The Wnt–Wingless (Wg) pathway regulates development through precisely controlled signaling. In this study, we show that intracellular trafficking regulates Wg signaling levels. In Drosophila melanogaster cells stimulated with Wg media, dynamin or Rab5 knockdown causes reduced Super8XTOPflash activity, suggesting that internalization and endosomal transport facilitate Wg signaling. In the wing, impaired dynamin function reduces Wg transcription. However, when Wg production is unaffected, extracellular Wg levels are increased. Despite this, target gene expression is reduced, indicating that internalization is also required for efficient Wg signaling in vivo. When endosomal transport is impaired, Wg signaling is similarly reduced. Conversely, the expression of Wg targets is enhanced by increased transport to endosomes or decreased hepatocyte growth factor–regulated tyrosine kinase substrate– mediated transport from endosomes. This increased signaling correlates with greater colocalized Wg, Arrow, and Dishevelled on endosomes. As these data indicate that endosomal transport promotes Wg signaling, our findings suggest that the regulation of endocytosis is a novel mechanism through which Wg signaling levels are determined.
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10 April 2006
Article|
April 10 2006
Internalization is required for proper Wingless signaling in Drosophila melanogaster
Elaine S. Seto,
Elaine S. Seto
3Program in Developmental Biology, Baylor College of Medicine, Houston, TX 77030
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Hugo J. Bellen
Hugo J. Bellen
1Department of Molecular and Human Genetics
2Department of Neuroscience, Howard Hughes Medical Institute,
3Program in Developmental Biology, Baylor College of Medicine, Houston, TX 77030
Search for other works by this author on:
Elaine S. Seto
3Program in Developmental Biology, Baylor College of Medicine, Houston, TX 77030
Hugo J. Bellen
1Department of Molecular and Human Genetics
2Department of Neuroscience, Howard Hughes Medical Institute,
3Program in Developmental Biology, Baylor College of Medicine, Houston, TX 77030
Correspondence to Hugo J. Bellen: [email protected]
Abbreviations used in this paper: Arm, Armadillo; Arr, Arrow; Ck1a, casein kinase 1a; CMV, cytomegalovirus; Dll, Distal-less; Dsh, Dishevelled; dsRNA, double-stranded RNA; DV, dorsal–ventral; Hrs, hepatocyte growth factor–regulated tyrosine kinase substrate; MVB, multivesicular body; RL, Renilla luciferase; Sens, Senseless; shi, shibire; Wg, Wingless; Wg(ex), extracellular Wg.
Received:
October 24 2005
Accepted:
March 08 2006
Online ISSN: 1540-8140
Print ISSN: 0021-9525
The Rockefeller University Press
2006
J Cell Biol (2006) 173 (1): 95–106.
Article history
Received:
October 24 2005
Accepted:
March 08 2006
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Elaine S. Seto, Hugo J. Bellen; Internalization is required for proper Wingless signaling in Drosophila melanogaster . J Cell Biol 10 April 2006; 173 (1): 95–106. doi: https://doi.org/10.1083/jcb.200510123
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