endosomes have been characterized as a recycling endosomal compartment for clathrin-independent cargoes. However, the molecular mechanism by which tubular endosome formation is regulated is poorly understood. In this study, we identified Rab10 as a novel protein localized at tubular endosomes by using a comprehensive localization screen of EGFP-tagged Rab small GTPases. Knockout of Rab10 completely abolished tubular endosomal structures in HeLaM cells. We also identified kinesin motors KIF13A and KIF13B as novel Rab10-interacting proteins by means of in silico screening. The results of this study demonstrated that both the Rab10-binding homology domain and the motor domain of KIF13A are required for Rab10-positive tubular endosome formation. Our findings provide insight into the mechanism by which the Rab10–KIF13A (or KIF13B) complex regulates tubular endosome formation. This article has an associated First Person interview with the first author of the paper.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
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?
RAB8A and RAB10 colocalize to a perinuclear tubular endocytic recycling compartment.
“This is consistent with their colocalization to a perinuclear tubular endocytic recycling compartment [37,38,39,40]”
From Distinct Roles for RAB10 and RAB29 in Pathogenic LRRK2-Mediated Endolysosomal Trafficking Alterations (2020) · cites this paper as [40]
RAB10 is widely expressed in peripheral tissues and brain, present in all cell types, and localized to a tubular perinuclear endocytic recycling compartment partially overlapping with RAB8A.
“It is widely expressed in peripheral tissues as well as in the brain, where it is present in all cell types [36], and localized to a tubular perinuclear endocytic recycling compartment partially overlapping with RAB8A [37,38,39,40].”
From Distinct Roles for RAB10 and RAB29 in Pathogenic LRRK2-Mediated Endolysosomal Trafficking Alterations (2020) · cites this paper as [40]
The study extended the known Retromer regulators to include DENND4A and DENND4C, TBC1D13, and a TBC1D1/TBC1D4 heterodimer, establishing mechanistic links between Retromer and the switching of RAB10 and RAB35.
“We have now extended these regulators to include DENND4A and DENND4C, TBC1D13, and a TBC1D1/TBC1D4 heterodimer, and in so doing, established mechanistic links between Retromer and the switching of RAB10 and RAB35; two RAB GTPases previously linked to the regulation of endosomal cargo recycling85,88–90,92,96,101,121,122.”
From Mapping of endosomal proximity proteomes reveals Retromer as a hub for RAB GTPase regulation (2025) · cites this paper as [90]
Activation of RAB10 is heavily implicated in general endosomal cargo recycling.
“Activation of RAB10 is heavily implicated in general endosomal cargo recycling85–93”
From Mapping of endosomal proximity proteomes reveals Retromer as a hub for RAB GTPase regulation (2025) · cites this paper as [90]
Citations
Cites
Rab GTPases as coordinators of vesicle traffic
Stenmark, H. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2728 · Cited by 3,413
Ishida, M., Ohbayashi, N., & Fukuda, M. (2015) · Scientific Reports · doi:10.1038/srep08238 · Cited by 49
Self-citation
Flagged first, then by citations
Research works printed but not linked: 70
- Babbey, 2006, Rab10 regulates membrane transport through early endosomes of polarized Madin-Darby canine kidney cells, Mol. Biol. Cell, 17, 3156, 10.1091/mbc.e05-08-0799 · DOI · Paper page
- Barr, 2013, Rab GTPases and membrane identity: causal or inconsequential?, J. Cell Biol., 202, 191, 10.1083/jcb.201306010 · DOI
- Bruno, 2016, SEC16A is a RAB10 effector required for insulin-stimulated GLUT4 trafficking in adipocytes, J. Cell Biol., 214, 61, 10.1083/jcb.201509052 · DOI
- Caplan, 2002, A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane, EMBO J., 21, 2557, 10.1093/emboj/21.11.2557 · DOI · Paper page
- Chaineau, 2013, Rab35: GEFs, GAPs and effectors, Traffic, 14, 1109, 10.1111/tra.12096 · DOI · Paper page
- Chavrier, 1990, Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments, Cell, 62, 317, 10.1016/0092-8674(90)90369-P · DOI · Paper page
- Chen, 2012, Rab10 and myosin-Va mediate insulin-stimulated GLUT4 storage vesicle translocation in adipocytes, J. Cell Biol., 198, 545, 10.1083/jcb.201111091 · DOI
- Chen, 2017, Segregation in the Golgi complex precedes export of endolysosomal proteins in distinct transport carriers, J. Cell Biol., 216, 4141, 10.1083/jcb.201707172 · DOI · Paper page
- Condon, 2018, Macropinosome formation by tent pole ruffling in macrophages, J. Cell Biol., 217, 3873, 10.1083/jcb.201804137 · DOI
- Delevoye, 2014, Recycling endosome tubule morphogenesis from sorting endosomes requires the kinesin motor KIF13A, Cell Rep., 6, 445, 10.1016/j.celrep.2014.01.002 · DOI
- Deng, 2014, JIP1 mediates anterograde transport of Rab10 cargos during neuronal polarization, J. Neurosci., 34, 1710, 10.1523/JNEUROSCI.4496-13.2014 · DOI · Paper page
- Doherty, 2009, Mechanisms of endocytosis, Annu. Rev. Biochem., 78, 857, 10.1146/annurev.biochem.78.081307.110540 · DOI · Paper page
- Du, 2016, Kinesin 1 drives autolysosome tubulation, Dev. Cell, 37, 326, 10.1016/j.devcel.2016.04.014 · DOI
- Dutta, 2015, Sorting of clathrin-independent cargo proteins depends on Rab35 delivered by clathrin-mediated endocytosis, Traffic, 16, 994, 10.1111/tra.12302 · DOI
- English, 2013, Rab10 GTPase regulates ER dynamics and morphology, Nat. Cell Biol., 15, 169, 10.1038/ncb2647 · DOI · Paper page
- Evans, 2003, Rab23, a negative regulator of hedgehog signaling, localizes to the plasma membrane and the endocytic pathway, Traffic, 4, 869, 10.1046/j.1600-0854.2003.00141.x · DOI
- Eyster, 2009, Discovery of new cargo proteins that enter cells through clathrin-independent endocytosis, Traffic, 10, 590, 10.1111/j.1600-0854.2009.00894.x · DOI
- Faire, 1999, E-MAP-115 (ensconsin) associates dynamically with microtubules in vivo and is not a physiological modulator of microtubule dynamics, J. Cell Sci., 112, 4243, 10.1242/jcs.112.23.4243 · DOI · Paper page
- Fukuda, 2008, Membrane traffic in the secretory pathway: regulation of secretory vesicle traffic by Rab small GTPases, Cell. Mol. Life Sci., 65, 2801, 10.1007/s00018-008-8351-4 · DOI
- Fukuda, 1999, A novel alternatively spliced variant of synaptotagmin VI lacking a transmembrane domain: implications for distinct functions of the two isoforms, J. Biol. Chem., 274, 31428, 10.1074/jbc.274.44.31428 · DOI
- Fukuda, 1999, Conserved N-terminal cysteine motif is essential for homo- and heterodimer formation of synaptotagmins III, V, VI, and X, J. Biol. Chem., 274, 31421, 10.1074/jbc.274.44.31421 · DOI
- Fukuda, 2002, Slac2-a/melanophilin, the missing link between Rab27 and myosin Va: implications of a tripartite protein complex for melanosome transport, J. Biol. Chem., 277, 12432, 10.1074/jbc.C200005200 · DOI
- Fukuda, 2008, Large scale screening for novel Rab effectors reveals unexpected broad Rab binding specificity, Mol. Cell. Proteomics, 7, 1031, 10.1074/mcp.M700569-MCP200 · DOI
- Gong, 2007, Identification and characterization of a new class of trafficking motifs for controlling clathrin-independent internalization and recycling, J. Biol. Chem., 282, 13087, 10.1074/jbc.M700767200 · DOI · Paper page
- Grant, 2009, Pathways and mechanisms of endocytic recycling, Nat. Rev. Mol. Cell Biol., 10, 597, 10.1038/nrm2755 · DOI · Paper page
- Hattula, 2006, Characterization of the Rab8-specific membrane traffic route linked to protrusion formation, J. Cell Sci., 119, 4866, 10.1242/jcs.03275 · DOI
- Homma, 2016, Rabin8 regulates neurite outgrowth in both GEF activity-dependent and -independent manners, Mol. Biol. Cell, 27, 2107, 10.1091/mbc.E16-02-0091 · DOI · Paper page
- Hunziker, 1998, Rab17 localizes to recycling endosomes and regulates receptor-mediated transcytosis in epithelial cells, J. Biol. Chem., 273, 15734, 10.1074/jbc.273.25.15734 · DOI
- Itoh, 2006, Screening for target Rabs of TBC (Tre-2/Bub2/Cdc16) domain-containing proteins based on their Rab-binding activity, Genes Cells, 11, 1023, 10.1111/j.1365-2443.2006.00997.x · DOI
- Itoh, 2008, Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation, Mol. Biol. Cell, 19, 2916, 10.1091/mbc.e07-12-1231 · DOI
- Katoh, 2015, Architectures of multisubunit complexes revealed by a visible immunoprecipitation assay using fluorescent fusion proteins, J. Cell Sci., 128, 2351, 10.1242/jcs.168740 · DOI
- Kauppi, 2002, The small GTPase Rab22 interacts with EEA1 and controls endosomal membrane trafficking, J. Cell Sci., 115, 899, 10.1242/jcs.115.5.899 · DOI
- Kuki, 2017, Quantitative confocal imaging method for analyzing cellulose dynamics during cell wall regeneration in Arabidopsis mesophyll protoplasts, Plant Direct, 1, e00021, 10.1002/pld3.21 · DOI
- Kuroda, 2005, Identification and biochemical analysis of Slac2-c/MyRIP as a Rab27A-, myosin Va/VIIa-, and actin-binding protein, Methods Enzymol., 403, 431, 10.1016/S0076-6879(05)03038-7 · DOI
- Liu, 2013, Myosin Vb controls biogenesis of post-Golgi Rab10 carriers during axon development, Nat. Commun., 4, 2005, 10.1038/ncomms3005 · DOI
- Lv, 2015, Targeted disruption of Rab10 causes early embryonic lethality, Protein Cell, 6, 463, 10.1007/s13238-015-0150-8 · DOI · Paper page
- Maldonado-Báez, 2013, Microtubule-dependent endosomal sorting of clathrin-independent cargo by Hook1, J. Cell Biol., 201, 233, 10.1083/jcb.201208172 · DOI
- Maxfield, 2004, Endocytic recycling, Nat. Rev. Mol. Cell Biol., 5, 121, 10.1038/nrm1315 · DOI · Paper page
- Mayor, 2007, Pathways of clathrin-independent endocytosis, Nat. Rev. Mol. Cell Biol., 8, 603, 10.1038/nrm2216 · DOI · Paper page
- Miki, 2005, Analysis of the kinesin superfamily: insights into structure and function, Trends Cell Biol., 15, 467, 10.1016/j.tcb.2005.07.006 · DOI
- Morita, 2000, Plat-E: an efficient and stable system for transient packaging of retroviruses, Gene Ther., 7, 1063, 10.1038/sj.gt.3301206 · DOI
- Mrozowska, 2016, Regulation of podocalyxin trafficking by Rab small GTPases in 2D and 3D epithelial cell cultures, J. Cell Biol., 213, 355, 10.1083/jcb.201512024 · DOI
- Nakajo, 2016, EHBP1L1 coordinates Rab8 and Bin1 to regulate apical-directed transport in polarized epithelial cells, J. Cell Biol., 212, 297, 10.1083/jcb.201508086 · DOI
- Navarro Negredo, 2017, Contribution of the clathrin adaptor AP-1 subunit µ1 to acidic cluster protein sorting, J. Cell Biol., 216, 2927, 10.1083/jcb.201602058 · DOI · Paper page
- Ohbayashi, 2012, Melanoregulin regulates retrograde melanosome transport through interaction with the RILP–p150Glued complex in melanocytes, J. Cell Sci., 125, 1508, 10.1242/jcs.094185 · DOI
- Peränen, 2011, Rab8 GTPase as a regulator of cell shape, Cytoskeleton, 68, 527, 10.1002/cm.20529 · DOI
- Pettersen, 2004, UCSF Chimera – a visualization system for exploratory research and analysis, J. Comput. Chem., 25, 1605, 10.1002/jcc.20084 · DOI
- Pfeffer, 2013, Rab GTPase regulation of membrane identity, Curr. Opin. Cell Biol., 25, 414, 10.1016/j.ceb.2013.04.002 · DOI
- Radhakrishna, 1997, ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway, J. Cell Biol., 139, 49, 10.1083/jcb.139.1.49 · DOI
- Rahajeng, 2012, MICAL-L1 is a tubular endosomal membrane hub that connects Rab35 and Arf6 with Rab8a, Traffic, 13, 82, 10.1111/j.1600-0854.2011.01294.x · DOI · Paper page
- Rai, 2016, bMERB domains are bivalent Rab8 family effectors evolved by gene duplication, eLife, 5, e18675, 10.7554/eLife.18675 · DOI
- Sabharanjak, 2002, GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway, Dev. Cell, 2, 411, 10.1016/S1534-5807(02)00145-4 · DOI
- Saitoh, 2003, TWEAK induces NF-κB2 p100 processing and long lasting NF-κB activation, J. Biol. Chem., 278, 36005, 10.1074/jbc.M304266200 · DOI
- Sakane, 2012, Rab13 small G protein and junctional Rab13-binding protein (JRAB) orchestrate actin cytoskeletal organization during epithelial junctional development, J. Biol. Chem., 287, 42455, 10.1074/jbc.M112.383653 · DOI
- Šali, 1993, Comparative protein modelling by satisfaction of spatial restraints, J. Mol. Biol., 234, 779, 10.1006/jmbi.1993.1626 · DOI · Paper page
- Scita, 2010, The endocytic matrix, Nature, 463, 464, 10.1038/nature08910 · DOI
- Shakya, 2018, Rab22A recruits BLOC-1 and BLOC-2 to promote the biogenesis of recycling endosomes, EMBO Rep., 19, e45918, 10.15252/embr.201845918 · DOI
- Sharma, 2009, MICAL-L1 links EHD1 to tubular recycling endosomes and regulates receptor recycling, Mol. Biol. Cell, 20, 5181, 10.1091/mbc.e09-06-0535 · DOI · Paper page
- Simpson, 2004, A role for the small GTPase Rab21 in the early endocytic pathway, J. Cell Sci., 117, 6297, 10.1242/jcs.01560 · DOI
- Solis, 2013, Reggies/flotillins interact with Rab11a and SNX4 at the tubulovesicular recycling compartment and function in transferrin receptor and E-cadherin trafficking, Mol. Biol. Cell, 24, 2689, 10.1091/mbc.e12-12-0854 · DOI
- Soppina, 2014, Dimerization of mammalian kinesin-3 motors results in superprocessive motion, Proc. Natl. Acad. Sci. USA, 111, 5562, 10.1073/pnas.1400759111 · DOI
- Ullrich, 1996, Rab11 regulates recycling through the pericentriolar recycling endosome, J. Cell Biol., 135, 913, 10.1083/jcb.135.4.913 · DOI · Paper page
- Vazirani, 2016, Disruption of adipose Rab10-dependent insulin signaling causes hepatic insulin resistance, Diabetes, 65, 1577, 10.2337/db15-1128 · DOI
- Wang, 2011, Lgl1 activation of Rab10 promotes axonal membrane trafficking underlying neuronal polarization, Dev. Cell, 21, 431, 10.1016/j.devcel.2011.07.007 · DOI
- Wang, 2016, RAB-10 promotes EHBP-1 bridging of filamentous actin and tubular recycling endosomes, PLoS Genet., 12, e1006093, 10.1371/journal.pgen.1006093 · DOI · Paper page
- Weigert, 2004, Rab22a regulates the recycling of membrane proteins internalized independently of clathrin, Mol. Biol. Cell, 15, 3758, 10.1091/mbc.e04-04-0342 · DOI
- Yamamura, 2008, The interaction of JRAB/MICAL-L2 with Rab8 and Rab13 coordinates the assembly of tight junctions and adherens junctions, Mol. Biol. Cell, 19, 971, 10.1091/mbc.e07-06-0551 · DOI
- Zacchi, 1998, Rab17 regulates membrane trafficking through apical recycling endosomes in polarized epithelial cells, J. Cell Biol., 140, 1039, 10.1083/jcb.140.5.1039 · DOI
- Zhang, 2017, Rab10 disruption results in delayed OPC maturation, Cell. Mol. Neurobiol., 37, 1303, 10.1007/s10571-017-0465-5 · DOI · Paper page
- Zhou, 2013, A molecular motor, KIF13A, controls anxiety by transporting the serotonin type 1A receptor, Cell Rep., 3, 509, 10.1016/j.celrep.2013.01.014 · DOI
Cited by
Sorted by citations
Rivero-Ríos, P., Romo-Lozano, M., Fernández, B., Fdez, E., & Hilfiker, S. (2020) · Cells · doi:10.3390/cells9071719 · Cited by 38
Differential effects of FcRn antagonists on the subcellular trafficking of FcRn and albumin
Ma, G., Crowley, A. R., Heyndrickx, L., Rogiers, I., Parthoens, E., Van Santbergen, J., Ober, R. J., Bobkov, V., de Haard, H., Ulrichts, P., et al. (2024) · JCI Insight · doi:10.1172/jci.insight.176166 · Cited by 28
Rab7B/42 is functionally involved in protein degradation on melanosomes in keratinocytes
Marubashi, S., & Fukuda, M. (2020) · Cell Structure and Function · doi:10.1247/csf.19039 · Cited by 25
Self-citationKhan, T. G., Ginsburg, D., & Emmer, B. T. (2022) · Journal of Lipid Research · doi:10.1016/j.jlr.2022.100248 · Cited by 21
Mapping of endosomal proximity proteomes reveals Retromer as a hub for RAB GTPase regulation
Antón-Plágaro, C., Chen, K.-E., Guo, Q., Liu, M., Evans, A. J., Lewis, P. A., Heesom, K. J., Wilkinson, K. A., Collins, B. M., & Cullen, P. J. (2025) · Nature Communications · doi:10.1038/s41467-025-61802-1 · Cited by 14
Cellular and subcellular localization of Rab10 and phospho-T73 Rab10 in the mouse and human brain
Singh, V., Menard, M. A., Serrano, G. E., Beach, T. G., Zhao, H. T., Riley-DiPaolo, A., Subrahmanian, N., LaVoie, M. J., & Volpicelli-Daley, L. A. (2023) · Acta Neuropathologica Communications · doi:10.1186/s40478-023-01704-9 · Cited by 9
Potential Roles of SNX17, Rab11, and Rab5 in LDLR Recycling
Zhao, X., Long, S., Zhu, M., Hao, H., Liao, Y., Zhang, C., & Liu, Z. (2025) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.125.322498 · Cited by 8
Metadata
- Authors
- Etoh, K., & Fukuda, M.
- Affiliations
- Graduate School of Life Sciences, Tohoku University Laboratory of Membrane Trafficking Mechanisms, Department of Integrative Life Sciences , , Aobayama, Aoba-ku, Sendai, Miyagi 980-8578 ,
- ORCID
- Fukuda, Mitsunori
- Venue
- Journal of Cell Science
- Publisher
- The Company of Biologists
- Published
- 2019-02-19
- Volume
- 132
- Issue
- 5
- ISSN
- 1477-9137
- 0021-9533
- Cited by
- 106
- References
- 2
- Language
- en
- Funders
- Ministry of Education, Culture, Sports, Science and Technology (15H04367, 17H05682)
- Japan Science and Technology Agency (JPMJCR17H4)
- Japan Society for the Promotion of Science
- Tohoku University
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