Abstract
Collagen is one of the most versatile tissues of living organisms that comes in many shapes and sizes, providing functions ranging from tissue matrix through, ligament formation up to enabling mineralization in teeth. The detailed light microscopy and Scanning Electron Microscopy (SEM) observations conducted in this study, allowed us to investigate morphology, sizes and crimp patterns of collagen fibers observed in crocodile skin and teeth. Moreover, the microscopy study revealed that although two completely different tissues were investigated, many similarities in their structure based on collagen fibers were observed. Collagen type I is present in crocodile skin and teeth, showing the flexibility in naturally constructed tissues to obtain various functions. The crimp size investigation of collagen fibers confirmed experimentally the theoretical 67 nm D-periodicity expected for collagen type I. The collagen in teeth provides a matrix for crystal growth and in the skin provides flexibility and is a precursor for corneous scales. Importantly, these observations of the collagen in the skin and tooth structure in crocodiles play an important role in designing biomimetic materials with similar functions and properties.
Article PDF
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
References
Metwally S, Martínez Comesaña S, Zarzyka M, Szewczyk P K, Karbowniczek J E, Stachewicz U. Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair. Acta Biomaterialia, 2019, 91, 270–283.
Römer L, Scheibel T. The elaborate structure of spider silk: Structure and function of a natural high performance fiber. Prion, 2008, 2, 154–161.
Szewczyk P K, Knapczyk-Korczak J, Ura D P, Metwally S, Gruszczyński A, Stachewicz U. Biomimicking wetting properties of spider web from Linothele megatheloides with electrospun fibers. Materials Letters, 2018, 233, 211–214.
Kadler K E, Holmes D F, Trotter J A, Chapman J A. Collagen fibril formation. Biochemical Journal, 1996, 316, 1–11.
Canty E G, Kadler K E. Procollagen trafficking, processing and fibrillogenesis. Journal of Cell Science, 2005, 118, 1341–1353.
Fratzl P, Misof K, Zizak I, Rapp G. Amenitsch H, Bernstorff S. Fibrillar structure and mechanical properties of collagen. Journal of Structural Biology, 1998, 122, 119–122.
Chintapalli R K, Mirkhalaf M, Dastjerdi A K, Barthelat F. Fabrication, testing and modeling of a new flexible armor inspired from natural fish scales and osteoderms. Bioinspiration & Biomimetics, 2014, 9, 036005.
Bernth J E, Ho V A, Liu H B. Morphological computation in haptic sensation and interaction: From nature to robotics. Advanced Robotics, 2018, 32, 340–362.
Kanhere E, Wang N, Kottapalli A G P, Asadnia M. Subramaniam V. Miao J, Triantafyllou M. Crocodile-inspired dome-shaped pressure receptors for passive hydrodynamic sensing. Bioinspiration & Biomimetics, 2016, 11, 056007.
Elkan E, Cooper J E. Skin biology of reptiles and amphibians. Proceedings of the Royal Society of Edinburgh, Section B: Biological Sciences, 1980, 79, 115–126.
Dubansky B H, Close M. A review of alligator and snake skin morphology and histotechnical preparations. Journal of Histotechnology, 2019, 42, 31–51.
Lin C P, Douglas W H, Erlandsen S L. Scanning electron microscopy of type I collagen at the dentin-enamel junction of human teeth. Journal of Histochemistry & Cytochemistry, 1993, 41, 381–388.
Erickson G M, Brochu C A. How the ‘terror crocodile’ grew so big. Nature, 1999, 398, 205–206.
Sennikov A G. The first ctenosauriscid (Reptilia: Archosauromorpha) from the lower triassic of eastern europe. Paleontological Journal, 2012, 46, 499–511.
Drymala S M, Zanno L E. Osteology of carnufex carolinensis (archosauria: psuedosuchia) from the pekin formation of north carolina and its implications for early crocodylomorph evolution. PLOS ONE, 2016, 11, e0157528.
Webb G J W, Manolis S C, Brien M L. Crocodiles: Status Survey and Conservation Action Plan, 3rd ed, Crocodile Specialist Group: Darwin, Darwin, Australia, 2010.
Alibardi L. Keratinization in crocodilian scales and avian epidermis: Evolutionary implications for the region of avian apteric epidermis. Belgian Journal of Zoology, 2005, 135, 9–20.
Alibardi L. Histology, ultrastructure, and pigmentation in the horny scales of growing crocodilians. Acta Zoologica, 2011, 92, 187–200.
Holthaus K B, Strasser B, Lachner J, Sukseree S, Sipos W, Weissenbacher A, Tschachler E, Alibardi L, Eckhart L. Comparative analysis of epidermal differentiation genes of crocodilians suggests new models for the evolutionary origin of avian feather proteins. Genome Biology and Evolution, 2018, 10, 694–704.
Pressinotti L N, Borges R M, Alves De Lima A P, Aleixo V M, Iunes R S, Borges J C S, Cogliati B, Cunha Da Silva J R M. Low temperatures reduce skin healing in the Jacare do Pantanal (Caiman yacare, Daudin 1802). Biology Open, 2013, 2, 1171–1178.
Dalla Valle L, Nardi A, Gelmi C, Toni M, Emera D, Alibardi L. β-keratins of the crocodilian epidermis: Composition, structure, and phylogenetic relationships. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 2009, 312B, 42–57.
Alibardi L, Toni M. Cytochemical, biochemical and molecular aspects of the process of keratinization in the epidermis of reptilian scales. Progress in Histochemistry and Cytochemistry, 2006, 40, 73–134.
Alibardi L, Thompson M B. Keratinization and ultrastructure of the epidermis of late embryonic stages in the alligator (Alligator mississippiensis). Journal of Anatomy, 2002, 201, 71–84.
Alibardi L. Adaptation to the land: The skin of reptiles in comparison to that of amphibians and endotherm amniotes. Journal of Experimental Zoology, 2003, 298B, 12–41.
Baden H P, Maderson P F. Morphological and biophysical identification of fibrous proteins in the amniote epidermis. Journal of Experimental Zoology, 1970, 174, 225–232.
Alibardi L. Sauropsids cornification is based on corneous beta-proteins, a special type of keratin-associated corneous proteins of the epidermis. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 2016, 326, 338–351.
Holthaus K B, Eckhart L, Dalla Valle L, Alibardi L. Review: Evolution and diversification of corneous beta-proteins, the characteristic epidermal proteins of reptiles and birds. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 2019, 330, 438–453.
Berthod F, Germain L, Li H, Xu W, Damour O, Auger F A. Collagen fibril network and elastic system remodeling in a reconstructed skin transplanted on nude mice. Matrix Biology, 2001, 20, 463–473.
Matoltsy A G, Huszar T. Keratinization of the reptilian epidermis: An ultrastructural study of the turtle skin. Journal of Ultrastructure Research, 1972, 38, 87–101.
Cheema U, Ananta M, Muder V. Collagen: Applications of a natural polymer in regenerative medicine regenerative medicine and tissue engineering, in: Cells and Biomaterials, InTech, London, UK, 2011, 13, 287–300.
Enax J, Fabritius H O, Rack A, Prymak O, Raabe D, Epple M. Characterization of crocodile teeth: Correlation of composition, microstructure, and hardness. Journal of Structural Biology, 2013, 184, 155–163.
Weiner S, Wagner H D. The material bone: Structure-mechanical function relations. Annual Review of Materials Science, 1998, 28, 271–298.
Gupta H S, Stachewicz U, Wagermaier W, Roschger P, Wagner H D, Fratzl P. Mechanical modulation at the lamellar level in osteonal bone. Journal of Materials Research, 2006, 21, 1913–1921.
Datta P, Vyas V, Dhara S, Chowdhury A R, Barui, A. Anisotropy properties of tissues: A basis for fabrication of biomimetic anisotropic scaffolds for tissue engineering. Journal of Bionic Engineering, 2019, 16, 842–868.
De Leeuw N H, Rabone J A L. Molecular dynamics simulations of the interaction of citric acid with the hydroxyapatite (0001) and (0110) surfaces in an aqueous environment. CrystEngComm, 2007, 9, 1178–1186.
Boskey A L. Mineralization of bones and teeth. Elements, 2007, 3, 385–391.
Erickson G M, Gignac P M, Steppan S J, Lappin A K, Vliet K A, Brueggen J D, Inouye B D, Kledzik D, Webb G J W. Insights into the ecology and evolutionary success of crocodilians revealed through bite-force and tooth-pressure experimentation. PLOS ONE, 2012, 7, e31781.
He G, George A. Dentin matrix protein 1 immobilized on type I collagen fibrils facilitates apatite deposition in vitro. Journal of Biological Chemistry, 2004, 279, 11649–11656.
Lodish H F, Berk A, Zipursky S L, Matsudaira P, Baltimore D, Darnell J. Molecular Cell Biology. W. H. Freeman, New York, USA, 2000, 1084.
Parry D A D, Barnes G R G, Craig A S. A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relation between fibril size distribution and mechanical properties. Proceedings of the Royal Society of London, Series B, Biological Sciences, 1978, 203, 305–321.
Franchi M, Raspanti M, Dell’Orbo C, Quaranta M, De Pasquale V, Ottani V, Ruggeri A. Different crimp patterns in collagen fibrils relate to the subfibrillar arrangement. Connective Tissue Research, 2008, 49, 85–91.
Franchi M, Fini M, Quaranta M, De Pasquale V, Raspanti M, Giavaresi G, Ottani V, Ruggeri A. Crimp morphology in relaxed and stretched rat Achilles tendon. Journal of Anatomy, 2007, 210, 1–7.
Raspanti M, Manelli A, Franchi M, Ruggeri A. The 3D structure of crimps in the rat Achilles tendon. Matrix Biology, 2005, 24, 503–507.
Acknowledgment
The authors thank Adam Hryniewicz from Warsaw Zoo for crocodile skin and teeth samples used in this study. This study was conducted as part of the “Nanofiber-based sponges for atopic skin treatment” project, which is carried out within the First TEAM programme of the Foundation for Polish Science co-financed by the European Union under the European Regional Development Fund, Project No. POIR. 04.04.00-00-4571/18-00. This study was supported by the infrastructure at the International Centre of Electron Microscopy for Materials Science (IC-EM) at AGH University of Science and Technology.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made.
The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.
To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Szewczyk, P.K., Stachewicz, U. Collagen Fibers in Crocodile Skin and Teeth: A Morphological Comparison Using Light and Scanning Electron Microscopy. J Bionic Eng 17, 669–676 (2020). https://doi.org/10.1007/s42235-020-0059-7
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42235-020-0059-7