Dishevelled localization and function are differentially regulated by structurally distinct sterols

Summary: The Dishevelled (DVL) protein family forms supramolecular protein and lipid complexes at the cytoplasmic interface of the plasma membrane to regulate tissue patterning, proliferation, cell polarity, and DVL-dependent signaling, such as Wnt/β-catenin. While DVL binding to cholesterol is requ...

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Main Authors: Sonali Sengupta, Jazmine D.W. Yaeger, Maycie M. Schultz, Danielle G. May, Kyle J. Roux, Kevin R. Francis
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:iScience
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Online Access:http://www.sciencedirect.com/science/article/pii/S2589004225009654
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author Sonali Sengupta
Jazmine D.W. Yaeger
Maycie M. Schultz
Danielle G. May
Kyle J. Roux
Kevin R. Francis
author_facet Sonali Sengupta
Jazmine D.W. Yaeger
Maycie M. Schultz
Danielle G. May
Kyle J. Roux
Kevin R. Francis
author_sort Sonali Sengupta
collection DOAJ
description Summary: The Dishevelled (DVL) protein family forms supramolecular protein and lipid complexes at the cytoplasmic interface of the plasma membrane to regulate tissue patterning, proliferation, cell polarity, and DVL-dependent signaling, such as Wnt/β-catenin. While DVL binding to cholesterol is required for its membrane association, the specific structural requirements and cellular impacts of DVL-sterol association are unclear. We report that sterols found within both natural and pathological conditions cause aberrant DVL activity. In silico and molecular analyses suggested orientation of the β- and α-sterol face within the DVL-PDZ domain regulates DVL-sterol binding. Aberrant sterols impaired DVL2 plasma membrane association, inducing DVL2 nuclear localization via FoxK2. Altered sterol homeostasis also selectively impaired DVL2 protein-protein interactions with impacts on multiple signaling pathways. This work identifies sterol specificity as a regulator of DVL signaling, demonstrates intracellular sterols impact DVL localization and activity, and supports a role for aberrant DVL activity within disorders of sterol metabolism.
format Article
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issn 2589-0042
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publishDate 2025-06-01
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series iScience
spelling doaj-art-a43d993065dc401495e48e6450cabcbd2025-08-20T03:26:35ZengElsevieriScience2589-00422025-06-0128611270410.1016/j.isci.2025.112704Dishevelled localization and function are differentially regulated by structurally distinct sterolsSonali Sengupta0Jazmine D.W. Yaeger1Maycie M. Schultz2Danielle G. May3Kyle J. Roux4Kevin R. Francis5Cellular Therapies and Stem Cell Biology Group, Sanford Research, Sioux Falls, SD 57104, USACellular Therapies and Stem Cell Biology Group, Sanford Research, Sioux Falls, SD 57104, USACellular Therapies and Stem Cell Biology Group, Sanford Research, Sioux Falls, SD 57104, USAEnabling Technologies Group, Sanford Research, Sioux Falls, SD 57104, USAEnabling Technologies Group, Sanford Research, Sioux Falls, SD 57104, USA; Department of Pediatrics, University of South Dakota Sanford School of Medicine, Sioux Falls, SD 57105, USACellular Therapies and Stem Cell Biology Group, Sanford Research, Sioux Falls, SD 57104, USA; Department of Pediatrics, University of South Dakota Sanford School of Medicine, Sioux Falls, SD 57105, USA; Corresponding authorSummary: The Dishevelled (DVL) protein family forms supramolecular protein and lipid complexes at the cytoplasmic interface of the plasma membrane to regulate tissue patterning, proliferation, cell polarity, and DVL-dependent signaling, such as Wnt/β-catenin. While DVL binding to cholesterol is required for its membrane association, the specific structural requirements and cellular impacts of DVL-sterol association are unclear. We report that sterols found within both natural and pathological conditions cause aberrant DVL activity. In silico and molecular analyses suggested orientation of the β- and α-sterol face within the DVL-PDZ domain regulates DVL-sterol binding. Aberrant sterols impaired DVL2 plasma membrane association, inducing DVL2 nuclear localization via FoxK2. Altered sterol homeostasis also selectively impaired DVL2 protein-protein interactions with impacts on multiple signaling pathways. This work identifies sterol specificity as a regulator of DVL signaling, demonstrates intracellular sterols impact DVL localization and activity, and supports a role for aberrant DVL activity within disorders of sterol metabolism.http://www.sciencedirect.com/science/article/pii/S2589004225009654Natural sciencesBiological sciencesBiochemistry
spellingShingle Sonali Sengupta
Jazmine D.W. Yaeger
Maycie M. Schultz
Danielle G. May
Kyle J. Roux
Kevin R. Francis
Dishevelled localization and function are differentially regulated by structurally distinct sterols
iScience
Natural sciences
Biological sciences
Biochemistry
title Dishevelled localization and function are differentially regulated by structurally distinct sterols
title_full Dishevelled localization and function are differentially regulated by structurally distinct sterols
title_fullStr Dishevelled localization and function are differentially regulated by structurally distinct sterols
title_full_unstemmed Dishevelled localization and function are differentially regulated by structurally distinct sterols
title_short Dishevelled localization and function are differentially regulated by structurally distinct sterols
title_sort dishevelled localization and function are differentially regulated by structurally distinct sterols
topic Natural sciences
Biological sciences
Biochemistry
url http://www.sciencedirect.com/science/article/pii/S2589004225009654
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AT mayciemschultz dishevelledlocalizationandfunctionaredifferentiallyregulatedbystructurallydistinctsterols
AT daniellegmay dishevelledlocalizationandfunctionaredifferentiallyregulatedbystructurallydistinctsterols
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