Carotenoids without hydroxyl groups provide the formation of an orthorhombic organisation of lipids in the human stratum corneum
Maxim E. Darvin1, Jin-Song Ri2, Se-Hyok Choe2, Kwang-Hyok Jong3, Song-Nam Hong2, Johannes Schleusener1, Juergen Lademann1, Chun-Sik Choe2
1 Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Dermatology, Venerology and Allergology, Center of Experimental and Applied Cutaneous Physiology, Charitéplatz 1, 10117 Berlin, Germany
2 Faculty of Materials Science, Kim Il Sung University, Pyongyang, DPR Korea
3 Faculty of Physics, Kim Il Sung University, Pyongyang, DPR Korea
Abstract
The stratum corneum (SC), the horny outermost layer of the skin, consists of enucleated corneocytes embedded into the intercellular lipid bilayer matrix and maintains the skin barrier function. Intercellular lipids form the structurally organised membrane-like lamellae structures [1]. Carotenoids in the SC are known to accumulate in high concentrations within lipid lamellae, where they have an antioxidant and photo-protectant function [2]. Here, we show an additional role of carotenoids in the formation of the lateral organisation of lipid bilayers in the SC, which has not been considered before. Molecular dynamics simulations were used to investigate the orientation of the exemplary carotenoids lycopene and zeaxanthin and their influence on the lateral organisation of lipids in an SC lipid bilayer model consisting of hydrated ceramides NS24 for 32 and 37 °C. The results show that lycopene is arranged parallel and zeaxanthin perpendicular to the surface of the lipid bilayer within lamellae. Furthermore, the lipid bilayers loaded with lycopene show a strong orthorhombic organisation, whereas the zeaxanthin-loaded and the pure lipid bilayers were organised in a disordered hexagonal and liquid state. The effect is stronger at 32 than at 37 °C. We show that the distance between carotenoid atoms coincides with the distance between atoms in lipids, indicating that parallel oriented carotenoids without hydroxyl groups (lycopene, α-carotene, β-carotene, γ-carotene, ξ-carotene, phytoene, phytofluene) serve as a skeleton for the formation and stabilization of lipid membranes within the lamellae. Thus, we confirm that carotenoids without hydroxyl polar groups in the SC are parallel to the lipid bilayer plane and facilitate the formation of the orthorhombic lipid organisation, which provides the skin barrier function. Carotenoids with a hydroxyl group (zeaxanthin, lutein and astaxanthin) are perpendicular to the surface of the lipid bilayer and have no or minor influence on the creation of the orthorhombic organisation in a lipid bilayer [3]. These results broaden our understanding of the physiological role of carotenoids in the formation and maintenance of orthorhombic organisation in the SC and, as a result, the entire skin barrier function.
References:
1. van Smeden, J.; Janssens, M.; Gooris, G.S.; Bouwstra, J.A. The Important Role of Stratum Corneum Lipids for the Cutaneous Barrier Function. Biochim. Biophys. Acta 2014, 1841, 295–313, doi:10.1016/j.bbalip.2013.11.006.
2. Darvin, M.E.; Lademann, J.; von Hagen, J.; Lohan, S.B.; Kolmar, H.; Meinke, M.C.; Jung, S. Carotenoids in Human Skin In Vivo: Antioxidant and Photo-Protectant Role against External and Internal Stressors. Antioxidants 2022, 11, 1451, doi:10.3390/antiox11081451.
3. Ri, J.-S.; Choe, C.-S.; Choe, S.-H.; Jong, K.-H.; Hong, S.-N.; Schleusener, J.; Lademann, J.; Darvin, M.E. Lycopene, but Not Zeaxanthin, Serves as a Skeleton for the Formation of an Orthorhombic Organization of Intercellular Lipids within the Lamellae in the Stratum Corneum. Biochim. Biophys. Acta. Submitted 2022.
Speaker
Maxim E. Darvin
Charité-Universitätsmedizin Berlin
Germany
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