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Epithelial tube morphogenesis during Drosophila tracheal development requires Piopio, a luminal ZP protein

Nature Cell Biology volume 5, pages 895–901 (2003)Cite this article

Abstract

The formation of branched epithelial networks is fundamental to the development of many organs, such as the lung, the kidney or the vasculature. Little is known about the mechanisms that control cell rearrangements during tubulogenesis and regulate the size of individual tubes. Recent studies indicate that whereas the basal surface of tube cells interacts with the surrounding tissues and helps to shape the ramification pattern of tubular organs, the apical surface has an important role in the regulation of tube diameter and tube growth. Here we report that two proteins, Piopio (Pio) and Dumpy (Dp), containing a zona pellucida (ZP) domain are essential for the generation of the interconnected tracheal network in Drosophila melanogaster. Pio is secreted apically, accumulates in the tracheal lumen and possibly interacts with Dp through the ZP domains. In the absence of Pio and Dp, multicellular tubes do not rearrange through cell elongation and cell intercalation to form narrow tubes with autocellular junctions; instead they are transformed into multicellular cysts, which leads to a severe disruption of the branched pattern. We propose that an extracellular matrix containing Pio and Dp provides a structural network in the luminal space, around which cell rearrangements can take place in an ordered fashion without losing interconnections. Our results suggest that a similar structural role might be attributed to other ZP-domain proteins in the formation of different branched organs.

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Figure 1: Characterization of a novel tracheal phenotype.
Figure 2: Expression of pio during embryonic development and localization of Pio protein.
Figure 3: Pio is specifically required for the formation of branches with autocellular AJs.
Figure 4: Pio and Dp are required to provide a barrier for autocellular AJ formation.

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Acknowledgements

We thank N. Brown and C. Bökel for communicating results before publication; K. Matthews and the Bloomington stock centre for fly strains; M. Neumann and P. Wassarman for discussion; C. Cabernard for technical help; E. Knust and N. Patel for providing large quantities of anti-Crb and monoclonal antibody 2A12, respectively; and N. C. Grieder and D. Ladle for comments on the manuscript. Financial support was provided by HFSPO, the Swiss National Science Foundation and the Kantons Basel-Stadt and Basel-Land. A.J. acknowledges EMBO and Roche Research Foundation postdoctoral fellowships.

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  1. Abteilung Zellbiologie, Biozentrum der Universität Basel, Klingelbergstrasse 70, Basel, CH-4056, Switzerland

    Anna Jaźwińska, Carlos Ribeiro & Markus Affolter

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  1. Anna Jaźwińska
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  2. Carlos Ribeiro
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Correspondence to Markus Affolter.

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Jaźwińska, A., Ribeiro, C. & Affolter, M. Epithelial tube morphogenesis during Drosophila tracheal development requires Piopio, a luminal ZP protein. Nat Cell Biol 5, 895–901 (2003). https://doi.org/10.1038/ncb1049

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