C-terminal phosphorylation modulates ERM-1 localization and dynamics to control cortical actin organization and support lumen formation during <i>Caenorhabditis</i> <i>elegans</i> development

Ramalho, João J.; Sepers, Jorian J.; Nicolle, Ophélie; Schmidt, Ruben; Cravo, Janine; Michaux, Grégoire; Boxem, Mike

doi:10.1242/dev.188011

Cited by 31 publications

(62 citation statements)

References 80 publications

(141 reference statements)

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“…10 We therefore generated an endogenous IFB-2::mCherry fusion and analyzed the localization of BBLN-1 relative to IFB-2 and ERM-1, which localizes to microvilli. 29,30 Consistent with localization to the endotube, we found that BBLN-1 co-localized with IFB-2, basal to ERM-1 (Figures 2C and 2D). To determine whether BBLN-1 stably associates with the IF network, we performed fluorescence recovery after photobleaching (FRAP) experiments.…”

Section: Loss Of Bbln-1 Causes Cytoplasmic Invaginations Of the Intestinal Apical Membranesupporting

confidence: 77%

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

et al. 2021

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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.

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Section: Loss Of Bbln-1 Causes Cytoplasmic Invaginations Of the Intestinal Apical Membranesupporting

confidence: 77%

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

et al. 2021

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“…To confirm that BBLN-1 resides at the endotube, we generated an endogenous mCherry fusion of the intestinal intermediate filament protein IFB-2. We then analyzed the localization of BBLN-1 relative to IFB-2 and to ERM-1, which localizes apically at microvilli (Bidaud-Meynard et al, 2019; Ramalho et al, 2020). Consistent with localization to the endotube, we found that BBLN-1 colocalizes with IFB-2, basal to ERM-1 (Fig.…”

Section: Resultsmentioning

confidence: 99%

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

Remmelzwaal

Geisler

Stucchi

et al. 2020

Preprint

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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, bublin recapitulates the localization pattern of BBLN-1 and can compensate for the loss of BBLN-1. In mouse intestinal organoids, bublin 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.SummaryWe identify BBLN-1 as an evolutionary conserved regulator of lumen morphology in the C. elegans intestine. Loss of bbln-1 causes intermediate filament network reorganization that induces severe apical morphology defects. We also identify bublin (BBLN) as the mammalian ortholog, which can compensate for the loss of BBLN-1 in C. elegans.

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“…The central lumen is surrounded by a thick electron-dense terminal web [ 25 ] (also seen in the nematode and mammalian intestine, among many other tissues) composed of actin filaments and intermediate filaments. Actin is held to the apical membrane by the Ezrin-Radixin-Moesin homologue ERM-1 [ 26 ], which itself is activated via phosphorylation of a terminal domain upon binding to phosphatidyl inositol 4,5-bisphosphate (PIP 2 ) lipid on the apical (luminal) surface [ 27 ]. Overlapping and surrounding the actin cytoskeleton is a thick layer of three intermediate filament proteins, IFA-4, IFB-1, and EXC-2/IFC-2 [ 22 , 28 ].…”

Section: Anatomy Of the Canal Cellmentioning

confidence: 99%

A Series of Tubes: The C. elegans Excretory Canal Cell as a Model for Tubule Development

Buechner

Yang

Al-Hashimi

2020

JDB

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Formation and regulation of properly sized epithelial tubes is essential for multicellular life. The excretory canal cell of C. elegans provides a powerful model for investigating the integration of the cytoskeleton, intracellular transport, and organismal physiology to regulate the developmental processes of tube extension, lumen formation, and lumen diameter regulation in a narrow single cell. Multiple studies have provided new understanding of actin and intermediate filament cytoskeletal elements, vesicle transport, and the role of vacuolar ATPase in determining tube size. Most of the genes discovered have clear homologues in humans, with implications for understanding these processes in mammalian tissues such as Schwann cells, renal tubules, and brain vasculature. The results of several new genetic screens are described that provide a host of new targets for future studies in this informative structure.

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C-terminal phosphorylation modulates ERM-1 localization and dynamics to control cortical actin organization and support lumen formation during Caenorhabditis elegans development

Cited by 31 publications

References 80 publications

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

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

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

A Series of Tubes: The C. elegans Excretory Canal Cell as a Model for Tubule Development

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