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Minerals and Aligned Collagen Fibrils in Tilapia Fish Scales: Structural Analysis Using Dark-Field and Energy-Filtered Transmission Electron Microscopy and Electron Tomography

Published online by Cambridge University Press:  08 September 2011

Mitsuhiro Okuda
Affiliation:
Biomaterials Center, National Institute for Materials Science, 1-2-1 Sengen, Tsukuba, Ibaraki 305-0047, Japan Advanced Nano-Characterization Center, National Institute for Materials Science, 3-13 Sakura, Tsukuba, Ibaraki 305-0003, Japan
Nobuhiro Ogawa
Affiliation:
Biomaterials Center, National Institute for Materials Science, 1-2-1 Sengen, Tsukuba, Ibaraki 305-0047, Japan
Masaki Takeguchi*
Affiliation:
Advanced Nano-Characterization Center, National Institute for Materials Science, 3-13 Sakura, Tsukuba, Ibaraki 305-0003, Japan
Ayako Hashimoto
Affiliation:
International Center for Young Scientists, National Institute for Materials Science, 1-2-1 Sengen, Tsukuba, Ibaraki 305-0047, Japan
Motohiro Tagaya
Affiliation:
Biomaterials Center, National Institute for Materials Science, 1-2-1 Sengen, Tsukuba, Ibaraki 305-0047, Japan
Song Chen
Affiliation:
Biomaterials Center, National Institute for Materials Science, 1-2-1 Sengen, Tsukuba, Ibaraki 305-0047, Japan
Nobutaka Hanagata
Affiliation:
Biomaterials Center, National Institute for Materials Science, 1-2-1 Sengen, Tsukuba, Ibaraki 305-0047, Japan
Toshiyuki Ikoma
Affiliation:
Department of Metallurgy and Ceramics Science, Tokyo Institute of Technology, 2-12-1-S7-6 Ookayama, Meguro-ku, Tokyo 152-8550, Japan
*
Corresponding author. E-mail: TAKEGUCHI.Masaki@nims.go.jp
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Abstract

The mineralized structure of aligned collagen fibrils in a tilapia fish scale was investigated using transmission electron microscopy (TEM) techniques after a thin sample was prepared using aqueous techniques. Electron diffraction and electron energy loss spectroscopy data indicated that a mineralized internal layer consisting of aligned collagen fibrils contains hydroxyapatite crystals. Bright-field imaging, dark-field imaging, and energy-filtered TEM showed that the hydroxyapatite was mainly distributed in the hole zones of the aligned collagen fibrils structure, while needle-like materials composed of calcium compounds including hydroxyapatite existed in the mineralized internal layer. Dark-field imaging and three-dimensional observation using electron tomography revealed that hydroxyapatite and needle-like materials were mainly found in the matrix between the collagen fibrils. It was observed that hydroxyapatite and needle-like materials were preferentially distributed on the surface of the hole zones in the aligned collagen fibrils structure and in the matrix between the collagen fibrils in the mineralized internal layer of the scale.

Type
Biological Applications
Copyright
Copyright © Microscopy Society of America 2011

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References

REFERENCES

Anderson, H.C. (2003). Matrix vesicles and calcification. Cur Rheumatol Rep 5, 222226.CrossRefGoogle ScholarPubMed
Ascenzi, A., Bonucci, E. & Bocciarelli, D.S. (1965). An electron microscope study of osteon calcification. J Ultrastruct Res 12, 287303.CrossRefGoogle ScholarPubMed
Ascenzi, M.G., Ascenzi, A., Benvenuti, A., Burghammer, M., Panzavolta, S. & Bigi, A. (2003). Structural differences between “dark” and “bright” isolated human osteonic lamellae. J Struct Biol 141, 2233.CrossRefGoogle ScholarPubMed
Bereiter-Hahn, J. & Zylberberg, L. (1993). Regeneration of teleost fish scale. Comp Biochem Physiol 105, 625641.CrossRefGoogle Scholar
Bigi, A., Burghammer, M., Falconi, R., Kosh, M.H.J., Panzavolta, S. & Riekel, C. (2001). Twisted plywood pattern of collagen fibrils in teleost scales: An X-ray diffraction investigation. J Struct Biol 136, 137143.CrossRefGoogle Scholar
Bigi, A., Gandolfi, M., Koch, M.H.J. & Roveri, N. (1991). Structural analysis of turkey tendon collagen upon removal of the inorganic phase. Int J Biol Macromol 13, 110114.CrossRefGoogle ScholarPubMed
Bigi, A., Koch, M.H.J., Ripamonti, A. & Roveri, N. (1988). Calcified turkey leg tendon as structural model for bone mineralization. Int J Biol Macromol 10, 282286.CrossRefGoogle Scholar
Capaldi, M.J. & Chapman, J.A. (1982). The C-terminal extrahelical peptide of type I collagen and its role in fibrillogenesis in vitro. Biopolymers 21, 22912313.CrossRefGoogle ScholarPubMed
Dechichi, P., Biffi, J.C., Moura, C.C. & de Ameida, A.W. (2007). A model of the early mineralization process of mantle dentin. Micron 38, 486491.CrossRefGoogle Scholar
Fujisawa, R., Nodasaka, Y. & Kuboki, Y. (1995). Further characterization of interaction between bone sialoprotein (BSP) and collagen. Calcif Tissue Int 56, 140144.CrossRefGoogle ScholarPubMed
Ge, J., Cui, F.-Z., Wang, X. & Wang, Y. (2007). New evidence of surface mineralization of collagen fibrils in wild type zebrafish skeleton by AFM and TEM. Mater Sci Eng C 27, 4650.CrossRefGoogle Scholar
Gregori, G., Kleebe, H.J., Mayer, H. & Ziegler, G. (2006). EELS characterisation of β-tricalcium phosphate and hydroxyapatite. J Eur Ceram Soc 26, 14731479.CrossRefGoogle Scholar
Ikoma, T., Kobayashi, H., Tanaka, J., Walsh, D. & Mann, S. (2003). Microstructure, mechanical, and biomimetic properties of fish scales from Pagrus major. J Struct Biol 142, 327333.CrossRefGoogle ScholarPubMed
Jiang, H., Ramunno-Johnson, D., Song, C., Amirbekian, B., Kohmura, Y., Nishino, Y., Takahashi, Y., Ishikawa, T. & Miao, J. (2008). Nanoscale imaging of mineral crystals inside biological composite materials using X-ray diffraction microscopy. Phys Rev Lett 100, 038103.CrossRefGoogle ScholarPubMed
Kadler, K.E., Holmers, D.F., Trotter, J.A. & Chapman, J.A. (1996). Collagen fibril formation. Biochem J 316, 111.CrossRefGoogle ScholarPubMed
Khemiri, S., Meunier, F.J., Laurin, M. & Zylberberg, L. (2001). Morphology and structure of the scales in the Gadiformes (Actinopterygii: Teleostei: Paracanthopterygii) and a comparison to the elasmoid scales of other Teleostei. Cah Biol Mar 42, 345362.Google Scholar
Kohler, D.M., Crenshaw, M.A. & Arsenault, A.L. (1994). Three-dimensional analysis of mineralizing turkey leg tendon: Matrix vesicle-collagen relationships. Matrix Biol 14, 543552.CrossRefGoogle Scholar
Landis, W.J. & Glimcher, M.J. (1978). Electron-diffraction and electron-probe microanalysis of mineral phase of bone tissue prepared by anhydrous techniques. J Ultrastruct Res 63, 188223.CrossRefGoogle ScholarPubMed
Landis, W.J. & Glimcher, M.J. (1982). Electron-optical and analytical observations of rat growth plate cartilage prepared by ultra-cryomicrotomy—The failure to detect a mineral phase in matrix vesicles and the identification of heterodispersed particles as the initial solid-phase of calcium-phosphate deposited in the extracellular-matrix. J Ultrastruct Res 78, 227268.CrossRefGoogle ScholarPubMed
Landis, W.J., Hauschka, B.T., Rogerson, C.A. & Glimcher, M.J. (1977). Electron-microscopic observations of bone tissue prepared by ultra-cryomicrotomy. J Ultrastruct Res 59, 185206.CrossRefGoogle Scholar
Landis, W.J., Hodgens, K.J., Song, M.J., Arena, J., Kiyonaga, S., Marko, M., Owen, C. & McEwen, B.F. (1996). Mineralization of collagen may occur on fibril surfaces: Evidence from conventional and high-voltage electron microscopy and three-dimensional imaging. J Struct Biol 117, 2435.CrossRefGoogle ScholarPubMed
Landis, W.J., Silver, F.H. & Freeman, J.W. (2006). Collagen as a scaffolding for biomimetic mineralization. J Mater Chem 16, 14951503.CrossRefGoogle Scholar
Landis, W.J., Song, M.J., Leith, A., McEwen, L. & McEwen, B. (1993). Mineral and organic matrix interaction in normally calcifying tendon visualized in 3 dimensions by high-voltage electron-microscopic tomography and graphic image-reconstruction. J Struct Biol 110, 3954.CrossRefGoogle ScholarPubMed
Lees, S. & Prostak, K. (1988). The locus of mineral crystallites in bone. Connect Tissue Res 18, 4154.CrossRefGoogle ScholarPubMed
Leibovich, S.J. & Weiss, J.B. (1970). Electron microscope studies of the effects of endo- and exopeptidase digestion on tropocollagen. A novel concept of the role of terminal regions in fibrillogenesis. Biochim Biophys Acta 214, 445454.CrossRefGoogle ScholarPubMed
Liao, S., Ngiam, M., Watari, F., Ramakrishna, S. & Chan, C.K. (2007). Systematic fabrication of nano-carbonated hydroxyapatite/collagen composites for biomimetic bone grafts. Bioinsp Biomim 2, 3741.CrossRefGoogle ScholarPubMed
Liou, A.C., Chen, A.Y., Lee, H.Y. & Bow, L.S. (2004). Structural characterization of nano-sized calcium deficient apatite powders. Biomaterials 25, 189196.CrossRefGoogle ScholarPubMed
Martin, R.B., Burr, D. & Sharkey, N. (1998). Skeletal Tissue Mechanics. New York: Springer-Verlag.CrossRefGoogle Scholar
Midgly, P.A. & Weyland, M. (2003). 3D electron microscopy in the physical sciences: The development of Z-contrast and EFTEM tomography. Ultramicroscopy 96, 413431.CrossRefGoogle Scholar
Neurath, M.F. (1993). Detection of luse bodies, spiraled collagen, dysplastic collagen, and intracellular collagen in rheumatoid connective tissues: An electron microscopic study. Ann Rheum Dis 52, 278284.CrossRefGoogle ScholarPubMed
Okuda, M., Takeguchi, M., Tagaya, M., Tonegawa, T., Hashimoto, A., Hanagata, N. & Ikoma, T. (2009). Elemental distribution analysis of type I collagen fibrils in tilapia fish scale with energy-filtered transmission electron microscope. Micron 40, 665668.CrossRefGoogle ScholarPubMed
Olson, O.P. & Watabe, N. (1980). Studies on formation and resorption of fish scales. Cell Tissue Res 211, 303316.CrossRefGoogle ScholarPubMed
Olszta, M., Cheng, X., Jee, S., Kumar, R., Kim, Y., Kaufman, M., Douglas, E. & Gower, L. (2007). Bone structure and formation: A new perspective. Mater Sci Eng R 58, 77116.CrossRefGoogle Scholar
Onozato, H. & Watabe, N. (1979). Studies on fish scale formation and resorption. III. Fine structure and calcification of the fibrillary plates of the scales in Carassius auratus (Cypriniformes: Cyprinidae). Cell Tissue Res 201, 409422.Google ScholarPubMed
Parfitt, G.J., Pinali, C., Young, R.D., Quantock, A.J. & Knupp, C. (2010). Three-dimensional reconstruction of collagen-proteoglycan interactions in the mouse corneal stroma by electron tomography. J Struct Biol 170, 392397.CrossRefGoogle ScholarPubMed
Petruska, J.A. & Hodge, A.J. (1963). In Aspects of Protein Structure, Ramachandran, G.N. (Ed.), pp. 289300. New York: Academic Press.Google Scholar
Petruska, J.A. & Hodge, A.J. (1964). A subunit model for the tropocollagen macromolecule. Proc Natl Acad Sci USA 51, 871876.CrossRefGoogle ScholarPubMed
Plate, U., Hohling, H.J., Reimer, L., Barckhaus, R.H., Wienecke, R., Wiesmann, H.P. & Boyde, A. (1992). Analysis of the calcium distribution in predentine by EELS and of the early crystal-formation in dentin by ESI and ESD. J Microsc 166(Pt 3), 329341.CrossRefGoogle ScholarPubMed
Schönbörner, A.A., Boivin, G. & Baud, C.A. (1979). The mineralization process in teleost fish scales. Cell Tissue Res 202, 203212.CrossRefGoogle ScholarPubMed
Vanmeerbeek, B.V., Dhem, A., Goret-Nicaise, M., Braem, M., Lambrechts, P. & VanHerle, G. (1993). Comparative SEM and TEM examination of the ultrastructure of the resin-dentin interdiffusion zone. J Dent Res 72, 495501.CrossRefGoogle Scholar
Weiner, S., Traub, W. & Wagner, D. (1993). Lamellar bone: Structure–function relations. J Struct Biol 126, 241255.CrossRefGoogle Scholar
Weiner, S. & Wagner, H.D. (1998). The material bone: Structure mechanical function relations. Ann Rev Mater Sci 28, 271298.CrossRefGoogle Scholar
Yamada, J. & Watabe, N. (1979). Studies on fish scale formation and resorption. I. Fine structure and calcification of the scales in Fundulus heteroclitus (Atheriniformes: Cyprinodontidae). J Morphol 159, 4966.CrossRefGoogle ScholarPubMed
Zylberberg, L., Bereiter-Hahn, J. & Sire, J.Y. (1988). Cytoskeletal organization and collagen orientation in the fish scales. Cell Tissue Res 253, 597607.CrossRefGoogle ScholarPubMed
Zylberberg, L., Bonaventure, J., Cohen-Solal, L., Hartmann, D.J. & Bereiter-Hahn, J. (1992). Organization and characterization of fibrillar collagens in fish scales in situ and in vitro. J Cell Sci 103, 273285.CrossRefGoogle Scholar
Zylberberg, L., Chanet, B., Wagemans, F. & Meunier, F.O.J. (2003). Structural peculiarities of the tubercles in the skin of the turbot, Scophthalmus maximus (L., 1758) (Osteichthyes, Pleuronectiformes, Scophthalmidae). J Morphol 258, 8496.CrossRefGoogle ScholarPubMed
Zylberberg, L. & Nicolas, G. (1982). Ultrastructure of scales in a teleost (Carassius auratus L.) after use of rapid freeze-fixation and freeze-substitution. Cell Tissue Res 223, 349367.CrossRefGoogle Scholar
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