Abstract
This is the first detailed report about the collar enamel of the teeth of Polypterus senegalus. We have examined the fine structure of the collar enamel and enamel organ of Polypterus during amelogenesis by light and transmission electron microscopy. An immunohistochemical analysis with an antibody against bovine amelogenin, an antiserum against porcine amelogenin and region-specific antibodies or antiserum against the C-terminus, middle region and N-terminus of porcine amelogenin has also been performed to examine the collar enamel matrix present in these teeth. Their ameloblasts contain fully developed Golgi apparatus, rough endoplasmic reticulum and secretory granules. During collar enamel formation, an amorphous fine enamel matrix containing no collagen fibrils is found between the dentin and ameloblast layers. In non-demineralized sections, the collar enamel (500 nm to 1 μm thick) is distinguishable from dentin, because of its higher density and differences in the arrangement of its crystals. The fine structural features of collar enamel in Polypterus are similar to those of tooth enamel in Lepisosteus (gars), coelacanths, lungfish and amphibians. The enamel matrix shows intense immunoreactivity to the antibody and antiserum against mammalian amelogenins and to the middle-region- and C-terminal-specific anti-amelogenin antibodies. These findings suggest that the proteins in the enamel of Polypterus contain domains that closely resemble those of bovine and porcine amelogenins. The enamel matrix, which exhibits positive immunoreactivity to mammalian amelogenins, extends to the cap enameloid surface, implying that amelogenin-like proteins are secreted by ameloblasts as a thin matrix layer that covers the cap enameloid after enameloid maturation.
Similar content being viewed by others
References
Bolte M, Clemen G (1992) The enamel of larval and adult teeth of Ambystoma mexicanum Shaw (Urodela: Ambystomatidae)—a SEM study. Zool Anz 228:167–173
Colbert EH, Morales M, Minkoff EC (2001) Colbert’s evolution of the vertebrates, 5th edn. Wily-Liss, New York
Davit-Beal T, Allizard F, Sire J-Y (2007) Enameloid/enamel transition through successive tooth replacements in Pleurodeles waltl (Lissamphibia, Caudata). Cell Tissue Res 328:167–183
Diekwisch TGH, Berman BJ, Anderton X, Gurinsky B, Ortega AJ, Satchell PG, Williams M, Arumugham C, Luan X, Mcintosh JE, Yamane A, Carlson DS, Sire J-Y, Shuler CF (2002) Membranes, minerals, and proteins of developing vertebrate enamel. Microsc Res Tech 59:373–395
Gurinsky B, Satchell P, Diekwisch TGH (1999) Teeth of the redfish Polypterus are covered by an outer layer different from enamel but containing enamel-like features such as enamel proteins and long and parallel crystals. J Dent Res 78:174
Herold RCB (1974) Ultrastructure of odontogenesis in the pike (Esox lucius). Role of dental epithelium and formation of enameloid layer. J Ultrastruct Res 48:435–454
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
Hsu SM, Aine LR, Fanger H (1981) A comparative study of the peroxidase-antiperoxidase method and an avidin-biotin complex method for studying polypeptide hormones with radioimmunoassay antibodies. Am J Clin Pathol 75:734–737
Hu C-C, Bartlett JD, Zhang CH, Qian Q, Ryu OH, Simmer JP (1996) Cloning, cDNA sequence, and alternative splicing of porcine amelogenin mRNAs. J Dent Res 75:1735–1741
Huysseune A, Takle H, Soenens M, Taerwe K, Witten PE (2008) Unique and shared gene expression patterns in Atlantic salmon (Salmo salar) tooth development. Dev Genes Evol 218:427–437
Ikeda T (1959) Histological and histogenetic studies on the teeth of fugu. J Stomatol Soc Jpn 26:1458–1476 (in Japanese)
Ishiyama M, Inage T, Shimokawa H (1993) Comparative immunohistochemistry on enamel proteins: in quest of the origin of tooth enamel. Arch Comp Biol Tooth Enamel 3:1–6 (in Japanese)
Ishiyama M, Inage T, Shimokawa H, Yoshie S (1994) Immunocytochemical detection of enamel proteins in dental matrix of certain fishes. Bull Inst Oceanogr (Monaco) 14–1:175–182
Ishiyama M, Mikami M, Shimokawa H, Oida S (1998) Amelogenin protein in tooth germs of the snake Elaphe quadrivirgata, immunohistochemistry, cloning and cDNA sequence. Arch Histol Cytol 61:467–474
Ishiyama M, Inage T, Shimokawa H (1999) An immunocytochemical study of amelogenin proteins in the developing tooth enamel of the gar-pike, Lepisosteus oculatus (Holostei, Actinopterygii). Arch Histol Cytol 62:191–197
Ishiyama M, Inage T, Shimokawa H (2001) Abortive secretion of an enamel matrix in the inner enamel epithelial cells during an enameloid formation in the gar-pike, Lepisosteus oculatus (Holostei, Actinopterygii). Arch Histol Cytol 64:99–107
Janvier P (1996) Early vertebrates. Oxford monographs on geology and geophysics, vol 33. Oxford University Press, Oxford
Kawasaki K (2009) The SCPP gene repertoire in bony vertebrates and graded differences in mineralized tissues. Dev Genes Evol 219:147–157
Kawasaki K, Suzuki T, Weiss KM (2005) Phenogenetic drift in evolution: the changing genetic basis of vertebrate teeth. Proc Natl Acad Sci USA 102:18063–18068
Kerr T (1960) Development and structure of some actinopterygian and urodele teeth. Proc R Soc Lond B Biol Sci 133:401–422
Kogaya Y (1995) Development of the hypermineralized tissue covering the tips of the larval urodele (Triturus pyrrhogaster) teeth and distribution pattern of sulfated glycoconjugates. Arch Comp Biol Tooth Enamel 4:15–20
Kogaya Y (1997) Histochemical and immunohistochemical characterization of the ganoine layer of Polypterus senegalus. Arch Comp Biol Tooth Enamel 5:23–29
Kogaya Y (1999) Immunohistochemical localisation of amelogenin-like proteins and type I collagen and histochemical demonstration of sulfated glycoconjugates in developing enameloid and enamel matrices of the larval urodele (Triturus pyrrhogaster) teeth. J Anat 195:455–464
Meinke DK (1982) A histological and histochemical study of developing teeth in Polypterus (Pisces, Actinopterygii). Arch Oral Biol 27:197–206
Moffatt P, Smith CE, St-Arnaud R, Nanci A (2008) Characterization of Apin, a secreted protein highly expressed in tooth-associated epithelia. J Cell Biochem 103:941–956
Park JC, Park JT, Son HH, Kim HJ, Jeong MJ, Lee CS, Dey R, Cho MII (2007) The amyloid protein APin is highly expressed during enamel mineralization and maturation in rat incisors. Eur J Oral Sci 115:153–160
Peyer B (1968) Comparative odontology. University of Chicago Press, Chicago
Poole DFG (1971) An introduction to the phylogeny of calcified tissues. In: Dahlberg AA (ed) Dental morphology and evolution. University of Chicago Press, Chicago, pp 65–79
Prostak K, Seifert P, Skobe Z (1989) Ultrastructure of developing teeth in the gar pike, (Lepisosteus). In: Fearnhead RW (ed) Tooth enamel V. Florence, Yokohama, pp 188–192
Reif W-E (1982) Evolution of dermal skeleton and dentition in vertebrates. The odontode regulation theory. Evol Biol 15:287–368
Sansom IJ, Smith MP, Armstrong HA, Smith MM (1992) Presence of the earliest vertebrate hard tissue in conodonts. Science 256:1308–1311
Sasagawa I (1995) Fine structure of tooth germs during the formation of enameloid matrix in Tilapia nilotica, a teleost fish. Arch Oral Biol 40:801–814
Sasagawa I, Ishiyama M (1988) The structure and development of the collar enameloid in two teleost fishes, Halichoeres poecilopterus and Pagrus major. Anat Embryol 178:499–511
Sasagawa I, Ishiyama M (2005a) Fine structural and cytochemical mapping of enamel organ during the enameloid formation stages in gars, Lepisosteus oculatus, Actinopterygii. Arch Oral Biol 50:373–391
Sasagawa I, Ishiyama M (2005b) Fine structural and cytochemical observations on the dental epithelial cells during cap enameloid formation stages in Polypterus senegalus, a bony fish (Actinopterygii). Connect Tissue Res 46:33–52
Sasagawa I, Ishiyama M, Kodera H (1984) Fine structure of the pharyngeal teeth in the Coelacanthid fish (Latimeria chalumnae). In: Fearnhead RW, Suga S (eds) Tooth enamel IV. Elsevier, Amsterdam, pp 462–466
Sasagawa I, Yokosuka H, Ishiyama M, Uchida T (2007) Fine structural and immunocytochemical observations on collar enamel and ganoine in Polypterus, an actinopterygian fish. Eur Cells Materials 14 (Suppl 2):127
Sasagawa I, Ishiyama M, Yokosuka H, Mikami M (2008) Fine structure and development of the collar enamel in gars, Lepisosteus oculatus, Actinopterygii. Front Mater Sci China 2:134–142
Sasagawa I, Ishiyama M, Yokosuka H, Mikami M, Uchida T (2009) Tooth enamel and enameloid in actinopterygian fish. Front Mater Sci China 3:174–182
Satchell PG, Shuler CF, Diekwisch TGH (2000) True enamel covering in teeth of the Australian lungfish Neoceratodus forsteri. Cell Tissue Res 299:27–37
Sawada T, Inoue S (2003) Ultrastructure of basement membranes in developing shark tooth. Calcif Tissue Int 72:65–73
Schmidt WJ, Keil A (1971) Polarizing microscopy of dental tissues. Pergamon, Oxford
Shellis RP, Miles AEW (1974) Autoradiographic study of the formation of enameloid and dentine matrices in teleost fishes using tritiated amino acid. Proc R Soc Lond B Biol Sci 185:51–72
Shellis RP, Miles AEW (1976) Observations with the electron microscope on enameloid formation in common eel (Anguilla anguilla; Teleostei). Proc R Soc Lond B Biol Sci 194:253–269
Shellis RP, Poole DFG (1978) The structure of the dental hard tissues of the Coelacanthid fish Latimeria chalumnae Smith. Arch Oral Biol 23:1105–1113
Shimokawa H, Wassmer P, Sobel ME, Termine JD (1984) Characterization of cell-free translation products of mRNA from bovine ameloblasts by monoclonal and polyclonal antibodies. In: Fearnhead RW, Suga S (eds) Tooth enamel IV. Elsevier, Amsterdam, pp 161–166
Sire J-Y (1994) Light and TEM study of nonregenerated and experimentally regenerated scales of Lepisosteus oculatus (Holostei) with particular attention to ganoine formation. Anat Rec 240:189–207
Sire J-Y (1995) Ganoine formation in the scales of primitive actinopterygian fishes, Lepisosteids and Polypterids. Connect Tissue Res 33:535–544
Sire J-Y (2010) Origin and relationships of amelogenin, and the evolutionary analysis of its conserved and variable regions in tetrapods. In: Goldberg M (ed) Amelogenins: multifaced proteins for dental and bone formation and repair. Bentham Science, Sharjah-Oak Park-Bussum-Karachi, pp 1–18
Slavkin HC, Diekwisch T (1996) Evolution in tooth developmental biology: of morphology and molecules. Anat Rec 245:131–150
Smith MM (1978) Enamel in the oral teeth of Latimeria chalumnae (Pisces: Actinistian): a scanning electron microscope study. J Zool Lond 185:355–369
Smith MM (1989) Distribution and variation in enamel structure in the oral teeth of sarcopterygians: its significance for the evolution of a protoprismatic enamel. Historical Biol 3:97–126
Smith MM (1992) Microstructure and evolution of enamel amongst osteichthyan fishes and early tetrapods. In: Smith P, Tchernov E (eds) Structure, function and evolution of teeth. Freund, London, pp 73–101
Smith MM, Hall BK (1990) Development and evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol Rev 65:277–373
Smith MM, Miles AEW (1971) The ultrastructure of odontogenesis in larval and adult urodeles; differentiation of the dental epithelial cells. Z Zellforsch 121:470–498
Toyosawa S, O’huigin C, Figueroa F, Tichy H, Klein J (1998) Identification and characterization of amelogenin genes in monotremes, reptiles, and amphibians. Proc Natl Acad Sci USA 95:13056–13061
Uchida T, Tanabe T, Fukae M (1989) Immunocytochemical localization of amelogenins in the deciduous tooth germs of the human fetus. Arch Histol Cytol 52:543–552
Uchida T, Tanabe T, Fukae M, Shimizu M (1991a) Immunocytochemical and immunochemical detection of a 32 kDa nonamelogenin and related proteins in procine tooth germs. Arch Histol Cytol 54:527–538
Uchida T, Tanabe T, Fukae M, Shimizu M, Yamada M, Miake K, Kobayashi S (1991b) Immunochemical and immunohistochemical studies, using antisera against porcine 25 kDa amelogenin, 89 kDa enamelin and the 13-17 kDa nonamelogenins, on immature enamel of the pig and rat. Histochemistry 96:129–138
Wang X, Ito Y, Luan X, Yamane A, Diekwisch TGH (2005) Amelogenin sequence and enamel biomineralization in Rana pipiens. J Exp Zool (Mol Dev Evol) 304B:177–186
Wistuba J, Greven H, Clemen G (2002) Development of larval and transformed teeth in Ambystoma mexicanum (Urodela, Amphibia): an ultrastructural study. Tissue Cell 34:14–27
Zylberberg L, Sire J-Y, Nanci A (1997) Immunodetection of amelogenin-like proteins in the ganoine of experimentally regenerating scales of Calamoichys calabaricus, a primitive actinopterygian fish. Anat Rec 249:86–95
Acknowledgements
We thank Dr. M. Fukae of Tsurumi University for donating the purified porcine amelogenin N-terminal segment.
Author information
Authors and Affiliations
Corresponding author
Additional information
This study was supported in part by Grants-in-Aid for Scientific Research nos. 16591844 and 21592329 from the Ministry of Education, Science, Sports, and Culture, Japan and by Research Promotion Grants (NDUF-07-12, -08-19, -09-18, -10-13) from the Nippon Dental University.
Rights and permissions
About this article
Cite this article
Sasagawa, I., Yokosuka, H., Ishiyama, M. et al. Fine structural and immunohistochemical detection of collar enamel in the teeth of Polypterus senegalus, an actinopterygian fish. Cell Tissue Res 347, 369–381 (2012). https://doi.org/10.1007/s00441-011-1305-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-011-1305-4