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Ascidian caveolin induces membrane curvature and protects tissue integrity and morphology during embryogenesis.

ABSTRACT: Cell morphology and tissue integrity are essential for embryogenesis. Caveolins are membrane proteins that induce the formation of surface pits called caveolae that serve as membrane reservoirs for cell and tissue protection during development. In vertebrates, caveolin 1 (Cav1) and caveolin 3 (Cav3) are required for caveola formation. However, the formation of caveola and the function of caveolins in invertebrates are largely unknown. In this study, three caveolins, Cav-a, Cav-b, and CavY, are identified in the genome of the invertebrate chordate Ciona spp. Based on phylogenetic analysis, Cav-a is found to be closely related to the vertebrate Cav1 and Cav3. In situ hybridization shows that Cav-a is expressed in Ciona embryonic notochord and muscle. Cell-free experiments, model cell culture systems, and in vivo experiments demonstrate that Ciona Cav-a has the ability to induce membrane curvature at the plasma membrane. Knockdown of Cav-a in Ciona embryos causes loss of invaginations in the plasma membrane and results in the failure of notochord elongation and lumenogenesis. Expression of a dominant-negative Cav-a point mutation causes cells to change shape and become displaced from the muscle and notochord to disrupt tissue integrity. Furthermore, we demonstrate that Cav-a vesicles show polarized trafficking and localize at the luminal membrane during notochord lumenogenesis. Taken together, these results show that the invertebrate chordate caveolin from Ciona plays crucial roles in tissue integrity and morphology by inducing membrane curvature and intracellular vesicle trafficking during embryogenesis.

SUBMITTER: Bhattachan P

PROVIDER: S-EPMC7383883 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Ascidian caveolin induces membrane curvature and protects tissue integrity and morphology during embryogenesis.

Bhattachan Punit P Rae James J Yu Haiyan H Jung WooRam W Wei Jiankai J Parton Robert G RG Dong Bo B

FASEB journal : official publication of the Federation of American Societies for Experimental Biology 20191130 1

Cell morphology and tissue integrity are essential for embryogenesis. Caveolins are membrane proteins that induce the formation of surface pits called caveolae that serve as membrane reservoirs for cell and tissue protection during development. In vertebrates, caveolin 1 (Cav1) and caveolin 3 (Cav3) are required for caveola formation. However, the formation of caveola and the function of caveolins in invertebrates are largely unknown. In this study, three caveolins, Cav-a, Cav-b, and CavY, are i ...[more]

PMID: 31914618

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Project description:BackgroundProtein membrane transduction domains that are able to cross the plasma membrane are present in several transcription factors, such as the homeodomain proteins and the viral proteins such as Tat of HIV-1. Their discovery resulted in both new concepts on the cell communication during development, and the conception of cell penetrating peptide vectors for internalisation of active molecules into cells. A promising cell penetrating peptide is Penetratin, which crosses the cell membranes by a receptor and metabolic energy-independent mechanism. Recent works have claimed that Penetratin and similar peptides are internalized by endocytosis, but other endocytosis-independent mechanisms have been proposed. Endosomes or plasma membranes crossing mechanisms are not well understood. Previously, we have shown that basic peptides induce membrane invaginations suggesting a new mechanism for uptake, "physical endocytosis".Methodology/principal findingsHerein, we investigate the role of membrane lipid phases on Penetratin induced membrane deformations (liquid ordered such as in "raft" microdomains versus disordered fluid "non-raft" domains) in membrane models. Experimental data show that zwitterionic lipid headgroups take part in the interaction with Penetratin suggesting that the external leaflet lipids of cells plasma membrane are competent for peptide interaction in the absence of net negative charges. NMR and X-ray diffraction data show that the membrane perturbations (tubulation and vesiculation) are associated with an increase in membrane negative curvature. These effects on curvature were observed in the liquid disordered but not in the liquid ordered (raft-like) membrane domains.Conclusions/significanceThe better understanding of the internalisation mechanisms of protein transduction domains will help both the understanding of the mechanisms of cell communication and the development of potential therapeutic molecular vectors. Here we showed that the membrane targets for these molecules are preferentially the fluid membrane domains and that the mechanism involves the induction of membrane negative curvature. Consequences on cellular uptake are discussed.

Dataset Information

Ascidian caveolin induces membrane curvature and protects tissue integrity and morphology during embryogenesis.

Publications

Ascidian caveolin induces membrane curvature and protects tissue integrity and morphology during embryogenesis.

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