Minerals and aligned collagen fibrils in tilapia fish scales: Structural analysis using dark-field and energy-filtered transmission electron microscopy and electron tomography

Microscopy and Microanalysis

Volumn 17, Issue 5, 2011, Pages 788-798

  Okuda, Mitsuhiro ^a   Ogawa, Nobuhiro ^a   Takeguchi, Masaki ^a   Hashimoto, Ayako ^a   Tagaya, Motohiro ^a   Chen, Song ^a   Hanagata, Nobutaka ^a   Ikoma, Toshiyuki ^b  

^a NATIONAL INSTITUTE FOR MATERIALS SCIENCE   (Japan)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

biomineralization; collagen; electron tomography; energy filtered TEM; fish scale; STEM tomography

Indexed keywords

COLLAGEN; MINERAL;

ANIMAL; ARTICLE; ELECTRON TOMOGRAPHY; ENERGY FILTERED TRANSMISSION ELECTRON MICROSCOPY; INTEGUMENTARY SYSTEM; TILAPIA; ULTRASTRUCTURE;

ANIMALS; COLLAGEN; ELECTRON MICROSCOPE TOMOGRAPHY; INTEGUMENTARY SYSTEM; MICROSCOPY, ENERGY-FILTERING TRANSMISSION ELECTRON; MINERALS; TILAPIA;

TILAPIA;

EID: 80054917151     PISSN: 14319276     EISSN: 14358115     Source Type: Journal    
DOI: 10.1017/S1431927611011949     Document Type: Article

References (47)

1. Anderson, H.C. (2003). Matrix vesicles and calcification. Cur Rheumatol Rep 5, 222-226.
2. Ascenzi, A., Bonucci, E. & Bocciarelli, D.S. (1965). An electron microscope study of osteon calcification. J Ultrastruct Res 12, 287-303.
3. 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, 22-33. (Pubitemid 36269103)
4. Bereiter-Hahn, J. & Zylberberg, L. (1993). Regeneration of teleost fish scale. Comp Biochem Physiol 105, 625-641. (Pubitemid 23224257)
5. 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, 137-143.
6. 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, 110-114.
7. 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, 282-286. (Pubitemid 19032277)
8. 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, 2291-2313. (Pubitemid 13166812)
9. 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, 486-491. (Pubitemid 46431213)
10. Fujisawa, R., Nodasaka, Y. & Kuboki, Y. (1995). Further characterization of interaction between bone sialoprotein (BSP) and collagen. Calcif Tissue Int 56, 140-144.
11. 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, 46-50. (Pubitemid 44839181)
12. Gregori,G., Kleebe,H.J., Mayer, H. & Ziegler, G. (2006). EELS characterisation of b-tricalcium phosphate and hydroxyapatite. J Eur Ceram Soc 26, 1473-1479. (Pubitemid 43245419)
13. 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, 327-333. (Pubitemid 36638266)
14. 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.
15. Kadler, K.E., Holmers, D.F., Trotter, J.A. & Chapman, J.A. (1996). Collagen fibril formation. Biochem J 316, 1-11. (Pubitemid 26158194)
16. 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, 345-362. (Pubitemid 33038555)
17. Kohler, D.M., Crenshaw, M.A. & Arsenault, A.L. (1994). Threedimensional analysis of mineralizing turkey leg tendon: Matrix vesicle-collagen relationships. Matrix Biol 14, 543-552.
18. 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, 188-223. (Pubitemid 8392855)
19. 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, 227-268. (Pubitemid 12127625)
20. 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, 185-206. (Pubitemid 8121677)
21. 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 threedimensional imaging. J Struct Biol 117, 24-35. (Pubitemid 26285624)
22. Landis, W.J., Silver, F.H. & Freeman, J.W. (2006). Collagen as a scaffolding for biomimetic mineralization. J Mater Chem 16, 1495-1503.
23. 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 highvoltage electron-microscopic tomography and graphic imagereconstruction. J Struct Biol 110, 39-54.
24. Lees, S. & Prostak, K. (1988). The locus of mineral crystallites in bone. Connect Tissue Res 18, 41-54.
25. 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, 445-454.
26. 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, 37-41. (Pubitemid 47407671)
27. Liou, A.C., Chen, A.Y., Lee, H.Y. & Bow, L.S. (2004). Structural characterization of nano-sized calcium deficient apatite powders. Biomaterials 25, 189-196.
28. Martin, R.B., Burr, D. & Sharkey, N. (1998). Skeletal Tissue Mechanics. New York: Springer-Verlag.
29. Midgly, P.A. & Weyland, M. (2003). 3D electron microscopy in the physical sciences: The development of Z-contrast and EFTEM tomography. Ultramicroscopy 96, 413-431. (Pubitemid 36840895)
30. 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, 278-284. (Pubitemid 23103358)
31. 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, 665-668.
32. Olson, O.P. & Watabe, N. (1980). Studies on formation and resorption of fish scales. Cell Tissue Res 211, 303-316.
33. 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, 77-116. (Pubitemid 350051885)
34. 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, 409-422. (Pubitemid 10196039)
35. Parfitt, G.J., Pinali, C., Young, R.D., Quantock, A.J. & Knupp, C. (2010). Three-dimensional reconstruction of collagenproteoglycan interactions in the mouse corneal stroma by electron tomography. J Struct Biol 170, 392-397.
36. Petruska, J.A. & Hodge, A.J. (1963). In Aspects of Protein Structure, Ramachandran, G.N. (Ed.), pp. 289-300. New York: Academic Press.
37. Petruska, J.A. & Hodge, A.J. (1964). A subunit model for the tropocollagen macromolecule. Proc Natl Acad Sci USA 51, 871-876.
38. 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), 329-341.
39. Schönbörner, A.A., Boivin, G. & Baud, C.A. (1979). The mineralization process in teleost fish scales. Cell Tissue Res 202, 203-212. (Pubitemid 10195445)
40. 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, 495-501.
41. Weiner, S., Traub, W. & Wagner, D. (1993). Lamellar bone: Structure-function relations. J Struct Biol 126, 241-255.
42. Weiner, S. & Wagner, H.D. (1998). The material bone: Structure mechanical function relations. Ann RevMater Sci 28, 271-298. (Pubitemid 128631421)
43. 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, 49-66.
44. Zylberberg, L., Bereiter-Hahn, J. & Sire, J.Y. (1988). Cytoskeletal organization and collagen orientation in the fish scales. Cell Tissue Res 253, 597-607.
45. 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, 273-285.
46. 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, 84-96. (Pubitemid 37195957)
47. 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, 349-367. (Pubitemid 12118686)