Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

Science 314 (5802): 1135-1139

Copyright © 2006 by the American Association for the Advancement of Science

Sara Endosomes and the Maintenance of Dpp Signaling Levels Across Mitosis

Christian Bökel,1* Anja Schwabedissen,1 Eugeni Entchev,1 Olivier Renaud,1{dagger} Marcos González-Gaitán1,2{ddagger}

Abstract: During development, cells acquire positional information by reading the concentration of morphogens. In the developing fly wing, a gradient of the transforming growth factor–ß (TGF-ß)–type morphogen decapentaplegic (Dpp) is transduced into a gradient of concentration of the phosphorylated form of the R-Smad transcription factor Mad. The endosomal protein Sara (Smad anchor for receptor activation) recruits R-Smads for phosphorylation by the type I TGF-ß receptor. We found that Sara, Dpp, and its type I receptor Thickveins were targeted to a subpopulation of apical endosomes in the developing wing epithelial cells. During mitosis, the Sara endosomes and the receptors therein associated with the spindle machinery to segregate into the two daughter cells. Daughter cells thereby inherited equal amounts of signaling molecules and thus retained the Dpp signaling levels of the mother cell.

1 Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, Germany.
2 Department of Biochemistry and Department of Molecular Biology, Geneva University, Sciences II, 30 Quai Ernest-Ansermet, 1211 Geneva 4, Switzerland.

* *Present address: Biotechnological Center, Dresden University of Technology, Tatzberg 47, 01307 Dresden, Germany.

{dagger} Present address: Automation Project, Plateforme d'Imagerie Dynamique, Institut Pasteur, 25–28, rue du Docteur Roux, 75015 Paris, France.

{ddagger} To whom correspondence should be addressed. E-mail: marcos.gonzalez{at}biochem.unige.ch


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Endocytosis and Signaling during Development.
C. Bokel and M. Brand (2014)
Cold Spring Harb Perspect Biol 6, a017020
   Abstract »    Full Text »    PDF »
Effects of Membrane Trafficking on Signaling by Receptor Tyrosine Kinases.
M. Miaczynska (2013)
Cold Spring Harb Perspect Biol 5, a009035
   Abstract »    Full Text »    PDF »
Quantitative Imaging of Morphogen Gradients in Drosophila Imaginal Discs.
A. Kicheva, L. Holtzer, O. Wartlick, T. Schmidt, and M. Gonzalez-Gaitan (2013)
Cold Spring Harb Protoc 2013, pdb.top074237
   Abstract »    Full Text »    PDF »
Relay of retrograde synaptogenic signals through axonal transport of BMP receptors.
R. B. Smith, J. B. Machamer, N. C. Kim, T. S. Hays, and G. Marques (2012)
J. Cell Sci. 125, 3752-3764
   Abstract »    Full Text »    PDF »
Coated Pit-mediated Endocytosis of the Type I Transforming Growth Factor-{beta} (TGF-{beta}) Receptor Depends on a Di-leucine Family Signal and Is Not Required for Signaling.
K. E. Shapira, A. Gross, M. Ehrlich, and Y. I. Henis (2012)
J. Biol. Chem. 287, 26876-26889
   Abstract »    Full Text »    PDF »
Distinct intracellular motifs of Delta mediate its ubiquitylation and activation by Mindbomb1 and Neuralized.
A. Daskalaki, N. A. Shalaby, K. Kux, G. Tsoumpekos, G. D. Tsibidis, M. A. T. Muskavitch, and C. Delidakis (2011)
J. Cell Biol. 195, 1017-1031
   Abstract »    Full Text »    PDF »
Apical-basal polarity in Drosophila neuroblasts is independent of vesicular trafficking.
N. Halbsgut, K. Linnemannstons, L. I. Zimmermann, and A. Wodarz (2011)
Mol. Biol. Cell 22, 4373-4379
   Abstract »    Full Text »    PDF »
Regulation of developmental intercellular signalling by intracellular trafficking.
B.-Z. Shilo and E. D. Schejter (2011)
EMBO J. 30, 3516-3526
   Abstract »    Full Text »    PDF »
Haematopoietic stem cell differentiation promotes the release of prominin-1/CD133-containing membrane vesicles--a role of the endocytic-exocytic pathway.
N. Bauer, M. Wilsch-Brauninger, J. Karbanova, A.-V. Fonseca, D. Strauss, D. Freund, C. Thiele, W. B. Huttner, M. Bornhauser, and D. Corbeil (2011)
EMBO Mol Med. 3, 398-409
   Abstract »    Full Text »    PDF »
Annexin A1 attenuates EMT and metastatic potential in breast cancer.
S. Maschler, C. A. Gebeshuber, E.-M. Wiedemann, M. Alacakaptan, M. Schreiber, I. Custic, and H. Beug (2010)
EMBO Mol Med. 2, 401-414
   Abstract »    Full Text »    PDF »
The novel endosomal membrane protein Ema interacts with the class C Vps-HOPS complex to promote endosomal maturation.
S. Kim, Y. P. Wairkar, R. W. Daniels, and A. DiAntonio (2010)
J. Cell Biol. 188, 717-734
   Abstract »    Full Text »    PDF »
Lighting up developmental mechanisms: how fluorescence imaging heralded a new era.
M. Mavrakis, O. Pourquie, and T. Lecuit (2010)
Development 137, 373-387
   Abstract »    Full Text »    PDF »
Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer.
R. A. Neumuller and J. A. Knoblich (2009)
Genes & Dev. 23, 2675-2699
   Abstract »    Full Text »    PDF »
The regulation of TGF{beta} signal transduction.
A. Moustakas and C.-H. Heldin (2009)
Development 136, 3699-3714
   Abstract »    Full Text »    PDF »
Rab5-mediated endocytosis of activin is not required for gene activation or long-range signalling in Xenopus.
A. I. Hagemann, X. Xu, O. Nentwich, M. Hyvonen, and J. C. Smith (2009)
Development 136, 2803-2813
   Abstract »    Full Text »    PDF »
Mechanisms and functions of endocytosis.
M. Miaczynska and H. Stenmark (2008)
J. Cell Biol. 180, 7-11
   Abstract »    Full Text »    PDF »
Endofin, a FYVE Domain Protein, Interacts with Smad4 and Facilitates Transforming Growth Factor-beta Signaling.
Y.-G. Chen, Z. Wang, J. Ma, L. Zhang, and Z. Lu (2007)
J. Biol. Chem. 282, 9688-9695
   Abstract »    Full Text »    PDF »
Partitioning endosomes.
N. LeBrasseur (2006)
J. Cell Biol. 175, 843b
   Full Text »    PDF »
CELL BIOLOGY: Sara Splits the Signal..
J. A. Knoblich (2006)
Science 314, 1094-1096
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882