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B2. Evolution and Development

Throughout millions of years of vertebrate mineralized tissue evolution, mammalian enamel structure has not just suddenly appeared but rather evolved gradually while incrementally increasing levels of complexity in tandem with the evolution of other features of the vertebrate dentition (Diekwisch et al. 2002, Satchell et al. 2002). For example, one property of enamel structure, the highly orderly arrangement of long and parallel crystals in symmetrically arranged enamel prisms, is unique for mammals. Invertebrates and non-mammalian vertebrates fall short of mammalian enamel structure in terms of 3D-complexity. Nevertheless, also reptilian and amphibian vertebrates display enamel-type outer tooth coverings. Reptilian enamel is distinguished from mammalian enamel by the lack of interprismatic enamel. Studies on the “true” enamel of the Australian Lungfish Neoceratodus show that basic mechanisms of enamel biomineralization are highly conserved throughout evolution and may date more than 500 Million years into the past (Satchell et al., 1999). Here we are using evolutionary biology as a means to understand complex biological phenomena such as enamel formation (Slavkin and Diekwisch 1996, 1997). As a first step, we have focused on the frog Rana pipiens as a model organism to study amphibian enamel development (Wang et al. 2005, Diekwisch et al. 2006). We have also cloned and sequenced several other amphibian and reptilian amelogenin sequences (Wang et al. 2006, Diekwisch et al. 2009).

Figure 1.

Enamel proteins and basic structures of enamel crystals are conserved in many vertebrates, including the lungfish. The Australian lungfish Neoceratodus forsteri belongs to the sarcopterygian clade of vertebrates and has a fossil record that dates back 500 Million years into the Devonian, suggesting that mechanisms of "true" enamel formation may have a history of at least 500 Million years. From: Satchell, P.G., Shuler, C.F., and Diekwisch, T.G.H. (2000). True enamel covering in teeth of the Australian lungfish Neoceratodus forsteri. Cell & Tiss. Res. 299, 27-37.

The Baltic zoologist Karl Ernst von Baer and the German zoologist Ernst Haeckel were among the first to call attention to the similarities between evolution and development and to use evolutionary biology as a means to understand complex biological phenomena (Slavkin and Diekwisch 1996, 1997; Diekwisch et al. 2002). We have studied a number of seemingly exotic animals to further understand tooth enamel development, among them:

(i) the onset of biomineralization in the sea urchin (Satchell et al. 1999)

(ii) the presence of "enamel-like" proteins and minerals in the earliest and most primitive vertebrates (hagfish)(Vahadi et al. 1996)

(iii) the dependence of "true" enamel crystals on the presence of amelogenin proteins in Pacific hornsharks (Gurinsky and Diekwisch 2000)

(iv) the presence of amelogenin in the reedfish Polypterus (Gurinsky et al. 1999)

(v) the presence of "true" enamel in the Australian Lungfish Neoceratodus, a living fossil that has remained unchanged since the early Devonian (500 Million. years ago)(Satchell et al. 1999).

Our studies have revealed that basic mechanisms of enamel biomineralization are highly conserved throughout evolution and may date more than 500 Million years into the past (Satchell et al., 2002). Currently we are utilizing some of the knowledge generated in our evolutionary studies to understand how to regenerate human enamel (enamel biomimetics).

Scientists

Drs. Paul Satchell and Xinping Wang have worked on earlier studies on the localization and cloning of enamel-related genes in lungfish, amphibians and reptiles. Currently, Drs. Tianquan Jin and Yoshihiro Ito are equally contributing to this area of research. In order to understand the role of protein sequence elongation during development, Dr. Yoshihiro Ito has made a number of mouse models that introduce amelogenins from other animals into the mouse amelogenin sequence. Dr. Tianquan Jin has focused on the role of the polyproline repeat elongation in vertebrate enamel formation.

Dr. Yoshohiro Ito

Dr. Tianquan Jin

Dr. Thomas Diekwisch

Related Publications

Diekwisch, T.G.H. Jin, T., Wang, X., Ito, Y., Schmidt, M.K., Druzinsky, R., Yamane, A., and Luan, X. (2009). Amelogenin evolution and tetrapod enamel structure. Frontiers of Oral Biology 13, 74-79.

Wang, X., Fan, J.-L., Ito, Y., Luan, X., and Diekwisch, T.G.H. (2006). Identification and characterization of a squamate reptilian amelogenin gene: Iguana iguana. J. Exp. Zool. Mol. Dev. Evol. 305B, 393-406.

Diekwisch, T.G.H., Wang, X., Fan, J.-L., Ito, Y., and Luan, X. (2006). Expression and characterization of a Rana pipiens amelogenin protein. Eur. J. Oral Sci. 114, 86- 92.

Wang, X., Ito Y., Luan, X., Yamane, A., and Diekwisch, T.G.H. (2005). Amelogenin sequence and enamel biomineralization in Rana pipiens. J. Exp. Zool. Mol. Dev. Evol. 304B:1-10.

Diekwisch, T.G.H., Berman, B.J., Anderton, X., Gurinsky, B., Ortega A.J., Satchell P.G., Williams, M., Arumugham C., Luan X., McIntosh J.E., Yamane A., Carlson, D.S., Sire, J.-Y., Simmer J.P., and Shuler, C.F. (in press). Membranes, Minerals, and Proteins of Developing Vertebrate Enamel. Microscopy Research Technique.

McIntosh J.E., Anderton, X., Flores-de-Jacoby, L., Carlson D.S., Shuler C.F., and Diekwisch, T.G.H. (in press). The Caiman Periodontium as an Intermediate Between Basal Vertebrate Ankylosis-Type Attachment and Mammalian "True" Periodontium. Microscopy Research Technique.

Satchell, P.G., Anderton, X., Ryu, O.H., Luan, X., Ortega, A.J., Opamen, R., Berman, B.J., Witherspoon, D.E., Gutmann, J.L., Yamane, A., Zeichner-David, M., Simmer, J.P., Shuler, C.F., and Diekwisch, T.G.H. (2002). Conservation and variation in enamel protein distribution during tooth development across vertebrates. Mol. Dev. Evol. 294, 91-106

Satchell, P.G., Shuler, C.F., and Diekwisch, T.G.H. (2000). True enamel covering in teeth of the Australian lungfish Neoceratodus forsteri. Cell & Tiss. Res. 299, 27-37.

Slavkin, H.C. and Diekwisch, T. (1997). Molecular strategies of tooth enamel formation are highly conserved during vertebrate evolution. Ciba Foundation Symposium 205 Dental Enamel. Wiley, Chichester: p. 73-84.

Slavkin, H.C. and Diekwisch, T. (1996). Evolution in tooth developmental biology: of morphology and molecules. Anat. Rec. 245, 131-150.

Diekwisch, T.G.H., Marches, F., Spears, R., and Dechow, P. (1995). Effect of enamel protein expression on enamel crystal formation: a phylogenetic study. R.J. Radlanski and H. Renz (Eds.) Proc. 10th Int. Symp. Dent. Morph., Berlin 1995, pp. 82-87.