A V0-ATPase-dependent apical trafficking pathway maintains the polarity of the intestinal absorptive membrane

Bidaud-Meynard, Aurélien; Nicolle, Ophélie; Heck, Michael; Cunff, Yann Le; Michaux, Grégoire

doi:10.1242/dev.174508

Cited by 24 publications

(39 citation statements)

References 76 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…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: 78%

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

et al. 2021

View full text Add to dashboard Cite

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.

show abstract

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

confidence: 78%

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

et al. 2021

View full text Add to dashboard Cite

show abstract

“…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

View full text Add to dashboard Cite

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.

show abstract

“…Loss of function mutations in syntaxin binding protein 2 result in familial hemophagocytic lymphohistiocytosis type 5, a disease that manifests gastrointestinal symptoms similar to MVID (Davidson et al, 1978;Côte et al, 2009;Pagel et al, 2012;Stepensky et al, 2013;Vogel et al, 2017;Mosa et al, 2018). Silencing of the V0-ATPase in Caenorhabditis elegans also revealed microvillus inclusion formation de novo in the cytoplasm or from internalization of large structures from the apical or basolateral plasma membrane (Bidaud-Meynard et al, 2019). The formation of microvillus-lined inclusions, best characterized in MVID, has been postulated to arise from nucleation in the cytoplasm or from internalization of the plasma membrane (Davidson et al, 1978;Cutz et al, 1989;Mosa et al, 2018;Bidaud-Meynard et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Loss of myosin Vb promotes apical bulk endocytosis in neonatal enterocytes

Engevik

Kaji

Postema

et al. 2019

Journal of Cell Biology

View full text Add to dashboard Cite

In patients with inactivating mutations in myosin Vb (Myo5B), enterocytes show large inclusions lined by microvilli. The origin of inclusions in small-intestinal enterocytes in microvillus inclusion disease is currently unclear. We postulated that inclusions in Myo5b KO mouse enterocytes form through invagination of the apical brush border membrane. 70-kD FITC-dextran added apically to Myo5b KO intestinal explants accumulated in intracellular inclusions. Live imaging of Myo5b KO–derived enteroids confirmed the formation of inclusions from the apical membrane. Treatment of intestinal explants and enteroids with Dyngo resulted in accumulation of inclusions at the apical membrane. Inclusions in Myo5b KO enterocytes contained VAMP4 and Pacsin 2 (Syndapin 2). Myo5b;Pacsin 2 double-KO mice showed a significant decrease in inclusion formation. Our results suggest that apical bulk endocytosis in Myo5b KO enterocytes resembles activity-dependent bulk endocytosis, the primary mechanism for synaptic vesicle uptake during intense neuronal stimulation. Thus, apical bulk endocytosis mediates the formation of inclusions in neonatal Myo5b KO enterocytes.

show abstract

A V0-ATPase-dependent apical trafficking pathway maintains the polarity of the intestinal absorptive membrane

Cited by 24 publications

References 76 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

Loss of myosin Vb promotes apical bulk endocytosis in neonatal enterocytes

Contact Info

Product

Resources

About