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Int J Mol Sci
2020 Aug 05;2116:. doi: 10.3390/ijms21165593.
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The Specific Molecular Composition and Structural Arrangement of Eleutherodactylus Coqui Gular SkinTissue Provide Its High Mechanical Compliance.
Hui J
,
Sharma S
,
Rajani S
,
Singh A
.
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A male Eleutherodactylus Coqui (EC, a frog) expands and contracts its gular skin to a great extent during mating calls, displaying its extraordinarily compliant organ. There are striking similarities between frog gular skin and the human bladder as both organs expand and contract significantly. While the high extensibility of the urinary bladder is attributed to the unique helical ultrastructure of collagen type III, the mechanism behind the gular skin of EC is unknown. We therefore aim to understand the structure-property relationship of gular skin tissues of EC. Our findings demonstrate that the male EC gular tissue can elongate up to 400%, with an ultimate tensile strength (UTS) of 1.7 MPa. Species without vocal sacs, Xenopus Laevis (XL) and Xenopus Muelleri (XM), elongate only up to 80% and 350% with UTS~6.3 MPa and ~4.5 MPa, respectively. Transmission electron microscopy (TEM) and histological staining further show that EC tissues' collagen fibers exhibit a layer-by-layer arrangement with an uninterrupted, knot-free, and continuous structure. The collagen bundles alternate between a circular and longitudinal shape, suggesting an out-of-plane zig-zag structure, which likely provides the tissue with greater extensibility. In contrast, control species contain a nearly linear collagen structure interrupted by thicker muscle bundles and mucous glands. Meanwhile, in the rat bladder, the collagen is arranged in a helical structure. The bladder-like high extensibility of EC gular skin tissue arises despite it having eight-fold lesser elastin and five times more collagen than the rat bladder. To our knowledge, this is the first study to report the structural and molecular mechanisms behind the high compliance of EC gular skin. We believe that these findings can lead us to develop more compliant biomaterials for applications in regenerative medicine.
Figure 1. (A) A male Hyperolius Cinnamomeoventris, with inflated gular skintissue to resonate its mating call. Reproduced from [5]. (B) Gross visual of tissue dissection areas. Shown here is the Xenopus Laevis specimen.
Figure 2. Representative uniaxial stress–strain curves of (A) gular skintissue and (B) leg skin of different anuran species and their comparison to the rat bladder.
Figure 3. Tissue morphology by histology of gular tissue dissected from various species of frogs. Scale bar 100 µm. Muscle bundles (black arrows), mucous glands (red arrows), collagen structure (green arrows), perpendicularly aligned collagen (yellow arrows), urothelium (orange), lamina propria (purple), and detrusor muscle (grey).
Figure 5. TEM images of gular tissue for (A) male EC, 3400×. Scale bar 2 µm; (B) female EC, 3400×. Scale bar 2 µm; (C) XL, 1000×. Scale bar 10 µm; (D) XM, 4200×. Scale bar 10 µm; (E) male EC, 13,500×. Scale bar 500 nm. Green lines represent the crimp angle measurements (θ1 = 80°, θ2 = 70°). (F) Female EC, 13,500×. Scale bar 500 nm. Green lines represent the crimp angle measurements (θ = 77°). (G) XL, 3400×. Scale bar 2 µm. (H) XM, 13,500×. Scale bar 500 nm. Red boxes indicate the area magnified.
Figure 6. TEM images of the rat bladder. (A) Alternating collagen orientation. 17,500×. Scale bar 500 nm. (B) Crimp structure. 13,500×. Scale bar 500 nm. (C) Helical structure. 9700×. Scale bar 500 nm. (D) Magnified alternating collagen orientation. 33,000×. Scale bar 500 nm. (E) Magnified crimp structure. 24,500×. Scale bar 500 nm. (F) Magnified helical structure. 17,500×. Scale bar 500 nm.
Figure 7. (A) Elastin content and (B) collagen content for the respective tissue sample. M: male, F: female. p < 0.05 (*) and p < 0.01 (**)
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