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Modeling membrane nanotube morphology: the role of heterogeneity in composition and material properties.

ABSTRACT: Membrane nanotubes are dynamic structures that may connect cells over long distances. Nanotubes are typically thin cylindrical tubes, but they may occasionally have a beaded architecture along the tube. In this paper, we study the role of membrane mechanics in governing the architecture of these tubes and show that the formation of bead-like structures along the nanotubes can result from local heterogeneities in the membrane either due to protein aggregation or due to membrane composition. We present numerical results that predict how membrane properties, protein density, and local tension compete to create a phase space that governs the morphology of a nanotube. We also find that there exists a discontinuity in the energy that impedes two beads from fusing. These results suggest that the membrane-protein interaction, membrane composition, and membrane tension closely govern the tube radius, number of beads, and the bead morphology.

SUBMITTER: Alimohamadi H

PROVIDER: S-EPMC7018976 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Modeling membrane nanotube morphology: the role of heterogeneity in composition and material properties.

Alimohamadi Haleh H Ovryn Ben B Rangamani Padmini P

Scientific reports 20200213 1

Membrane nanotubes are dynamic structures that may connect cells over long distances. Nanotubes are typically thin cylindrical tubes, but they may occasionally have a beaded architecture along the tube. In this paper, we study the role of membrane mechanics in governing the architecture of these tubes and show that the formation of bead-like structures along the nanotubes can result from local heterogeneities in the membrane either due to protein aggregation or due to membrane composition. We pr ...[more]

PMID: 32054874

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Project description:BackgroundCentipedes are terrestrial and predatory arthropods that possess an evolutionary transformed pair of appendages used for venom injection-the forcipules. Many arthropods incorporate reinforcing elements into the cuticle of their piercing or biting structures to enhance hardness, elasticity or resistance to wear and structural failure. Given their frequent exposure to high mechanical stress, we hypothesise that the cuticle of the centipede forcipule might be mechanically reinforced. With a combination of imaging, analytical techniques and mechanical testing, we explore the centipede forcipule in detail to shed light on its morphology and performance. Additionally, we compare these data to characteristics of the locomotory leg to infer evolutionary processes.ResultsWe examined sclerotization patterns using confocal laser-scanning microscopy based on autofluorescence properties of the cuticle (forcipule and leg) and elemental composition by energy-dispersive X-ray spectroscopy in representative species from all five centipede lineages. These experiments revealed gradually increasing sclerotization towards the forcipular tarsungulum and a stronger sclerotization of joints in taxa with condensed podomeres. Depending on the species, calcium, zinc or chlorine are present with a higher concentration towards the distal tarsungulum. Interestingly, these characteristics are more or less mirrored in the locomotory leg's pretarsal claw in Epimorpha. To understand how incorporated elements affect mechanical properties, we tested resistance to structural failure, hardness (H) and Young's modulus (E) in two representative species, one with high zinc and one with high calcium content. Both species, however, exhibit similar properties and no differences in mechanical stress the forcipule can withstand.ConclusionsOur study reveals similarities in the material composition and properties of the forcipules in centipedes. The forcipules transformed from an elongated leg-like appearance into rigid piercing structures. Our data supports their serial homology to the locomotory leg and that the forcipule's tarsungulum is a fusion of tarsus and pretarsal claw. Calcium or zinc incorporation leads to comparable mechanical properties like in piercing structures of chelicerates and insects, but the elemental incorporation does not increase H and E in centipedes, suggesting that centipedes followed their own pathways in the evolutionary transformation of piercing tools.

Dataset Information

Modeling membrane nanotube morphology: the role of heterogeneity in composition and material properties.

Publications

Modeling membrane nanotube morphology: the role of heterogeneity in composition and material properties.

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