Drosophila E-cadherin is required for the maintenance of ring canals anchoring to mechanically withstand tissue growth

Nicolas Loyer, Irina Kolotuev, Mathieu Pinot, Roland Le Borgne (Lead / Corresponding author)

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

Intercellular bridges called "ring canals" (RCs) resulting from incomplete cytokinesis play an essential role in intercellular communication in somatic and germinal tissues. During Drosophila oogenesis, RCs connect the maturing oocyte to nurse cells supporting its growth. Despite numerous genetic screens aimed at identifying genes involved in RC biogenesis and maturation, how RCs anchor to the plasma membrane (PM) throughout development remains unexplained. In this study, we report that the clathrin adaptor protein 1 (AP-1) complex, although dispensable for the biogenesis of RCs, is required for the maintenance of the anchorage of RCs to the PM to withstand the increased membrane tension associated with the exponential tissue growth at the onset of vitellogenesis. Here we unravel the mechanisms by which AP-1 enables the maintenance of RCs' anchoring to the PM during size expansion. We show that AP-1 regulates the localization of the intercellular adhesion molecule E-cadherin and that loss of AP-1 causes the disappearance of the E-cadherin-containing adhesive clusters surrounding the RCs. E-cadherin itself is shown to be required for the maintenance of the RCs' anchorage, a function previously unrecognized because of functional compensation by N-cadherin. Scanning block-face EM combined with transmission EM analyses reveals the presence of interdigitated, actin- And Moesin-positive, microvilli-like structures wrapping the RCs. Thus, by modulating E-cadherin trafficking, we show that the sustained E-cadherin-dependent adhesion organizes the microvilli meshwork and ensures the proper attachment of RCs to the PM, thereby counteracting the increasing membrane tension induced by exponential tissue growth.

Original languageEnglish
Pages (from-to)12717-12722
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume112
Issue number41
DOIs
Publication statusPublished - 13 Oct 2015

Fingerprint

Cadherins
Drosophila
Maintenance
Growth
Cell Membrane
Microvilli
Adaptor Protein Complex 1
Vitellogenesis
Oogenesis
Proteins
Cytokinesis
Membranes
Cell Adhesion Molecules
Adhesives
Oocytes
Actins
Nurses
Genes

Keywords

  • E-cadherin
  • Membrane tension
  • Ring canals
  • Tissue growth
  • Trafficking

Cite this

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Drosophila E-cadherin is required for the maintenance of ring canals anchoring to mechanically withstand tissue growth. / Loyer, Nicolas; Kolotuev, Irina; Pinot, Mathieu; Borgne, Roland Le (Lead / Corresponding author).

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, No. 41, 13.10.2015, p. 12717-12722.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Drosophila E-cadherin is required for the maintenance of ring canals anchoring to mechanically withstand tissue growth

AU - Loyer, Nicolas

AU - Kolotuev, Irina

AU - Pinot, Mathieu

AU - Borgne, Roland Le

PY - 2015/10/13

Y1 - 2015/10/13

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AB - Intercellular bridges called "ring canals" (RCs) resulting from incomplete cytokinesis play an essential role in intercellular communication in somatic and germinal tissues. During Drosophila oogenesis, RCs connect the maturing oocyte to nurse cells supporting its growth. Despite numerous genetic screens aimed at identifying genes involved in RC biogenesis and maturation, how RCs anchor to the plasma membrane (PM) throughout development remains unexplained. In this study, we report that the clathrin adaptor protein 1 (AP-1) complex, although dispensable for the biogenesis of RCs, is required for the maintenance of the anchorage of RCs to the PM to withstand the increased membrane tension associated with the exponential tissue growth at the onset of vitellogenesis. Here we unravel the mechanisms by which AP-1 enables the maintenance of RCs' anchoring to the PM during size expansion. We show that AP-1 regulates the localization of the intercellular adhesion molecule E-cadherin and that loss of AP-1 causes the disappearance of the E-cadherin-containing adhesive clusters surrounding the RCs. E-cadherin itself is shown to be required for the maintenance of the RCs' anchorage, a function previously unrecognized because of functional compensation by N-cadherin. Scanning block-face EM combined with transmission EM analyses reveals the presence of interdigitated, actin- And Moesin-positive, microvilli-like structures wrapping the RCs. Thus, by modulating E-cadherin trafficking, we show that the sustained E-cadherin-dependent adhesion organizes the microvilli meshwork and ensures the proper attachment of RCs to the PM, thereby counteracting the increasing membrane tension induced by exponential tissue growth.

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KW - Membrane tension

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KW - Tissue growth

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M3 - Article

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JF - Proceedings of the National Academy of Sciences

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