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C. Development and Remodeling of the Tooth Attachment Apparatus

C.1. Evolution and Development of the Periodontium

The emergence of the vertebrate head has been tightly linked to a sophistication of feeding behavior and enhanced abilities to capture prey (Gans and Northcutt 1983). In tandem with an increasingly enlarged and specialized vertebrate brain, vertebrates have developed powerful jaws and muscles as well as complex tooth organs formed through epithelial-mesenchymal interactions. In order to efficiently anchor teeth in tooth-bearing elements, tooth roots and a number of attachment modes have evolved, among them proto-acrodont, acrodont, acro-protothecodont, pleurodont, and thecodent variations. In earlier studies we have demonstrated that mesenchymal periodontal tissues such as cementum, alveolar bone, and periodontal ligament are neural crest-derived entities that emerge from the dental follicle at the onset of root formation (Diekwisch 2001, 2002). In most teleosts and amphibians, teeth are attached to the jaw bone by ankylosis, while crocodilians and mammals feature a non-mineralized periodontal ligament (McIntosh et al. 2002, Luan et al. 2006, Luan et al. 2009). Our studies revealed that the ancient mosasaurs and the recent caimans represented two successive stages during the evolution from bony attachment to elastic periodontal ligament (Luan et al. 2006, 2009). Studies from our laboratory have also linked the presence of tooth roots to the presence of Hertwig’s Epithelial Root Sheath (HERS) during development (Luan et al. 2006).

Figure 1: Developing Tooth Root as Journal Cover Art for: Diekwisch, T.G.H. (2001). The developmental biology of cementum. Int. J. Dev. Biol. 45, 605-706.

Figure 2: Mosasaur Tooth Anatomy as Journal Cover Art for: Luan, X., Walker, C., Dangaria, S., Ito, Y., Druzinsky, R., Jarosius, K., Lesot, H., and Rieppel, O. (2009). The mosasaur tooth attachment apparatus as paradigm for the evolution of the gnathostome periodontium. Evolution and Development 11, 247-259.

Tissue Dynamics in the Developing Periodontium

During late stages of tooth development, the developing periodontium is a highly dynamic environment. There are at least four different processes of tissue remodeling occurring in various areas of the developing tooth and its integument. (i) Between the erupting tooth crown and the regional oral mucosa, the coronal segment of the alveolar bone crypt is reduced by osteoclasts to facilitate tooth crown eruption (Figure 2). (ii) In apical direction, the developing tooth root extends from the tooth cervix (Figure 2). (iii) Tissues of the dental follicle migrate in apical direction to aid the formation of periodontal ligament, root cementum, and alveolar bone (Figures 3 and 4). (iv) After the completion of tooth root development, the entire tooth moves in coronal direction, breaks the oral mucosa barrier, and erupts.

Figure 3: This figure illustrates the growth of the tooth root in apical direction (A-C) and the reduction of the alveolar bone crypt prior to tooth eruption (F-G). Also featured is the dental follicle, a connective tissue unit surrounding the developing tooth organ (H). From: Diekwisch (2002). Pathways and fate of migratory cells during late tooth organogenesis. Connective Tissue Research 43. 245-256.

Figure 4: Sagittal sections and 3D reconstructions of fluorescently labeled dental follicle tissues surrounding the developing tooth organ and migrating in apical direction during late tooth development. From: Diekwisch (2002). Pathways and fate of migratory cells during late tooth organogenesis. Connective Tissue Research 43. 245.

Figure 5

Figure 4. Model system illustrating tissue dynamics during late tooth development. Arrows indicate dental follicle cells migrating from the oral mucosa toward the tooth apex

Evolution of the Periodontium

The emergence of the vertebrate head has been tightly linked to a sophistication of feeding behavior and enhanced abilities to capture prey (Gans and Northcutt 1983). In tandem with an increasingly enlarged and specialized vertebrate brain, vertebrates have developed powerful jaws and muscles as well as complex tooth organs formed through epithelial-mesenchymal interactions. In order to efficiently anchor teeth in tooth-bearing elements, tooth roots and a number of attachment modes have evolved, among them proto-acrodont, acrodont, acro-protothecodont, pleurodont, and thecodent variations. In earlier studies we have demonstrated that mesenchymal periodontal tissues such as cementum, alveolar bone, and periodontal ligament are neural crest-derived entities that emerge from the dental follicle at the onset of root formation (Diekwisch 2001, 2002). In most teleosts and amphibians, teeth are attached to the jaw bone by ankylosis, while crocodilians and mammals feature a non-mineralized periodontal ligament (McIntosh et al. 2002, Luan et al. 2006, Luan et al. 2009). Our studies revealed that the ancient mosasaurs and the recent caimans represented two successive stages during the evolution from bony attachment to elastic periodontal ligament (Luan et al. 2006, 2009). Studies from our laboratory have also linked the presence of tooth roots to the presence of Hertwig’s Epithelial Root Sheath (HERS) during development (Luan et al. 2006).

Figure 6

Dr. Smit Dangaria

Dr. Xianghong Luan

Dr. Callum Ross

Walker, C.G.*, Dangaria, S.*, Ito, Y., Luan, X., and Diekwisch, T.G.H. (2010). Osteopontin is Required for Unloading-Induced Osteoclast Recruitment and Modulation of RANKL Expression during Tooth Drift-associated Bone Remodeling, but Not for Super-Eruption. BONE in 47, 1020-1029.

Luan, X., Walker, C., Dangaria, S., Ito, Y., Druzinsky, R., Jarosius, K., Lesot, H., and Rieppel, O. (2009). The mosasaur tooth attachment apparatus as paradigm for the evolution of the gnathostome periodontium. Evolution and Development 11, 247-259.

Luan, X., Ito, Y., and Diekwisch, T.G.H. (2006). Evolution and development of Hertwig’s Epithelial Root Sheath. Developmental Dynamics 235, 1167-1180.

Luan, X., Ito, Y., Dangaria, S., and Diekwisch, T.G.H. (2006). Dental follicle progenitor cell heterogeneity in the developing mouse periodontium. Stem Cells and Development 15, 595-608.

McIntosh J.E., Anderton, X., Flores-de-Jacoby, L., Carlson D.S., Shuler C.F., and Diekwisch, T.G.H. (2002). The caiman periodontium as an intermediate between basal vertebrate ankylosis-type attachment and mammalian “true” periodontium. Microscopy Research Technique 59, 449-459.

Diekwisch, T.G.H. (2002). Pathways and fate of migratory cells during late tooth organogenesis. Connective Tissue Research 43, 245-256.

Diekwisch, T.G.H. (2001). The developmental biology of cementum. Int. J. Dev. Biol. 45, 605-706.