Pericentrosomal targeting of Rab6 secretory vesicles by Bicaudal-D-related protein 1 (BICDR-1) regulates neuritogenesis
Open accessAbstract
Membrane and secretory trafficking are essential for proper neuronal development. However, the molecular mechanisms that organize secretory trafficking are poorly understood. Here, we identify Bicaudal-D-related protein 1 (BICDR-1) as an effector of the small GTPase Rab6 and key component of the molecular machinery that controls secretory vesicle transport in developing neurons. BICDR-1 interacts with kinesin motor Kif1C, the dynein/dynactin retrograde motor complex, regulates the pericentrosomal localization of Rab6-positive secretory vesicles and is required for neural development in zebrafish. BICDR-1 expression is high during early neuronal development and strongly declines during neurite outgrowth. In young neurons, BICDR-1 accumulates Rab6 secretory vesicles around the centrosome, restricts anterograde secretory transport and inhibits neuritogenesis. Later during development, BICDR-1 expression is strongly reduced, which permits anterograde secretory transport required for neurite outgrowth. These results indicate an important role for BICDR-1 as temporal regulator of secretory trafficking during the early phase of neuronal differentiation.
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During neuronal development, BCDR-1 decreases significantly.
“During neuronal development, BCDR-1 decreases significantly (Schlager et al., 2010).”
From The Rab6-regulated KIF1C kinesin motor domain contributes to Golgi organization (2015) · cites this paper as Schlager et al., 2010
Additional Rab6A effectors BICDR-1 and myosin IIA interact at least indirectly with KIF1C.
“In addition to the direct interaction between Rab6A and KIF1C described here, additional Rab6A effectors have been reported to interact at least indirectly with KIF1C. These include BICDR-1, which interacts in lysates and by yeast two-hybrid at the C-terminus of KIF1C (Schlager et al., 2010), and myosin IIA, which in lysates, interacts in the region before the C-terminus (residues 713–811; Kopp et”
From The Rab6-regulated KIF1C kinesin motor domain contributes to Golgi organization (2015) · cites this paper as Schlager et al., 2010
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Cites
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
The Mechanisms of Vesicle Budding and Fusion
Bonifacino, J. S., & Glick, B. S. (2004) · Cell · doi:10.1016/s0092-8674(03)01079-1 · Cited by 1,863 · see citing works
Microtubule assembly, organization and dynamics in axons and dendrites
Conde, C., & Cáceres, A. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2631 · Cited by 1,086 · see citing works
The Mechanism of Ca2+-Dependent Regulation of Kinesin-Mediated Mitochondrial Motility
Wang, X., & Schwarz, T. L. (2009) · Cell · doi:10.1016/j.cell.2008.11.046 · Cited by 871 · see citing works
Molecular motors and mechanisms of directional transport in neurons
Hirokawa, N., & Takemura, R. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1624 · Cited by 830 · see citing works
Miro1 Is a Calcium Sensor for Glutamate Receptor-Dependent Localization of Mitochondria at Synapses
MacAskill, A. F., Rinholm, J. E., Twelvetrees, A. E., Arancibia‐Cárcamo, I. L., Muir, J., Fransson, Å., Aspenström, P., Attwell, D., & Kittler, J. T. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.030 · Cited by 677 · see citing works
Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity
Jaworski, J., Kapitein, L. C., Gouveia, S. M., Dortland, B. R., Wulf, P. S., Grigoriev, I., Camera, P., Spangler, S. A., Di Stefano, P., Demmers, J., et al. (2009) · Neuron · doi:10.1016/j.neuron.2008.11.013 · Cited by 643 · see citing works
Self-citationRegulators of the cytoplasmic dynein motor
Kardon, J. R., & Vale, R. D. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2804 · Cited by 603 · see citing works
Bidirectional transport along microtubules
Welte, M. A. (2004) · Current Biology · doi:10.1016/j.cub.2004.06.045 · Cited by 577 · see citing works
Interaction of a Golgi-Associated Kinesin-Like Protein with Rab6
Échard, A., Jollivet, F., Martinez, O., Lacapère, J.-J., Rousselet, A., Janoueix‐Lerosey, I., & Goud, B. (1998) · Science · doi:10.1126/science.279.5350.580 · Cited by 518 · see citing works
Intracellular Transport and Kinesin Superfamily Proteins, KIFs: Structure, Function, and Dynamics
Hirokawa, N., & Noda, Y. (2008) · Physiological Reviews · doi:10.1152/physrev.00023.2007 · Cited by 510 · see citing works
Johansson, M., Rocha, N., Zwart, W., Jordens, I., Janssen, L., Kuijl, C., Olkkonen, V. M., & Neefjes, J. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200606077 · Cited by 505 · see citing works
Matanis, T., Akhmanova, A., Wulf, P., Del Nery, E., Weide, T., Stepanova, T., Galjart, N., Grosveld, F., Goud, B., De Zeeuw, C. I., et al. (2002) · Nature Cell Biology · doi:10.1038/ncb891 · Cited by 413 · see citing works
Self-citationRab6 regulates transport and targeting of exocytotic carriers
Grigoriev, I., Splinter, D., Keijzer, N., Wulf, P. S., Demmers, J., Ohtsuka, T., Modesti, M., Maly, I. V., Grosveld, F., Hoogenraad, C. C., et al. (2007) · Developmental Cell · doi:10.1016/j.devcel.2007.06.010 · Cited by 361 · see citing works
Self-citationColin, E., Zala, D., Liot, G., Rangone, H., Borrell-Pagés, M., Li, X., Saudou, F., & Humbert, S. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.133 · Cited by 360 · see citing works
Membrane traffic in the secretory pathway
Fukuda, M. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8351-4 · Cited by 359 · see citing works
Self-citationSecretory Mechanisms in Cell-Mediated Cytotoxicity
Stinchcombe, J. C., & Griffiths, G. M. (2007) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.23.090506.123521 · Cited by 313 · see citing works
Hoogenraad, C. C., Akhmanova, A. S., Howell, S. A., Dortland, B. R., Zeeuw, C. I. D., Willemsen, R., Visser, P., Grosveld, F. G., & Galjart, N. (2001) · The EMBO Journal · doi:10.1093/emboj/20.15.4041 · Cited by 312 · see citing works
Self-citationDynactin is required for bidirectional organelle transport
Deacon, S. W., Serpinskaya, A. S., Vaughan, P. S., Fanárraga, M. L., Vernos, I., Vaughan, K. T., & Gelfand, V. I. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200210066 · Cited by 311 · see citing works
Microtubule motors at the intersection of trafficking and transport
Caviston, J. P., & Holzbaur, E. L. F. (2006) · Trends in Cell Biology · doi:10.1016/j.tcb.2006.08.002 · Cited by 303 · see citing works
Conserved signals and machinery for RNA transport in Drosophila oogenesis and embryogenesis
Bullock, S. L., & Ish‐Horowicz, D. (2001) · Nature · doi:10.1038/414611a · Cited by 269 · see citing works
Plasma membrane expansion: a neuron's Herculean task
Pfenninger, K. H. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2593 · Cited by 257 · see citing works
Swan, A., Nguyen, T. N., & Suter, B. (1999) · Nature Cell Biology · doi:10.1038/15680 · Cited by 219 · see citing works
Bicaudal D induces selective dynein‐mediated microtubule minus end‐directed transport
Hoogenraad, C. C., Wulf, P. S., Schiefermeier-Mach, N., Stepanova, T., Galjart, N., Small, J. V., Grosveld, F. G., Zeeuw, C. I. D., & Akhmanova, A. S. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg592 · Cited by 219 · see citing works
Self-citationThe centrosome in neuronal development
Higginbotham, H., & Gleeson, J. G. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.04.001 · Cited by 218 · see citing works
Egalitarian is a selective RNA-binding protein linking mRNA localization signals to the dynein motorPreprint
Dienstbier, M., Boehl, F., Li, X., et al. (2009) · Genes & Development · doi:10.1101/gad.531009 · Cited by 214 · see citing works
The Rab6 GTPase Regulates Recruitment of the Dynactin Complex to Golgi Membranes
Short, B., Preisinger, C., Schaletzky, J., Kopajtich, R., & Barr, F. A. (2002) · Current Biology · doi:10.1016/s0960-9822(02)01221-6 · Cited by 210 · see citing works
Egalitarian binds dynein light chain to establish oocyte polarity and maintain oocyte fate
Navarro, C., Puthalakath, H., Adams, J. M., Strasser, A., & Lehmann, R. (2004) · Nature Cell Biology · doi:10.1038/ncb1122 · Cited by 200 · see citing works
Barkus, R. V., Klyachko, O., Horiuchi, D., Dickson, B. J., & Saxton, W. M. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-03-0261 · Cited by 185 · see citing works
Secretory Outposts for the Local Processing of Membrane Cargo in Neuronal Dendrites
Hanus, C., & Ehlers, M. (2008) · Traffic · doi:10.1111/j.1600-0854.2008.00775.x · Cited by 116 · see citing works
Alternative Splicing of the HumanRab6AGene Generates Two Close but Functionally Different Isoforms
Échard, A., Opdam, F. J. M., de Leeuw, H. P. J. C., Jollivet, F., Savelkoul, P. J. M., Hendriks, W. J. A. J., Voorberg, J., Goud, B., & Fransen, J. A. M. (2000) · Molecular Biology of the Cell · doi:10.1091/mbc.11.11.3819 · Cited by 115 · see citing works
Dense Core Vesicle Dynamics in Caenorhabditis elegans Neurons and the Role of Kinesin UNC‐104
Zahn, T. R., Angleson, J. K., MacMorris, M., Domke, E., Hutton, J. F., Schwartz, C., & Hutton, J. C. (2004) · Traffic · doi:10.1111/j.1600-0854.2004.00195.x · Cited by 109 · see citing works
Zakharenko, S. S., & Popov, S. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.143.4.1077 · Cited by 105 · see citing works
Differentiated neurons retain the capacity to generate axons from dendrites
Bradke, F., & Dotti, C. G. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00807-1 · Cited by 103 · see citing works
Basic mechanisms for recognition and transport of synaptic cargos
Schlager, M. A., & Hoogenraad, C. C. (2009) · Molecular Brain · doi:10.1186/1756-6606-2-25 · Cited by 94 · see citing works
Self-citationErez, H., Malkinson, G., Prager‐Khoutorsky, M., Zeeuw, C. I. D., Hoogenraad, C. C., & Spira, M. E. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200607098 · Cited by 92 · see citing works
Self-citationNull alleles reveal novel requirements for Bic-D during Drosophila oogenesis and zygotic development
Ran, B., Bopp, R., & Suter, B. (1994) · Development · doi:10.1242/dev.120.5.1233 · Cited by 88 · see citing works
Vesicular Trafficking of Semaphorin 3A is Activity‐Dependent and Differs Between Axons and Dendrites
de Wit, J., Toonen, R. F. G., Verhaagen, J., & Verhage, M. (2006) · Traffic · doi:10.1111/j.1600-0854.2006.00442.x · Cited by 82 · see citing works
Rab6 family proteins interact with the dynein light chain protein DYNLRB1
Wanschers, B. F. J., van de Vorstenbosch, R. A., Wijers, M., Wieringa, B., King, S. M., & Fransen, J. A. M. (2007) · Cell Motility and the Cytoskeleton · doi:10.1002/cm.20254 · Cited by 80 · see citing works
Matrix-Dependent Local Retention of Secretory Vesicle Cargo in Cortical Neurons
de Wit, J., Toonen, R. F. G., & Verhage, M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3931-08.2009 · Cited by 73 · see citing works
Rab6 mediates membrane organization and determinant localization duringDrosophilaoogenesis
Coutelis, J., & Ephrussi, A. (2007) · Development · doi:10.1242/dev.02821 · Cited by 72 · see citing works
A role for the Rab6B Bicaudal–D1 interaction in retrograde transport in neuronal cells
Wanschers, B. F. J., van de Vorstenbosch, R. A., Schlager, M. A., Splinter, D., Akhmanova, A. S., Hoogenraad, C. C., Wieringa, B., & Fransen, J. A. M. (2007) · Experimental Cell Research · doi:10.1016/j.yexcr.2007.05.032 · Cited by 71 · see citing works
Self-citationRab6 and the secretory pathway affect oocyte polarity inDrosophila
Januschke, J., Nicolas, E., Compagnon, J., et al. (2007) · Development · doi:10.1242/dev.008078 · Cited by 61 · see citing works
BicD-dependent localization processes: from Drosophilia development to human cell biology
Claußen, M., & Suter, B. (2005) · Annals of Anatomy - Anatomischer Anzeiger · doi:10.1016/j.aanat.2005.07.004 · Cited by 56 · see citing works
BicaudalD Actively Regulates Microtubule Motor Activity in Lipid Droplet Transport
Larsen, K. S., Xu, J., Cermelli, S., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003763 · Cited by 53 · see citing works
Zebrafish R‐cadherin (Cdh4) controls visual system development and differentiation
Clendenon, S. G., Kotradi, S. M., Shah, B. D., Chiappini-Williamson, C., Bell, L. N., Schmeiser, G., Chen, E., Liu, Q., & Marrs, J. A. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20431 · Cited by 51 · see citing works
Houalla, T., Vuong, D. H., Ruan, W., et al. (2004) · Mechanisms of Development · doi:10.1016/j.mod.2004.08.005 · Cited by 40 · see citing works
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The Rab6-regulated KIF1C kinesin motor domain contributes to Golgi organization
Lee, P. L., Ohlson, M. B., & Pfeffer, S. R. (2015) · eLife · doi:10.7554/elife.06029 · Cited by 65 · see citing works
Ishida, M., Ohbayashi, N., & Fukuda, M. (2015) · Scientific Reports · doi:10.1038/srep08238 · Cited by 49 · see citing works
Self-citationIshida, M., Ohbayashi, N., Maruta, Y., Ebata, Y., & Fukuda, M. (2012) · Journal of Cell Science · doi:10.1242/jcs.109314 · Cited by 49 · see citing works
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- Authors
- Schlager, M. A., Kapitein, L. C., Grigoriev, I., Burzynski, G. M., Wulf, P. S., Keijzer, N., de Graaff, E., Fukuda, M., Shepherd, I. T., Akhmanova, A., & Hoogenraad, C. C.
- Affiliations
- Erasmus MC (NL)
- Emory University (US)
- Tohoku University (JP)
- Corresponding author
- Hoogenraad, Casper C
- ORCID
- Venue
- The EMBO Journal
- Published
- 2010-04-01
- Volume
- 29
- Issue
- 10
- Pages
- 1637-1651
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC2876961
- OpenAlex
- W2029768388
- Cited by
- 165
- References
- 48
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 15 · 2023: 8 · 2022: 14 · 2021: 12 · 2020: 15 · 2019: 14 · 2018: 11 · 2017: 14 · 2016: 14 · 2015: 8 · 2014: 10 · 2013: 4 · 2012: 10
- FWCI
- 2.94
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- The EMBO Journal (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
- RePub (Erasmus University Rotterdam) (submittedVersion)
- Funders
- Japan Society for the Promotion of Science
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- Rab6, secretory vesicle transport, neurite outgrowth, neuronal differentiation, secretory trafficking, centrosome
- MeSH terms
- Animals, Brain, Cell Differentiation, Cell Membrane, Chlorocebus aethiops, Cytoskeletal Proteins, Humans, Kidney, Models, Biological, Neurons, Zebrafish, Kinesins, Centrosome, COS Cells, rab GTP-Binding Proteins, Adaptor Proteins, Vesicular Transport, Adaptor Proteins, Signal Transducing
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