Structure and Nanomechanics of Dry and Hydrated Intermediate Filament Films and Fibers Produced from Hagfish Slime Fibers

Böni, Lukas; Sánchez‐Ferrer, Antoni; Widmer, Madeleine; Biviano, Matthew; Mezzenga, Raffaele; Windhab, Erich J.; Dagastine, Raymond R.; Fischer, Peter

doi:10.1021/acsami.8b17166

Cited by 12 publications

(5 citation statements)

References 113 publications

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“…Similarly, the dense cytoskeletal scaffold in ribbontail stingray iridophores are likely intermediate filaments, based on their diameter ( Figures 5F, G ; Figure 9E ). In other animals, thick intermediate filaments are known to form remarkably flexible and viscoelastic interconnected networks ( Fudge et al, 2003 ; Böni et al, 2018 ), promoting important dynamic behaviors to intracellular components of skin when hydrated. We therefore posit that the hydration-sensitive mechanical properties (e.g., extensibility, stiffness) of the intermediate filament scaffold in stingray iridophores are key factors for maintaining the necessary inter-crystal spacing to produce blue structural color.…”

Section: Discussionmentioning

confidence: 99%

Intermediate filaments spatially organize intracellular nanostructures to produce the bright structural blue of ribbontail stingrays across ontogeny

Blumer,

Surapaneni,

Ciecierska-Holmes

et al. 2024

Front. Cell Dev. Biol.

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In animals, pigments but also nanostructures determine skin coloration, and many shades are produced by combining both mechanisms. Recently, we discovered a new mechanism for blue coloration in the ribbontail stingray Taeniura lymma, a species with electric blue spots on its yellow-brown skin. Here, we characterize finescale differences in cell composition and architecture distinguishing blue from non-blue regions, the first description of elasmobranch chromatophores and the nanostructures responsible for the stingray’s novel structural blue, contrasting with other known mechanisms for making nature’s rarest color. In blue regions, the upper dermis comprised a layer of chromatophore units —iridophores and melanophores entwined in compact clusters framed by collagen bundles— this structural stability perhaps the root of the skin color’s robustness. Stingray iridophores were notably different from other vertebrate light-reflecting cells in having numerous fingerlike processes, which surrounded nearby melanophores like fists clenching a black stone. Iridophores contained spherical iridosomes enclosing guanine nanocrystals, suspended in a 3D quasi-order, linked by a cytoskeleton of intermediate filaments. We argue that intermediate filaments form a structural scaffold with a distinct optical role, providing the iridosome spacing critical to produce the blue color. In contrast, black-pigmented melanosomes within melanophores showed space-efficient packing, consistent with their hypothesized role as broadband-absorbers for enhancing blue color saturation. The chromatophore layer’s ultrastructure was similar in juvenile and adult animals, indicating that skin color and perhaps its ecological role are likely consistent through ontogeny. In non-blue areas, iridophores were replaced by pale cells, resembling iridophores in some morphological and nanoscale features, but lacking guanine crystals, suggesting that the cell types arise from a common progenitor cell. The particular cellular associations and structural interactions we demonstrate in stingray skin suggest that pigment cells induce differentiation in the progenitor cells of iridophores, and that some features driving color production may be shared with bony fishes, although the lineages diverged hundreds of millions of years ago and the iridophores themselves differ drastically.

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Section: Discussionmentioning

confidence: 99%

Intermediate filaments spatially organize intracellular nanostructures to produce the bright structural blue of ribbontail stingrays across ontogeny

Blumer,

Surapaneni,

Ciecierska-Holmes

et al. 2024

Front. Cell Dev. Biol.

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“…Background scans were collected before each bundle with the exact conditions that were used for the bundle. Spectral correction and deconvolution for secondary structure quantification was performed at the Amide I region (~1600 to 1700 cm −1 ) using OriginPro and a similar method as previously described by (Böni et al ., 2018). The only variation to the described method was the use of Gaussian curves for peak fitting.…”

Section: Methodsmentioning

confidence: 99%

The next generation of protein super‐fibres: robust recombinant production and recovery of hagfish intermediate filament proteins with fibre spinning and mechanical–structural characterizations

Oliveira

Chen

Bell

et al. 2021

Microbial Biotechnology

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Summary Native hagfish intermediate filament proteins have impressive mechanical properties. However, using these native fibres for any application is impractical, necessitating their recombinant production. In the only literature report on the proteins (denoted α and ɣ), heterologous expression levels, using E. coli, were low and no attempts were made to optimize expression, explore wet‐spinning, or spin the two proteins individually into fibres. Reported here is the high production (~8 g l−1 of dry protein) of the hagfish intermediate filament proteins, with yields orders of magnitude higher (325–1000×) than previous reports. The proteins were spun into fibres individually and in their native‐like 1:1 ratio. For all fibres, the hallmark α‐helix to β‐sheet conversion occurred after draw‐processing. The native‐like 1:1 ratio fibres achieved the highest average tensile strength in this study at nearly 200 MPa with an elastic modulus of 5.7 GPa, representing the highest tensile strength reported for these proteins without chemical cross‐linking. Interestingly, the recombinant α protein achieved nearly the same mechanical properties when spun as a homopolymeric fibre. These results suggest that varying the two protein ratios beyond the natural 1:1 ratio will allow a high degree of tunability. With robust heterologous expression and purification established, optimizing fibre spinning will be accelerated compared to difficult to produce proteins such as spider silks.

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“…Slime formation occurs when the contents of the GTC skeins and GMC mucin vesicles are ejected by the animal and mixed turbulently in a seawater environment (Figure ). Once deployed into the saline and basic conditions of the marine milieu, the skeins of IF-like slime threads unravel to their full length ,, and the mucin vesicles rupture, ,− producing the native slime. Interestingly, the presence of specific ions (especially Ca 2+ and Na + ) results in a more controlled skein unravelling process, suggesting a key role of electrostatic interactions in the material assembly process. , Both components are critical for slime formation; the slime threads by themselves will not form a network, and the mucin material on its own lacks any mechanical consistency .…”

Section: Hagfish Slimementioning

confidence: 99%

“… Once deployed into the saline and basic conditions of the marine milieu, the skeins of IF-like slime threads unravel to their full length ,, and the mucin vesicles rupture, ,− producing the native slime. Interestingly, the presence of specific ions (especially Ca 2+ and Na + ) results in a more controlled skein unravelling process, suggesting a key role of electrostatic interactions in the material assembly process. , Both components are critical for slime formation; the slime threads by themselves will not form a network, and the mucin material on its own lacks any mechanical consistency . Yet, together, the components create a stable network that can trap a large amount of water, creating a gel-like materials that can clog the gills of attacking predators …”

Section: Hagfish Slimementioning

confidence: 99%

Biological Materials Processing: Time-Tested Tricks for Sustainable Fiber Fabrication

Rising

Harrington

2022

Chem. Rev.

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There is an urgent need to improve the sustainability of the materials we produce and use. Here, we explore what humans can learn from nature about how to sustainably fabricate polymeric fibers with excellent material properties by reviewing the physical and chemical aspects of materials processing distilled from diverse model systems, including spider silk, mussel byssus, velvet worm slime, hagfish slime, and mistletoe viscin. We identify common and divergent strategies, highlighting the potential for bioinspired design and technology transfer. Despite the diversity of the biopolymeric fibers surveyed, we identify several common strategies across multiple systems, including: (1) use of stimuliresponsive biomolecular building blocks, (2) use of concentrated fluid precursor phases (e.g., coacervates and liquid crystals) stored under controlled chemical conditions, and (3) use of chemical (pH, salt concentration, redox chemistry) and physical (mechanical shear, extensional flow) stimuli to trigger the transition from fluid precursor to solid material. Importantly, because these materials largely form and function outside of the body of the organisms, these principles can more easily be transferred for bioinspired design in synthetic systems. We end the review by discussing ongoing efforts and challenges to mimic biological model systems, with a particular focus on artificial spider silks and mussel-inspired materials.

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Structure and Nanomechanics of Dry and Hydrated Intermediate Filament Films and Fibers Produced from Hagfish Slime Fibers

Abstract: Intermediate filament (IF) films produced from hagfish fiber protein readily hydrate and change from a stiff (10 9 Pa) to a soft (10 6 Pa) viscoelastic material.

Cited by 12 publications

References 113 publications

Intermediate filaments spatially organize intracellular nanostructures to produce the bright structural blue of ribbontail stingrays across ontogeny

Intermediate filaments spatially organize intracellular nanostructures to produce the bright structural blue of ribbontail stingrays across ontogeny

The next generation of protein super‐fibres: robust recombinant production and recovery of hagfish intermediate filament proteins with fibre spinning and mechanical–structural characterizations

Biological Materials Processing: Time-Tested Tricks for Sustainable Fiber Fabrication

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