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Mechanical Constraint from Growing Jaw Facilitates Mammalian Dental Diversity

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Mechanical Constraint from Growing Jaw Facilitates Mammalian Dental Diversity Mechanical constraint from growing jaw facilitates mammalian dental diversity Elodie Renvoiséa,1, Kathryn D. Kavanaghb, Vincent Lazzaric, Teemu J. Häkkinena, Ritva Ricea, Sophie Pantalaccid, Isaac Salazar-Ciudada,e, and Jukka Jernvalla,1 aDevelopmental Biology Program, Institute of Biotechnology, University of Helsinki, FIN-00014 Helsinki, Finland; bBiology Department, University of Massachusetts Dartmouth, Dartmouth, MA 02747; cInstitut de Paleoprimatologie, Paléontologie Humaine: Evolution et Paléoenvironments, UMR CNRS 7262, University of Poitiers, 86022 Poitiers cedex, France; dUnivLyon, École Normale Supérieure de Lyon, University Claude Bernard, CNRS UMR 5239, INSERM U1210, Laboratoire de Biologie et Modélisation de la Cellule, F-69007 Lyon, France; and eDepartament de Genètica i Microbiologia, Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallès, Spain Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved July 17, 2017 (received for review May 9, 2017) Much of the basic information about individual organ development of bone formation (20). Conversely, experiments using cultured comes from studies using model species. Whereas conservation of sections of mouse jaws show that molars grow larger after alve- gene regulatory networks across higher taxa supports generaliza- olar bone has been removed (21). tions made from a limited number of species, generality of mecha- To address the limited comparative evidence on the self- nistic inferences remains to be tested in tissue culture systems. Here, regulation of teeth, here we asked whether molar cusp patterns are using mammalian tooth explants cultured in isolation, we investigate indeed entirely self-regulatory, or whether the surrounding jaw self-regulation of patterning by comparing developing molars of the should also be considered in tooth patterning and evolution. Our mouse, the model species of mammalian research, and the bank vole. specific focus is inspired by early computational modeling, which A distinct patterning difference between the vole and the mouse has implicated that the lateral configuration of cusps depends on molars is the alternate cusp offset present in the vole. Analyses of lateral expansion of the developing molar (22). Molars typically both species using 3D reconstructions of developing molars and have lateral cusp configurations that range from largely parallel, as jaws, computational modeling of cusp patterning, and tooth explants in mice and humans, to alternate, as in the evolutionarily basal cultured with small braces show that correct cusp offset requires mammalian molar, the tribosphenic molar. Teeth of several lineages constraints on the lateral expansion of the developing tooth. Vole have repeatedly evolved from alternate to parallel cusp configura- molars cultured without the braces lose their cusp offset, and mouse tions during the Cenozoic, and in particular, rodents show great molars cultured with the braces develop a cusp offset. Our results evolutionary diversity in their lateral cusp configurations (Fig. 1; suggest that cusp offset, which changes frequently in mammalian Table S1)(23–26). Functionally, lateral cusp configuration is related evolution, is more dependent on the 3D support of the developing – to occlusion and to chewing direction in cuspidate teeth (26, 27). jaw than other aspects of tooth shape. This jaw tooth integration of a Developmentally, parallel and alternate cusp configurations specific aspect of the tooth phenotype indicates that organs may out- are one of the earliest features to appear during crown pat- source specific aspects of their morphology to be regulated by adja- terning (28), suggesting a relatively narrow time during which the cent body parts or organs. Comparative studies of morphologically cusp offset can be influenced. Despite the increasing knowledge different species are needed to infer the principles of organogenesis. about developmental regulation of tooth patterning, none of the known pathways or mutations in the mouse has transformed its evodevo | patterning | odontogenesis | diversity | tissue engineering parallel cusp configuration to the pattern of alternate cusp configuration (2, 6–8, 10–12, 29–31). This lack of suitable mouse he conservation of gene regulatory networks in the devel- opment of homologous organs is well exemplified by denti- T Significance tions. Teeth in fish, reptiles, and mammals have been found to use largely shared developmental gene networks (1, 2). Fur- thermore, tooth development, similar to organ development in Good examples of the relative autonomy of organ develop- general, results from sequential events that appear to be rela- ment are teeth, and for decades researchers have cultured tively independent from the development of other organs. In isolated mouse teeth on a petri dish by starting from the ear- particular, mammalian teeth have been considered highly self- liest recognizable stage. We have cultured cheek teeth of voles, regulatory, as they form inside the dental follicle buffered from another species of rodent, and show how the cultured vole the surrounding environment (3–5). The self-regulatory aspect of teeth lack their species-specific morphology. Based on compu- EVOLUTION teeth is further supported by the reiterative use of the same tational modeling, 3D imaging, and experiments in which we signaling pathways and signaling centers, called enamel knots, culture mouse and vole teeth between microscopic braces, we present within each growing tooth (2). Experiments on growing suggest that the development of vole tooth shape requires the teeth have revealed how an activator–inhibitor balance of sig- lateral support of the jaw. Because mice lack the vole-specific naling molecules within a developing tooth and between adjacent morphology, the requirement of the jaw for tooth shape has teeth regulate dental patterning (6–12). not been possible to uncover previously. Comparative studies Despite the evidence from mice indicating self-regulation of are required for the understanding of organogenesis. teeth, several observations suggest an intriguing link between jaw bone and tooth crown formation (3, 13, 14). In humans, abnor- Author contributions: E.R., K.D.K., and J.J. designed research; E.R., K.D.K., V.L., T.J.H., R.R., S.P., I.S.-C., and J.J. performed research; V.L., T.J.H., R.R., S.P., and I.S.-C. contributed new mal crown patterns in patients with congenital syphilis have been reagents/analytic tools; E.R., K.D.K., V.L., and J.J. analyzed data; and E.R., K.D.K., and J.J. ascribed to result from infection of the tooth follicle (3). Like- wrote the paper. wise, loss of function of parathyroid hormone-related protein The authors declare no conflict of interest. (PTHrP) leads to loss of alveolar bone resorption and de- This article is a PNAS Direct Submission. – formation of the tooth crown in the mouse (15 19). A lethal 1To whom correspondence may be addressed. Email: [email protected] or erenvoise@ human syndrome called Blomstrand chondrodysplasia, which yahoo.fr. involves a loss of function of the receptor for PTHrP, results in a This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. severe deformation of the base of a tooth crown due to an excess 1073/pnas.1707410114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1707410114 PNAS | August 29, 2017 | vol. 114 | no. 35 | 9403–9408 Downloaded by guest on October 1, 2021 30 25 20 15 10 Offset angle (degrees) Offset Lateral 5 cusp offset 0 Arvicolinae Cricetinae Stem Murinae Gerbillinae No offset Cricetodontini Arvicolinae Stem Gerbillinae 0 Stem Murinae 5 Offset 10 15 20 Millions of years ago 25 Fig. 1. Cusp offsets show diverse evolutionary patterns across the phylogeny of muroids. The plot shows the range of protoconid (white arrow) and metaconid (black arrow) angular values measured for extant and extinct muroid families (Materials and Methods; Table S1). Mouse (Murinae) and vole (Arvicolinae) cusp offsets are in the extreme ends of muroids. The teeth are not to scale. mutants further necessitates a comparative approach to studying Our ToothMaker simulations show that a substantial re- lateral cusp configurations. duction in the parameters affecting lingual (Lbi) and buccal We examined molar development of two extreme cases: the (Bbi) expansion of the tooth at a critical stage results in the al- mouse (Mus musculus), the model species used in mammalian ternate vole cusp pattern (Fig. 2; Table S2; Fig. S2). The de- tooth development with parallel cusps, and the bank vole velopment of the alternate vole pattern results from a narrower (Myodes glareolus), with alternate cusps (Fig. 1; Fig. S1). cross-section of the simulated tooth germ, which fit in the sec- ondary enamel knots only in the alternating pattern (Fig. 2B; Fig. Results S2). These modeled patterns suggest mechanisms limiting lateral Computational Modeling Implicates Lateral Expansion in the expansion of developing teeth at this stage are needed for al- Regulation of Cusp Offset. First we used soft tissue micro- ternate cusp configuration. To specifically simulate the rapid computed tomography (microCT; Materials and Methods)to longitudinal extension of the vole first molar (33), anterior and measure cusp-offset angles in the first (m1) lower molars of the posterior biases also need to be changed (Fig. 2; Fig. S2C). mouse and the vole. This method allowed us to examine the de- However, minimizing lateral biases alone is sufficient to produce velopment of lateral
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