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Evolution and Developmental Diversity of Tooth Regeneration

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Seminars in Cell & Developmental Biology 25–26 (2014) 71–80 Contents lists available at ScienceDirect Seminars in Cell & Developmental Biology j ournal homepage: www.elsevier.com/locate/semcdb ଝ Evolution and developmental diversity of tooth regeneration a b,∗ Abigail S. Tucker , Gareth J. Fraser a Department of Craniofacial Development and Stem Cell Biology, Floor 27 Guy’s Tower, Guys Campus, King’s College London, SE1 9RT, UK b Department of Animal and Plant Sciences, Alfred Denny Building, Western Bank, University of Sheffield, S10 2TN, UK a r t i c l e i n f o a b s t r a c t Article history: This review considers the diversity observed during both the development and evolution of tooth replace- Available online 6 January 2014 ment throughout the vertebrates in a phylogenetic framework from basal extant chondrichthyan fish and more derived teleost fish to mammals. We illustrate the conservation of the tooth regeneration process Keywords: among vertebrate clades, where tooth regeneration refers to multiple tooth successors formed de novo Tooth development for each tooth position in the jaws from a common set of retained dental progenitor cells. We discuss the Stem cells conserved genetic mechanisms that might be modified to promote morphological diversity in replace- Regeneration ment dentitions. We review current research and recent progress in this field during the last decade that Tooth replacement have promoted our understanding of tooth diversity in an evolutionary developmental context, and show Dental lamina how tooth replacement and dental regeneration have impacted the evolution of the tooth-jaw module Vertebrate diversity in vertebrates. © 2014 Elsevier Ltd. All rights reserved. Contents 1. Introduction . 71 2. Tooth replacement: an ancient system . 72 3. Replacing a vertebrate dentition . 72 3.1. Fish . 72 3.1.1. Chondrichthyans (sharks, rays and their relatives). 72 3.1.2. Osteichthyans (bony fishes). 73 3.1.3. Dental diversity through replacement in fish dentitions . 73 3.2. Amphibians and reptiles . 73 3.2.1. Amphibians. 73 3.2.2. Reptiles . 75 3.3. Mammals . 76 4. The dental lamina as a conserved feature of replacement dentitions . 77 5. The conserved genetic basis for tooth replacement . 77 6. Conclusions . 78 Acknowledgements . 79 References . 79 1. Introduction Vertebrate animals show morphological diversity that is the product of change during the process of evolution based on developmental modulation; this is the basis of Evo-Devo. For a complete understanding of the dentition, evolutionary and devel- ଝ This is an open-access article distributed under the terms of the Creative opmental studies are essential for the appreciation of complexities Commons Attribution License, which permits unrestricted use, distribution and that have led to changes in tooth development, form, function and reproduction in any medium, provided the original author and source are credited. ∗ regeneration. Given the diversity in form observed among verte- Corresponding author. Tel.: +44 114 222 4317. brates, the dentition presents an intriguing paradox; while there E-mail addresses: [email protected] (A.S. Tucker), g.fraser@sheffield.ac.uk (G.J. Fraser). is great structural and developmental conservation of tooth unit 1084-9521/$ – see front matter © 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.semcdb.2013.12.013 72 A.S. Tucker, G.J. Fraser / Seminars in Cell & Developmental Biology 25–26 (2014) 71–80 formation, there is vast diversity of form, replacement potential 2. Tooth replacement: an ancient system and module integration, i.e. the combined system of both jaws and teeth. The dentition has remained extremely similar throughout The teeth have been relatively unchanged throughout the evo- vertebrate evolution, both in terms of the genetic basis and the lution of vertebrates. Their development is governed by a highly structure of the unit tooth; however vertebrates have highly diverse conserved network of genes. This ‘dental network’ controls oral dentitions and capacities for dental regeneration. This contradic- epithelial and mesenchymal cells towards the production of a tooth tory notion is ideal for the field of ‘Evolutionary Developmental composed for the most part of dentine and enamel-like mineralised Biology’; how does a system so highly conserved as the dentition tissues, surrounding an innervated, vascularised pulp cavity. The become so vastly modified to provide the diversity of dental form conservation of the tooth unit is extremely stable with the excep- observed among vertebrates? tion of those vertebrates, like the birds (Class Aves), turtles (order In this context we define dental regeneration as repeated and Testudines/Chelonii) and some mammals (including the anteaters; cyclical induction of tooth germs, from a set of well-maintained suborder Vermilingua) that have lost their tooth building capability dental progenitor cells at each tooth position in the jaw, primed and are for the most part, toothless. These toothless clades have all to replace each functional tooth in a one-for-one (a single replace- secondarily lost their teeth with fossil evidence showing toothed ment tooth is formed at any one time for a single tooth position) or forms of most groups [6,15]. Interestingly, there are many verte- many-for-one (where many replacement teeth are formed ahead brates that do develop an initial and complete set of teeth that are of function for a single tooth position) capacity. This concept sug- lost and never replaced. In some groups, these first generation teeth gests that there are two basic strategies for tooth replacement: (1) are replaced by keratinous projections that develop in place of the the formation of one replacement tooth before replacing the func- teeth and act as a substitute dentition ([6] as observed in the duck- tional tooth after which the next single replacement forms and (2) billed platypus – Ornithorhynchus anatinus), while in other animals many teeth are formed in a developmental time series to replace a alternative feeding devices are adopted that do not require a den- single functional tooth. Teeth are replaced during an animal’s life tition, i.e. filter feeding mechanisms observed in baleen whales in order to counter the problems of tooth wear, or tooth damage, (suborder Mysticeti [6]) and some ray-finned fishes, e.g. Acipenser- while also providing the possibility of change to tooth morphology iformes [16]. and complexity, which might be required during the lifetime of The basal tooth condition for early vertebrates was likely poly- the animal, for example, changing diets from larval to adult forms. phyodonty [17–21]. The capacity for teeth to replace themselves Not all animals replace their dentition, and as such are classed is a potential defining character of true teeth, and distinguishes as monophyodont (single generation of functional teeth). At the them from dermal tooth-like elements (odontodes). Continuous opposite end of the spectrum are the polyphyodonts, which replace tooth replacement is an ancient biological process and for this their teeth continuously. How the dentition is replaced has been a progenitor cells must be maintained. This ancient regenerative sys- largely forgotten subject, partly because the standard animal mod- tem must have utilised a population of stem cells that has been els used in developmental biology are not ideal for the study of conserved for the same function throughout vertebrate evolution. tooth replacement. The mouse, the main mammalian model for Vertebrates have reduced the number of tooth sets over time with development, does not have the capacity to replace its dentition de fewer teeth in the mouth at any one time, combined with a loss of novo. Instead of replacing whole teeth the mouse counteracts the tooth replacement capabilities [6]. This appears to correlate with a problems of tooth wear by having continuously growing incisors, general shift to complex teeth, indicating a trade off between how with a continuous production of enamel and dentine tissue secret- many teeth are produced and the level of tooth shape complexity ing cells – a tooth renewal system [1–4]. The mouse is therefore [22]. insufficient to understand how mammals replace teeth. The chick (Gallus gallus) lacks teeth, although some reports suggest that some 3. Replacing a vertebrate dentition chick embryos (at approximately stage 27 [5]) can start the process of tooth initiation soon after which the rudimentary dental lam- 3.1. Fish ina is aborted [5–7]. The zebrafish (Danio rerio) is a highly derived Teleost species of the order Cypriniformes and over the past 30 Fish can be separated into two distinct clades and for the years has become the top fish developmental model owing to its purposes of this discussion these two clades represent (i) the transparency during embryogenesis, the ease of vast embryo pro- bony fishes (Osteichthyes) – Actinopterygii and Sarcopterygii; and duction and the development of genomic tools. The zebrafish has (ii) the cartilaginous fishes (Chondrichthyes) – sharks, rays and become a useful model for tooth development and manipulation [8] chimaeras. Most fish groups possess oral teeth that undergo contin- however the tiny teeth of zebrafish and teeth in all Cypriniformes uous tooth replacement (polyphyodonty) and represent the most are confined to the back of the gill arches, embedded deep within basal extant vertebrates, important for an evolutionary and phylo- the pharyngeal cavity, with oral teeth in this order having been lost
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