Scale calcification in the goldfish in vitro: histological and quantitative analysis
- 128 Downloads
- 5 Citations
Abstract
The external layer of a teleost fish scale is composed of type I collagen, an amorphous matrix substance and hydroxyapatite crystals. Calcification of this layer can be inhibited in the scale-regenerating process under calcium- and phosphate-deficient (CaDPD) conditions, and can be facilitated by incubation in physiological saline. The aim of this study was to evaluate this model of calcification using histological and quantitative analysis in order to promote further understanding of the mechanism of calcification in fish scales. We found that the external layer of the scales produced under CaDPD conditions contained more densely aligned collagen fibrils with a small amount of the amorphous matrix substance. The CaDPD scale contained only one-third of the amount of calcium and phosphate present in the control fish. After 4 hours of incubation, a two- to threefold increase in calcium content and a 1.5-fold increase in phosphate content were observed. Calcification proceeded in the external layer, and mineral deposits grew only in the electron-dense matrix substance. We conclude that this model would be suitable for studying the early process of fish scale calcification that occurs in the noncollagenous substance. The electron-dense substance may contain key molecules that promote calcification.
Keywords
Biomineralization Carasssius auratus Goldfish In vitro calcification Scale regenerationNotes
Acknowledgments
This study was supported in part by a Grant-in-Aid for Exploratory Research (No. 16658077) and a Twenty-First Century COE program awarded by the Ministry of Education, Culture, Sports, Science and Technology of Japan. The study was also supported in part by a Grant-in-Aid for Creative Scientific Research (No. 17GS0311) and a Research Grant for Young Scientists (No. 18-04520), awarded by the Japan Society for Promotion of Science.
References
- 1.Zylberberg L, Géraudie J, Meunier FJ, Sire J-Y (1992) Biomineralization in the integumental skeleton of the living lower vertebrates. In: Hall BK (ed) Bone 4. Bone metabolism and mineralization. CRC, Boca Raton, pp 171–224Google Scholar
- 2.Bereiter-Hahn J, Zylberberg L (1993) Regeneration of teleost fish scale. Comp Biochem Physiol 105A:625–641CrossRefGoogle Scholar
- 3.Huysseune A, Sire J-Y (1998) Evolution of patterns and processes in teeth and tooth-related tissues in non-mammalian vertebrates. Eur J Oral Sci 106:437–481PubMedGoogle Scholar
- 4.Sire J-Y, Akimenko M-A (2004) Scale development in fish: a review, with description of sonic hedgehoc (shh) expression in the zebrafish (Danio rerio). Int J Dev Biol 48:223–247CrossRefGoogle Scholar
- 5.Takagi Y, Ura K (2007) Teleost fish scales: a unique biological model for the fabrication of materials for corneal stroma regeneration. J Nanosci Nanotechnol 7:757–762CrossRefPubMedGoogle Scholar
- 6.Maekawa K, Yamada J (1970) Some histochemical and fine structural aspects of growing scales of the rainbow trout. Bull Fac Fish Hokkaido Univ 21:70–77Google Scholar
- 7.Sire J-Y, Géraudie J (1984) Fine structure of regenerating scales and their associated cells in the cichlid Hemichromis bimaculatus (Gill). Cell Tissue Res 237:537–547CrossRefGoogle Scholar
- 8.Zylberberg L, Nicolas G (1982) Ultrastructure of scales in teleosts (Carassius auratus L.) after use of rapid freeze-fixation and freeze-substitution. Cell Tissue Res 223:349–367CrossRefPubMedGoogle Scholar
- 9.Sauk JJ, Cocking-Johnson D, Cervenka VA, Van Kampen CL (1984) Noncollagenous phosphoprotein derived from teleostean fish-scales. Biochim Biophys Acta 798:199–203PubMedGoogle Scholar
- 10.Ekblom P, Vestweber D, Kemler R (1986) Cell–matrix interactions and cell adhesion during development. Ann Rev Cell Biol 2:27–47PubMedGoogle Scholar
- 11.Xie J, Baumann MJ, McCabe LR (2004) Osteoblasts respond to hydroxyapatite surfaces with immediate changes in gene expression. J Biomed Mater Res 71A:108–117CrossRefGoogle Scholar
- 12.Iguchi M (1985) Gyoruikousoshiki (hone uroko) no seichou to sekkaika ni okeru karusiumu to rin no kyodou ni kansuru kenkyu. (Studies on the actions of calcium and phosphate in the growth and calcification of fish bones and scales) (Ph.D. dissertation). Hokkaido University, Hakodate (in Japanese)Google Scholar
- 13.Yamane S, Iguchi M, Ogasawara T, Nakamura Y (1982) Effects of blockage of exogenous calcium and phosphorus on the calcium regulatory systems in goldfish. Comp Biochem Physiol 72A:709–713Google Scholar
- 14.Takagi Y, Hirano T, Yamada J (1989) Scale regeneration of tilapia (Oreochromis niloticus) under various ambient and dietary calcium concentrations. Comp Biochem Physiol 92A:605–608Google Scholar
- 15.Goldenberg H, Fernandez A (1966) Simplified method for the estimation of inorganic phosphorus in body fluids. Clin Chem 12:871–882PubMedGoogle Scholar
- 16.Yamada J (1971) A fine structural aspect of the development of scales in the chum salmon fry. Nippon Suisan Gakkaishi 37:18–29Google Scholar
- 17.Fouda MM (1979) Studies on scale regeneration in the Common goby, Pomatoschistus microps (Pisces). J Zool Lond 189:503–509CrossRefGoogle Scholar
- 18.Sire J-Y, Géraudie J (1983) Fine structure of developing scale in the Chichlid Hemichromis bimaculatus (Pisces, Teleostei, Perciformes). Acta Zool 64:1–8CrossRefGoogle Scholar
- 19.Takagi Y, Yamada J (1992) Effect of calcium deprivation on the metabolism of acellular bone in tilapia, Oreochromis niloticus. Comp Biochem Physiol 102A:481–485CrossRefGoogle Scholar
- 20.Anderson HC (1984) Mineralization by matrix vesicles. Scan Electron Microsc 2:953–964Google Scholar
- 21.Anderson HC (1995) Molecular biology of matrix vesicles. Clin Orthop Relat Res 314:266–280PubMedGoogle Scholar
- 22.Anderson HC (2003) Matrix vesicles and calcification. Curr Rheumatol Rep 5:222–226CrossRefPubMedGoogle Scholar
- 23.Arsenault AL, Frankland BW, Ottensmeyer FP (1991) Vectorial sequence of mineralization in the turkey leg tendon determined by electron microscopic imaging. Calcif Tissue Int 48:46–55CrossRefPubMedGoogle Scholar
- 24.Olson OP, Watabe N (1980) Studies on formation and resorption of fish scales. IV. Ultrastructure of developing scales in newly hatched fry of the Sheepshead minnow (Cyprinodon variegatus). Cell Tissue Res 211:303–316CrossRefPubMedGoogle Scholar
- 25.Schörnbörner AA, Boivin G, Baud CA (1979) The mineralization processes in teleost fish scales. Cell Tissue Res 202:203–212Google Scholar
- 26.Huffman NT, Keightley JA, Chaoying C, Midura RJ, Lovitch D, Veno PA, Dallas SL, Gorski JP (2007) Association of specific proteolytic processing of bone sialoprotein and bone acidic glycoprotein-75 with mineralization within biomineralization foci. J Biol Chem 282:26002–26013CrossRefPubMedGoogle Scholar
- 27.Gorski JP, Kremer EA, Chen Y (1996) Bone acidic glycoprotein-75 self-associates to form large macromolecular complexes. Connect Tissue Res 35:137–143CrossRefPubMedGoogle Scholar
- 28.Gorski JP, Kremer EA, Chen Y, Ryan S, Fullenkamp C, Delviscio J, Jensen K, McKee MD (1997) Bone acidic glycoprotein-75 self-associates to form macromolecular complexes in vitro and in vivo with the potential to sequester phosphate ions. J Cell Biochem 64:547–564CrossRefPubMedGoogle Scholar
- 29.Hunter GK, Hauschka PV, Poole AR, Rosenberg LC, Goldenberg HA (1996) Nucleation and inhibition of hydroxylapatite formation by mineralized tissue proteins. Biochem J 317:59–64PubMedGoogle Scholar
- 30.Halver JE, Coastes JA (1957) A vitamin test diet for long-term feeding studies. Prog Fish Cult 19:112–118CrossRefGoogle Scholar