Summary
The composition and morphology of crystals formed in fish enameloid were investigated at various developmental stages. Species studied were shark, skate, red seabream, puffer, and carp. For comparative purposes, mammalian enamel samples were obtained from developing porcine teeth and erupted human teeth. Chemical and physical analyses (FTIR, X-ray diffraction, and electron microprobe) indicated that the mineral phase of enameloid in elasmobranch and teleost fish was most adequately characterized as fluoridated carbonatoapatites but that the degree of fluoridation and carbonation of the apatite latice varied among species and, within species, with the developmental stage. High resolution electron microscopy demonstrated differences in the nature and morphology of the initially precipitating crystallites of the enameloids of elasmobranch as compared with those of teleost fish. The elasmobranch enameloid contained high levels of fluoride (2.5% wt or more) at the beginning of precipitation and its mineralization was characterized by the initial formation and subsequent growth of prismatic apatite crystals having hexagonal (frequently equilateral) cross-sectional areas. In contrast, the initially precipitating crystallites in the teleost fish appeared as thin ribbons, like those commonly reported in mammalian enamel. The crystal morphology of the teleost fish enameloid may be related to the low fluoride contents maintained in the early stages of enameloid formation. However, the growth process of enameloid crystallites varied within the teleostei depending on the fluoride accretion during the mineralization stages. In the seabream enameloid (the highfluoride group), the growth on the side planes of the apatitic prisms was accelerated with increasing fluoride concentration in the tissue; the resulting crystallites had equilateral hexagonal cross sections. The morphology and growth of enameloid crystallites in puffer and carp (the low-fluoride group) were similar to those reported in mammalian enamel. However, appreciable differences existed between the enameloid of this fish group and the mammalian enamel with respect to carbonation, fluoridation, and central defects of their crystallites. The overall results support the contention that fluoride significantly affects the morphology and structure of enameloid crystals, most probably by increasing the driving force for carbonatoapatite formation and by accelerating hydrolysis of possible acidic precursors.
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References
Bawden JW, Merriff DH, Deaton TG (1981) In vitro study of calcium-45 and phosphorus-32 uptake in developing rat enamel using quantitative methods. Arch Oral Biol 26:477–482
Crenshaw MA, Takano Y (1982) Mechanisms by which the enamel organ controls calcium entry into developing enamel. J Dent Res 61(Sp Iss):1574–1579
Aoba T, Moreno EC (1987) The enamel fluid in the early secretory stage of porcine amelogenesis: chemical composition and saturation with respect to enamel mineral. Calcif Tissue Int 41:86–94
Moreno EC, Aoba T (1987) Calcium binding in enamel fluid and driving force for enamel mineralization in the secretory stage of amelogenesis. Adv Dent Res 1:245–251
Termine JD, Belcourt AB, Christner PJ, Conn KM, Nylen MV (1980) Properties of dissociatively extracted fetal tooth matrix proteins. I. Principal molecular species in developing bovine enamel. J Biol Chem 255:9760–9768
Robinson C, Kirkham J (1984) Enamel matrix components. Alterations during development and possible interactions with the mineral phase. In: Fearnhead RW, Suga S (ed) Tooth enamel IV, Elsevier, Amsterdam, pp 261–265
Aoba T, Fukae M, Tanabe T, Shimizu M, Moreno EC (1987) Selective adsorption of porcine amelogenins onto hydroxyapatite and their inhibitory activity on hydroxyapatite growth in supersaturated solutions. Calcif Tissue Int 41:281–289
Trautz OR, Klein E, Addelston HK (1952) Variations in the x-ray diffractograms of dental enamel of man and shark. J Dent Res 31:472–473
Glas JE (1962) Studies on the ultrastructure of dental enamel. VI: crystal chemistry of shark's teeth. Odont Rev 13:315–326
Garant P (1970) An electron microscopic study of the crystal-matrix relationship in the teeth of the dogfishSqualus acanthias. J Ultrastruct Mol Struct Res 30:441–449
Daculsi G, Kerebel LM (1980), Ultrastructural study and comparative analysis of fluoride content of enameloid in seawater and fresh-water sharks. Arch Oral Biol 25:145–151
Shellis RP, Miles AEW (1976) Observations with the electron microscope on enameloid formation in the common eel (Anguilla anguilla: Teleostei). Proc R Soc Lond (B) 194:253–269
Fearnhead RW (1979) Matrix-mineral relationships in enamel tissues. J Dent Res 58(B):909–916
Gaunt WA, Miles AEW (1967) Fundamental aspects of tooth morphogenesis. In: Structural and chemical organization of teeth. Vol. 1. Academic Press, New York, pp 151–198
Slavkin HC, Zeichner-David M, Ferguson MWJ, Termine JD, Graham E, MacDougall M, Bringas P Jr, Bessem C, Grodin M (1982) Phylogenetic and immunogenetic aspects of enamel proteins. In: Riviere GR, Hildemann W (eds) Oral immunogenetics and tissue transplantation. Elsevier/North Holland, New York, pp 241–251
Herold R, Rosenbloom J, Granovsky M (1989) Phylogenetic distribution of enamel proteins: immunohistochemical localization with monoclonal antibodies indicates the evolutionary appearance of enamelins prior to amelogenins. Calcif Tissue Int 45:88–94
Samuel N, Bringas P Jr, Santos V, Nanci A, Slavkin HC (1983) Selachian tooth development. I. Histogenesis, morphogenesis and anatomical features inSqualus acanthias. J Craniofac Genet Dev Biol 3:29–42
Garant P (1970) Observations on the ultrastructure of the ectodermal component during odontogenesis inHelostoma temmincki. Anat Rec 166:167–188
Herold RCB (1974) Ultrastructure of odontogenesis in the pike (Esox lucius). Role of dental epithelium and formation of enameloid layer. J Ultrastruct Mol Struct Res 48:435–454
Kerebel B, Daculsi G, Renaudin S (1977) Ameloblast, ultrastructure during enameloid formation in selachians. Biol Cell 28:125–130
Everett MM, Miller WA (1981) Histochemistry of lower vertebrate calcified structures. I. Enamel of the dogfishSqualus acanthias compared with mammalian enamel and homologous dentine. J Morphol 170:95–111
Nanci A, Bringas P Jr, Samuel N, Slavkin HC (1983) Selachian tooth development. 3. Ultrastructural features of secretory amelogenesis inSqualus acanthias. J Craniofac Genet Dev Biol 3:53–74
Kemp NE (1985) Ameloblastic secretion and calcification of the enamel layer in shark teeth. J Morphol 184:215–230
Prostak K, Skobe Z (1985) The effects of colchicine on the ultrastructure of the dental epithelium and odontoblasts of teleost tooth buds. J Craniofac Genet Dev Biol 5:75–88
Prostak K, Skobe Z (1986) Ultrastructure of the dental epithelium during enameloid mineralization in a teleost fish.Cichlasoma Cyanoguttatum. Arch Oral Biol 31:73–85
Prostak K, Skobe Z (1986) Ultrastructure of the dental epithelium and odontoblasts during enameloid matrix deposition in Cichlid teeth. J Morphol 187:159–172
Prostak K, Skobe Z (1988) Ultrastructure of odontogenic cells during enameloid matrix synthesis in tooth buds from an Elasmobranch,Raja erinacae. Am J Anat 182:59–72
Prostak K, Seifert P, Skobe Z (1989) The penetration of exogenous tracers through the enameloid organ of developing teleost fish teeth. Tissue Cell 21:419–430
Suga S, Wada K, Ogawa M (1978) Mineralization pattern and fluoride distribution of the developing and matured enameloid of the shark. Jpn J Oral Biol 20:67–81
Suga S, Wada K, Ogawa M (1980) Fluoride concentration in the enameloid of fishes. In: Omori M, Watabe N (eds) The mechanisms of biomineralization in animals and plants. Tokai University Press, Tokyo, pp 229–240
Suga S, Wada K, Ogawa M (1981) Fluoride concentration in teeth of tetraodontiform fishes and its phylogenetic significance. Jpn J Ichthyol 28:304–312
Suga S, Wada K, Ogawa M (1981) Fluoride concentration in the enameloid of fish teeth and its relationship to the phylogeny of fishes. In: Binder K, Hohenegger M (eds) Fluoride metabolism. Verlag Wilhelm Maudrich, Wien, pp 79–88
Suga S, Taki Y, Wada K (1983) Fluoride concentration in the teeth of Perciform fishes and its phylogenetic significance. Jpn J Ichthyol 30:81–93
Suga S (1983) Comparative histology of progressive mineralization pattern of developing enamel. In: Suga S (ed) Mechanisms of tooth enamel formation. Quintessence, Tokyo, pp 167–203
Suga S (1984) The role of fluoride and iron in mineralization of fish enameloid. In: Fearnhead RW, Suga S (eds) Tooth enamel. IV. Elsevier, Amsterdam, pp 472–477
Lowenstam HA, Weiner S (1989) On biomineralization. Oxford University Press, New York, Oxford, pp 175–188
Aoba T, Moreno EC (in press) Changes in the nature and composition of enamel mineral during porcine amelogenesis. Calcif Tissue Int 46
McClellan GH, Lehr JR (1969) Crystal-chemical investigations of natural apatites. Amer Min 54:1374–1391
Elliott JC (1964) The crystallographic structure of dental enamel and related apatites. Ph.D. Thesis, University of London, London, England
Holcomb DW, Young RA (1980) Thermal decomposition of human tooth enamel. Calcif Tissue Int 31:189–201
LeGeros RZ (1981) Apatites in biological systems. Prog Crystal Growth Charact 4:1–45
Doi Y, Eanes ED (1984) Transmission electron microscopic study of calcium phosphate formation in supersaturated solutions seeded with apatite. Calcif Tissue Int 36:39–47
Aoba T, Yoshioka C, Yagi T, Moreno EC (1984) High-resolution electron microscopy of hydroxyapatite grown in dilute solutions. J Dent Res 63:1348–1354
Kerebel B, Daculsi G, Kerebel LM (1979) Ultrastructural studies of enamel crystallites. J Dent Res 58B:844–850
LeGeros RZ, Suga S (1980) Crystallographic nature of fluoride in enameloids of fish. Calcif Tissue Int 32:169–174
Aoba T, Moreno EC (1989) Mechanism of amelogenetic mineralization in minipig secretory enamel. In: Fearnhead RW (ed) Tooth enamel V. Florence Publishers, Yokohama. pp 163–167
Poole DFG (1971) An introduction to the phylogeny of calcified tissues. In: Dahlberg AA (ed) Dental morphology and evolution. Chicago University Press, Chicago, p 65
Kemp NE, Park JH (1974) Ultrastructure of the enamel layer in developing teeth of the sharkCarcharhinus menisorrah. Arch Oral Biol 19:633–644
Tanabe T, Aoba T, Moreno EC (1988) Effect of fluoride in the apatitic lattice on adsorption of enamel proteins onto calcium apatites. J Dent Res 67:536–542
Brown WE, Mathew M, Tung MS (1981) Crystal chemistry of octacalcium phosphate. Prog Crystal Growth Charact 4:59–87
Nelson DGA, Barry JC (1989) High resolution electron microscopy of nonstoichiometric apatite crystals. Anat Rec 224:265–276
Weatherell JA, Deutsch D, Robinson C, Hallsworth AS (1975) Fluoride concentrations in developing enamel. Nature 256:230–232
Aoba T, Collins J, Moreno EC (1989) Possible function of matrix proteins in fluoride incorporation into enamel mineral during porcine amelogenesis. J Dent Res 68:1162–1168
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Miake, Y., Aoba, T., Moreno, E.C. et al. Ultrastructural studies on crystal growth of enameloid minerals in elasmobranch and teleost fish. Calcif Tissue Int 48, 204–217 (1991). https://doi.org/10.1007/BF02570556
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DOI: https://doi.org/10.1007/BF02570556