The Specific Molecular Composition and Structural Arrangement of Eleutherodactylus Coqui Gular Skin Tissue Provide Its High Mechanical Compliance
Open Access
- 4 August 2020
- journal article
- research article
- Published by MDPI AG in International Journal of Molecular Sciences
- Vol. 21 (16), 5593
- https://doi.org/10.3390/ijms21165593
Abstract
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.Keywords
Funding Information
- National Institute of Biomedical Imaging and Bioengineering (R21EB026711)
This publication has 44 references indexed in Scilit:
- Fabrication of Microropes via Bi‐electrospinning with a Rotating Needle CollectorMacromolecular Rapid Communications, 2010
- Tendon and ligament fibrillar crimps give rise to left‐handed helices of collagen fibrils in both planar and helical crimpsJournal of Anatomy, 2010
- The bladder extracellular matrix. Part I: architecture, development and diseaseNature Reviews Urology, 2009
- Structure‐function relationships in tendons: a reviewJournal of Anatomy, 2008
- Biomedical Applications of Layer‐by‐Layer Assembly: From Biomimetics to Tissue EngineeringAdvanced Materials, 2006
- Composition and biomechanical properties of the bladder acellular matrix graft: comparative analysis in rat, pig and humanBritish Journal of Urology, 1998
- Fibrillar Structure and Mechanical Properties of CollagenJournal of Structural Biology, 1998
- Pufferfish inflation: Functional morphology of postcranial structures in Diodon holocanthus (Tetraodontiformes)Journal of Morphology, 1994
- Vocal Sac Variation among Frogs of the Genus Rana from Western North AmericaIchthyology & Herpetology, 1986