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Observations on Continuously Growing Roots of the Sloth and the K14-Eda

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Observations on Continuously Growing Roots of the Sloth and the K14-Eda EVOLUTION & DEVELOPMENT 10:2, 187–195 (2008) Observations on continuously growing roots of the sloth and the K14-Eda transgenic mice indicate that epithelial stem cells can give rise to both the ameloblast and root epithelium cell lineage creating distinct tooth patterns Mark Tummersà and Irma Thesleff1 Institute of Biotechnology, Viikki Biocenter, University of Helsinki, Finland ÃAuthor for correspondence (email: [email protected]) 1Current address and address at time of work for both authors: Institute of Biotechnology, P.O. Box 56, FIN-00014 University of Helsinki, Finland. SUMMARY Root development is traditionally associated that it acts as a functional stem cell niche. Similarly we show with the formation of Hertwig’s epithelial root sheath (HERS), that continuously growing roots represented by the sloth molar whose fragments give rise to the epithelial cell rests of and K14-Eda transgenic incisor maintain a cervical loop with a Malassez (ERM). The HERS is formed by depletion of the small core of stellate reticulum cells around the entire core of stellate reticulum cells, the putative stem cells, in the circumference of the tooth and do not form a HERS, and still cervical loop, leaving only a double layer of the basal give rise to ERM. We propose that HERS is not a necessary epithelium with limited growth capacity. The continuously structure to initiate root formation. Moreover, we conclude that growing incisor of the rodent is subdivided into a crown analog crown vs. root formation, i.e. the production of enamel vs. half on the labial side, with a cervical loop containing a large cementum, and the differentiation of the epithelial cells into core of stellate reticulum, and its progeny gives rise to enamel ameloblasts vs. ERM, can be regulated independently from producing. The lingual side is known as the root analog and the regulation of stem cell maintenance. This developmental gives rise to ERM. We show that the lingual cervical loop flexibility may underlie the developmental and evolutionary contains a small core of stellate reticulum cells and suggest diversity in tooth patterning. INTRODUCTION abrasive diets. For instance, a significant increase in the prev- alence of hypsodonty in commonly found mammals of many The teeth can be roughly subdivided into three groups. The taxonomic groups occurred during the Neogene due to an first group consists of brachydont or low-crowned teeth where increased aridity in the environment of Europe (Jernvall and the root is relatively long compared with the crown. This is Fortelius 2002). Hypselodonty can be seen as an extreme form the tooth type usually described in textbooks when describing of hypsodonty. The crown never stops growing and root for- root formation (Nanci 2003). The second group consists of mation is postponed indefinitely, but often with small tracts of hypsodont, or high–crowned, teeth, where the crown is high dentin covered with cementum acting as regions attaching the compared with the root. The third group consists of the tooth to the jaw bone with a periodontal ligament. hypselodont teeth, ever-growing or open-rooted teeth that Within closely related species there can be a variation be- grow continuously during the lifetime of the animal. Open- tween brachydont, hypsodont, and hypselodont teeth, indi- rooted refers solely to the large apical opening present in all cating that the regulation of crown height is rather flexible. continuously growing teeth and does not imply that the tooth For instance in closely related rodent species, the Mouse (Mus actually needs to have a root in a classical sense as described musculus) molar is brachydont, the molars of the Bank vole in the textbooks. and the Southern Red-backed vole (Clethrionomys glareolus, It is thought that brachydonty is the ancestral state Clethrionomys gapperi) are hypsodont, and the molars of the of mammalian teeth. During evolution the shift from Sibling vole and Meadow vole (Microtus rossiaemeridionalis brachydont to hypsodont teeth is a common phenomenon and Microtus clethrionomys) are hypselodont (Phillips and (Macfadden 2000). This trend is often initiated by environ- Oxberry 1972; Tummers and Thesleff 2003). It has been mental pressures. Teeth with higher crowns last longer with proposed that the switch from hypsodont to hypselodont & 2008 The Author(s) 187 Journal compilation & 2008 Blackwell Publishing Ltd. 188 EVOLUTION & DEVELOPMENT Vol. 10, No. 2, March^April 2008 between the microtine genera of Clethrionomys and Microtus basal epithelium is left that is known as Hertwig’s epithelial is caused by the maintenance of a regenerative unit, possibly root sheath (HERS) (Thomas 1995). As HERS proliferates, due to a simple mutation (Phillips and Oxberry 1972), or that the growing epithelial sheet becomes discontinuous and forms increased crown height results from delayed termination/ a fenestrated network lining the root surface known as the cytodifferentiation and that hypselodonty is an extreme out- epithelial cell rests of Malassez (ERM) (Ten Cate 1996). come of such a delay (von Koenigswald 1982). We have more Through this network the follicular mesenchyme cells can recently proposed that the increase in crown height is a result migrate to the dentin surface and differentiate into cemento- of prolonging the period during which the epithelial stem cell blasts depositing the cementum. The ERM functions in the niche is maintained (Tummers and Thesleff 2003). induction of cementoblast differentiation and regulation of During classic root formation the dental epithelium of their function (Thomas 1995; Bosshardt and Schroeder 1996; the cervical loop undergoes some major structural changes Kagayama et al. 1998). Fibers of the periodontal ligament are (Fig. 1). The cervical loop is created during crown morpho- embedded in the cementum and connect the root to the jaw genesis and with root initiation loses the central core of bone. HERS forms in brachydont and hypsodont teeth when stellate reticulum and stratum intermedium cells, including the root formation is initiated and crown formation ends, and its putative epithelial stem cells (Ten Cate 1961; Starkey 1963; transition to ERM is generally regarded as a typical feature of Harada et al. 1999; Harada et al. 2002). A double layer of root formation. Interestingly, the continuously growing ro- dent incisor is subdivided into two halves. The labial side is called crown analog because it produces ameloblasts and enamel, whereas the lingual half is called root analog, because its epithelium fragments and forms ERM and cementum is produced. Both root and crown analogs are generated con- tinuously by the apical end of the incisor. It has been sug- gested that the labial cervical loop of the crown analog in the incisor is a specialized stem cell niche providing the epithelial progeny for the entire incisor and that lingually HERS is formed (Ohshima et al. 2005). This last notion is questioned by the existence of a special type of continuously growing or hypselodont teeth as is rep- resented by the sloth molar. The dentition of the contemporary sloth species is heavily modified, lacking both incisors and ca- nines. Sloth teeth are open-rooted, grow continuously, and at the same time lack enamel (Naples, 1982). In juvenile speci- Fig. 1. Formation of the cervical loop, the putative epithelial stem mens the tooth erupts as a simple cone. In adult specimens the cell niche, during early development and its fate in the mouse molar cap of the dentin is worn off, leaving a hard shell of dentin with and incisor. During early stages of morphogenesis all teeth go a soft pulp in the center. The edges of the dentin get sharper through the same developmental stages (initiation, bud stage, cap stage, and the bell stage) generating the crown. During bud stage a with age due to wear (Naples 1982). Similarly, the dentition of core of loosely arranged epithelium is formed in the center of the the mouse, as a representative of the rodents, is also heavily bud. During the cap stage the cervical loop is formed, a protrusion modified during evolution, with only two incisors in each jaw, from the bud that envelopes the condensed dental papilla me- followed by a diastema region lacking teeth, and three molars. senchyme. The cervical loop is extended during the bell stage and The transgenic K14-Eda mouse has ectodysplasin (Eda) the inner enamel epithelium starts to differentiate into ameloblasts. During the late bell stage crown morphology is established and expressed under the keratin 14 promoter leading to an ex- cells producing mineralized tissues differentiate terminally. Cell cessive production of Eda throughout the ectoderm from E10 differentiation starts from the cusp tips and extends toward the onwards, including the oral and dental epithelium (Mustonen base. Enamel is deposited by ameloblasts and dentin by odonto- et al. 2003). The constitutive expression of Eda in the dental blasts. In the mouse molar the cervical loop loses its core of stellate epithelium leads to the formation of supernumerary molars reticulum, the putative stem cells, and forms the HERS, which fragments into ERM, typical of a root. On the labial side of the and the loss of enamel on crown analog of the incisors. This mouse incisor the cervical loop is maintained as a stem cell niche transgenic mouse line therefore has possibly transformed its and it keeps giving rise to ameloblasts. On the lingual side no incisor into a continuously growing root, and serves in this ameloblasts differentiate and instead ERM is formed. The fate of paper as a model system for continuously growing roots. If the lingual cervical loop is unclear, although it has been suggested HERS is required for the production of root epithelium, these that HERS is present (Ohshima et al. 2005). ERM, epithelial cell rests of Malassez; HERS, Hertwig’s epithelial root sheath; iee, teeth would not have a cervical loop and a stem cell niche.
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