Bicaudal-D regulates COPI-independent Golgi–ER transport by recruiting the dynein–dynactin motor complex (original) (raw)

Nature Cell Biology volume 4, pages 986–992 (2002)Cite this article

An Erratum to this article was published on 01 January 2003

Abstract

The small GTPase Rab6a is involved in the regulation of membrane traffic from the Golgi apparatus towards the endoplasmic reticulum (ER) in a coat complex coatomer protein I (COPI)-independent pathway1,2,3,4,5,6. Here, we used a yeast two-hybrid approach to identify binding partners of Rab6a. In particular, we identified the dynein–dynactin-binding protein Bicaudal-D1 (BICD1), one of the two mammalian homologues of Drosophila Bicaudal-D7,8,9,10. BICD1 and BICD2 colocalize with Rab6a on the _trans_-Golgi network (TGN) and on cytoplasmic vesicles, and associate with Golgi membranes in a Rab6-dependent manner. Overexpression of BICD1 enhances the recruitment of dynein–dynactin to Rab6a-containing vesicles. Conversely, overexpression of the carboxy-terminal domain of BICD, which can interact with Rab6a but not with cytoplasmic dynein, inhibits microtubule minus-end-directed movement of green fluorescent protein (GFP)–Rab6a vesicles and induces an accumulation of Rab6a and COPI-independent ER cargo in peripheral structures. These data suggest that coordinated action between Rab6a, BICD and the dynein–dynactin complex controls COPI-independent Golgi–ER transport.

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Acknowledgements

We thank I. G. Macara, S. R. Pfeffer, D. Gallwitz, E. G. Berger and H. P. Hauri for providing reagents. We also thank M. Rosing, K. Bilbilis, M. Koester, E. Ossendorf and A. Theil for experimental assistance. This research was supported by grants from the Netherlands Organisation for Scientific Research (ZonMw/900-00-001), the Erasmus University and grants from Fonds der Chemischen Industrie (FCI) and Deutsche Forschungsgemeinschaft (DFG) to A.B. This study contains major parts of the PhD thesis of T.M. T.M. is a fellow of the Graduiertenfoerderung of Nordrhein-Westfalen.

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Author notes

  1. Casper C. Hoogenraad
    Present address: Picower Center for Learning and Memory, Massachusetts Institute of Technology, 77 Massachusetts Avenue (E18-215), Cambridge, MA 02139, USA
  2. Theodoros Matanis and Anna Akhmanova: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Experimental Tumorbiology, University of Muenster, Badestrasse 9, Muenster, D-48149, Germany
    Theodoros Matanis, Thomas Weide & Angelika Barnekow
  2. Department of Neuroscience, Erasmus University Rotterdam, P.O. Box 1738, Rotterdam, 3000, DR, The Netherlands
    Phebe Wulf, Chris I. De Zeeuw & Casper C. Hoogenraad
  3. Department of Cell Biology and Genetics, Erasmus University Rotterdam, P.O. Box 1738, Rotterdam, 3000, DR, The Netherlands
    Anna Akhmanova, Tatiana Stepanova, Niels Galjart & Frank Grosveld
  4. UMR CNRS 144, Institut Curie, 26 rue d'Ulm, Paris, 75248, Cedex 05, France
    Elaine Del Nery & Bruno Goud

Authors

  1. Theodoros Matanis
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  2. Anna Akhmanova
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  3. Phebe Wulf
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  4. Elaine Del Nery
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  5. Thomas Weide
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  6. Tatiana Stepanova
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  7. Niels Galjart
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  8. Frank Grosveld
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  9. Bruno Goud
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  10. Chris I. De Zeeuw
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  11. Angelika Barnekow
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  12. Casper C. Hoogenraad
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Corresponding authors

Correspondence toAnna Akhmanova or Casper C. Hoogenraad.

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Supplementary information

Figure S1

Specificity of the #2293 and #2296 antibodies using immunofluorescence microscopy and colocalisation between BICD proteins and Golgi markers (JPG 239 kb)

Figure S2

Silencing of Rab6 in HeLa cells. (JPG 1160 kb)

Figure S3

BICD2-C causes peripheral accumulation of COPI-independent Golgi-ER cargo, but has no effect on GM130 and γ-adaptin (JPG 1126 kb)

Figure S4

BICD2-C has no effect on the microtubule network and induces no accumulation of dynein or dynactin. (JPG 713 kb)

Movie 1

GFP-Rab6A movement in HeLa cells (AVI 903 kb)

Movie 2

GFP-Rab6A movement in HeLa cells expressing BICD2-C (AVI 796 kb)

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Matanis, T., Akhmanova, A., Wulf, P. et al. Bicaudal-D regulates COPI-independent Golgi–ER transport by recruiting the dynein–dynactin motor complex.Nat Cell Biol 4, 986–992 (2002). https://doi.org/10.1038/ncb891

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