A lipid transfer protein ensures nematode cuticular impermeability
Summary: The cuticle of C. elegans is impermeable to chemicals, toxins, and pathogens. However, increased permeability is a desirable phenotype because it facilitates chemical uptake. Surface lipids contribute to the permeability barrier. Here, we identify the lipid transfer protein GMAP-1 as a crit...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-11-01
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| Series: | iScience |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004222016297 |
| _version_ | 1797991815677214720 |
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| author | Ferdinand Ngale Njume Adria Razzauti Miguel Soler Veronika Perschin Gholamreza Fazeli Axelle Bourez Cedric Delporte Stephen M. Ghogomu Philippe Poelvoorde Simon Pichard Catherine Birck Arnaud Poterszman Jacob Souopgui Pierre Van Antwerpen Christian Stigloher Luc Vanhamme Patrick Laurent |
| author_facet | Ferdinand Ngale Njume Adria Razzauti Miguel Soler Veronika Perschin Gholamreza Fazeli Axelle Bourez Cedric Delporte Stephen M. Ghogomu Philippe Poelvoorde Simon Pichard Catherine Birck Arnaud Poterszman Jacob Souopgui Pierre Van Antwerpen Christian Stigloher Luc Vanhamme Patrick Laurent |
| author_sort | Ferdinand Ngale Njume |
| collection | DOAJ |
| description | Summary: The cuticle of C. elegans is impermeable to chemicals, toxins, and pathogens. However, increased permeability is a desirable phenotype because it facilitates chemical uptake. Surface lipids contribute to the permeability barrier. Here, we identify the lipid transfer protein GMAP-1 as a critical element setting the permeability of the C. elegans cuticle. A gmap-1 deletion mutant increases cuticular permeability to sodium azide, levamisole, Hoechst, and DiI. Expressing GMAP-1 in the hypodermis or transiently in the adults is sufficient to rescue this gmap-1 permeability phenotype. GMAP-1 protein is secreted from the hypodermis to the aqueous fluid filling the space between collagen fibers of the cuticle. In vitro, GMAP-1 protein binds phosphatidylserine and phosphatidylcholine while in vivo, GMAP-1 sets the surface lipid composition and organization. Altogether, our results suggest GMAP-1 secreted by hypodermis shuttles lipids to the surface to form the permeability barrier of C. elegans. |
| first_indexed | 2024-04-11T08:57:01Z |
| format | Article |
| id | doaj.art-3e0e2469a0304b9d98eb1c1c06653455 |
| institution | Directory Open Access Journal |
| issn | 2589-0042 |
| language | English |
| last_indexed | 2024-04-11T08:57:01Z |
| publishDate | 2022-11-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj.art-3e0e2469a0304b9d98eb1c1c066534552022-12-22T04:33:09ZengElsevieriScience2589-00422022-11-012511105357A lipid transfer protein ensures nematode cuticular impermeabilityFerdinand Ngale Njume0Adria Razzauti1Miguel Soler2Veronika Perschin3Gholamreza Fazeli4Axelle Bourez5Cedric Delporte6Stephen M. Ghogomu7Philippe Poelvoorde8Simon Pichard9Catherine Birck10Arnaud Poterszman11Jacob Souopgui12Pierre Van Antwerpen13Christian Stigloher14Luc Vanhamme15Patrick Laurent16Department of Molecular Biology, Institute of Biology and Molecular Medicine, IBMM, Université Libre de Bruxelles, Bruxelles, Belgium; Molecular and Cell Biology Laboratory, Biotechnology Unit, University of Buea, Buea, Cameroon; Laboratory of Neurophysiology, ULB Institute for Neuroscience, Université Libre de Bruxelles, Bruxelles, BelgiumLaboratory of Neurophysiology, ULB Institute for Neuroscience, Université Libre de Bruxelles, Bruxelles, BelgiumLaboratory of Neurophysiology, ULB Institute for Neuroscience, Université Libre de Bruxelles, Bruxelles, BelgiumImaging Core Facility, Biocenter, University of Würzburg, Würzburg, GermanyImaging Core Facility, Biocenter, University of Würzburg, Würzburg, GermanyRD3-Pharmacognosy, Bioanalysis and Drug Discovery and Analytical Platform of the Faculty of Pharmacy, Universite libre de Bruxelles, Bruxelles, BelgiumRD3-Pharmacognosy, Bioanalysis and Drug Discovery and Analytical Platform of the Faculty of Pharmacy, Universite libre de Bruxelles, Bruxelles, BelgiumMolecular and Cell Biology Laboratory, Biotechnology Unit, University of Buea, Buea, CameroonDepartment of Molecular Biology, Institute of Biology and Molecular Medicine, IBMM, Université Libre de Bruxelles, Bruxelles, BelgiumDepartment of Integrated Structural Biology, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Strasbourg, FranceDepartment of Integrated Structural Biology, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Strasbourg, FranceDepartment of Integrated Structural Biology, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Strasbourg, FranceDepartment of Molecular Biology, Institute of Biology and Molecular Medicine, IBMM, Université Libre de Bruxelles, Bruxelles, BelgiumRD3-Pharmacognosy, Bioanalysis and Drug Discovery and Analytical Platform of the Faculty of Pharmacy, Universite libre de Bruxelles, Bruxelles, BelgiumImaging Core Facility, Biocenter, University of Würzburg, Würzburg, GermanyDepartment of Molecular Biology, Institute of Biology and Molecular Medicine, IBMM, Université Libre de Bruxelles, Bruxelles, BelgiumLaboratory of Neurophysiology, ULB Institute for Neuroscience, Université Libre de Bruxelles, Bruxelles, Belgium; Corresponding authorSummary: The cuticle of C. elegans is impermeable to chemicals, toxins, and pathogens. However, increased permeability is a desirable phenotype because it facilitates chemical uptake. Surface lipids contribute to the permeability barrier. Here, we identify the lipid transfer protein GMAP-1 as a critical element setting the permeability of the C. elegans cuticle. A gmap-1 deletion mutant increases cuticular permeability to sodium azide, levamisole, Hoechst, and DiI. Expressing GMAP-1 in the hypodermis or transiently in the adults is sufficient to rescue this gmap-1 permeability phenotype. GMAP-1 protein is secreted from the hypodermis to the aqueous fluid filling the space between collagen fibers of the cuticle. In vitro, GMAP-1 protein binds phosphatidylserine and phosphatidylcholine while in vivo, GMAP-1 sets the surface lipid composition and organization. Altogether, our results suggest GMAP-1 secreted by hypodermis shuttles lipids to the surface to form the permeability barrier of C. elegans.http://www.sciencedirect.com/science/article/pii/S2589004222016297Biological sciencesmolecular biologyphysiology |
| spellingShingle | Ferdinand Ngale Njume Adria Razzauti Miguel Soler Veronika Perschin Gholamreza Fazeli Axelle Bourez Cedric Delporte Stephen M. Ghogomu Philippe Poelvoorde Simon Pichard Catherine Birck Arnaud Poterszman Jacob Souopgui Pierre Van Antwerpen Christian Stigloher Luc Vanhamme Patrick Laurent A lipid transfer protein ensures nematode cuticular impermeability iScience Biological sciences molecular biology physiology |
| title | A lipid transfer protein ensures nematode cuticular impermeability |
| title_full | A lipid transfer protein ensures nematode cuticular impermeability |
| title_fullStr | A lipid transfer protein ensures nematode cuticular impermeability |
| title_full_unstemmed | A lipid transfer protein ensures nematode cuticular impermeability |
| title_short | A lipid transfer protein ensures nematode cuticular impermeability |
| title_sort | lipid transfer protein ensures nematode cuticular impermeability |
| topic | Biological sciences molecular biology physiology |
| url | http://www.sciencedirect.com/science/article/pii/S2589004222016297 |
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