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BBLN-1 is essential for intermediate filament organization and apical membrane morphology

Remmelzwaal, Sanne; Geisler, Florian; Stucchi, Riccardo; van der Horst, Suzanne; Pasolli, Milena; Kroll, Jason R.; Jarosinska, Olga D.; Akhmanova, Anna; Richardson, Christine A.; Altelaar, Maarten; Leube, Rudolf E.; Ramalho, João J.; Boxem, Mike

BBLN-1 is essential for intermediate filament organization and apical membrane morphology Thumbnail


Authors

Sanne Remmelzwaal

Florian Geisler

Riccardo Stucchi

Suzanne van der Horst

Milena Pasolli

Jason R. Kroll

Olga D. Jarosinska

Anna Akhmanova

Christine A. Richardson

Maarten Altelaar

Rudolf E. Leube

João J. Ramalho

Mike Boxem



Abstract

Epithelial tubes are essential components of metazoan organ systems that control the flow of fluids and the exchange of materials between body compartments and the outside environment. The size and shape of the central lumen confer important characteristics to tubular organs and need to be carefully controlled. Here, we identify the small coiled-coil protein BBLN-1 as a regulator of lumen morphology in the C. elegans intestine. Loss of BBLN-1 causes the formation of bubble-shaped invaginations of the apical membrane into the cytoplasm of intestinal cells and abnormal aggregation of the subapical intermediate filament (IF) network. BBLN-1 interacts with IF proteins and localizes to the IF network in an IF-dependent manner. The appearance of invaginations is a result of the abnormal IF aggregation, indicating a direct role for the IF network in maintaining lumen homeostasis. Finally, we identify bublin (BBLN) as the mammalian ortholog of BBLN-1. When expressed in the C. elegans intestine, BBLN recapitulates the localization pattern of BBLN-1 and can compensate for the loss of BBLN-1 in early larvae. In mouse intestinal organoids, BBLN localizes subapically, together with the IF protein keratin 8. Our results therefore may have implications for understanding the role of IFs in regulating epithelial tube morphology in mammals.

Citation

Remmelzwaal, S., Geisler, F., Stucchi, R., van der Horst, S., Pasolli, M., Kroll, J. R., …Boxem, M. (2021). BBLN-1 is essential for intermediate filament organization and apical membrane morphology. Current Biology, 31(11), 2334-2346. https://doi.org/10.1016/j.cub.2021.03.069

Journal Article Type Article
Acceptance Date Mar 19, 2021
Online Publication Date Apr 14, 2021
Publication Date Jun 7, 2021
Deposit Date Apr 15, 2021
Publicly Available Date Mar 28, 2024
Journal Current Biology
Print ISSN 0960-9822
Publisher Cell Press
Peer Reviewed Peer Reviewed
Volume 31
Issue 11
Pages 2334-2346
DOI https://doi.org/10.1016/j.cub.2021.03.069

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