A lipid transfer protein ensures nematode cuticular impermeability

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

doi:10.1016/j.isci.2022.105357

A lipid transfer protein ensures nematode cuticular impermeability

iScience. 2022 Oct 14;25(11):105357. doi: 10.1016/j.isci.2022.105357. eCollection 2022 Nov 18.

Authors

Ferdinand Ngale Njume^{1

2

3}, Adria Razzauti³, Miguel Soler³, Veronika Perschin⁴, Gholamreza Fazeli⁴, Axelle Bourez⁵, Cedric Delporte⁵, Stephen M Ghogomu², Philippe Poelvoorde¹, Simon Pichard⁶, Catherine Birck⁶, Arnaud Poterszman⁶, Jacob Souopgui¹, Pierre Van Antwerpen⁵, Christian Stigloher⁴, Luc Vanhamme¹, Patrick Laurent³

Affiliations

¹ Department of Molecular Biology, Institute of Biology and Molecular Medicine, IBMM, Université Libre de Bruxelles, Bruxelles, Belgium.
² Molecular and Cell Biology Laboratory, Biotechnology Unit, University of Buea, Buea, Cameroon.
³ Laboratory of Neurophysiology, ULB Institute for Neuroscience, Université Libre de Bruxelles, Bruxelles, Belgium.
⁴ Imaging Core Facility, Biocenter, University of Würzburg, Würzburg, Germany.
⁵ RD3-Pharmacognosy, Bioanalysis and Drug Discovery and Analytical Platform of the Faculty of Pharmacy, Universite libre de Bruxelles, Bruxelles, Belgium.
⁶ Department of Integrated Structural Biology, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Strasbourg, France.

Abstract

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.

Keywords: Biological sciences; molecular biology; physiology.