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Unraveling the Molecular Mechanisms That Lead to Supernumerary Teeth in Mice and Men: Current Concepts and Novel Approaches

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Unraveling the Molecular Mechanisms That Lead to Supernumerary Teeth in Mice and Men: Current Concepts and Novel Approaches Cells Tissues Organs 2007;186:60–69 DOI: 10.1159/000102681 Unraveling the Molecular Mechanisms That Lead to Supernumerary Teeth in Mice and Men: Current Concepts and Novel Approaches a b Rena N. D’Souza Ophir D. Klein a Department of Biomedical Sciences, Baylor College of Dentistry, Texas A&M University Health Science Center, b Dallas, Tex. , and Department of Pediatrics, University of California, San Francisco, Calif. , USA Key Words basic mechanisms involved is essential. The purpose of this Fibroblast growth factors Runx2 Sprouty manuscript is to review current knowledge about how su- Supernumerary teeth Transgenic mice pernumerary teeth form, the molecular insights gained through studies on mice that are deficient in certain tooth signaling molecules and the questions that require further Abstract research in the field. Copyright © 2007 S. Karger AG, Basel Supernumerary teeth are defined as those that are present in excess of the normal complement of human dentition and represent a unique developmental anomaly of patterning and morphogenesis. Despite the wealth of information gen- erated from studies on normal tooth development, the ge- netic etiology and molecular mechanisms that lead to con- genital deviations in tooth number are poorly understood. Abbreviations used in this paper For developmental biologists, the phenomenon of supernu- merary teeth raises interesting questions about the devel- BMP bone morphogenic protein opment and fate of the dental lamina. For cell and molecular CCD cleidocranial dysplasia biologists, the anomaly of supernumerary teeth inspires sev- Eda ectodysplasin gene eral questions about the actions and interactions of tran- FGF3–10 fibroblast growth factors 3–10 scription factors and growth factors that coordinate mor- FGFR1, 2 fibroblast growth factor receptors 1, 2 M1 first molar phogenesis, cell survival and programmed cell death. For MSX1 homeo box, msh-like 1 human geneticists, the condition as it presents itself in either PAX6, PAX9 paired box genes 6, 9 syndromic or non-syndromic forms offers an opportunity to RUNX2 runt-related gene 2 discover mutations in known or novel genes. For clinicians SHH sonic hedgehog faced with treating the dental complications that arise from Spry2, 4 sprouty genes 2, 4 Wnt an oncogene the presence of supernumerary teeth, knowledge about the © 2007 S. Karger AG, Basel Dr. Rena N. D’Souza Department of Biomedical Sciences, Baylor College of Dentistry Fax +41 61 306 12 34 Texas A&M University System, Health Science Center, 3302 Gaston Avenue E-Mail [email protected] Accessible online at: Dallas, TX 75246 (USA) www.karger.com www.karger.com/cto Tel. +1 214 828 8260, Fax +1 214 828 8375, E-Mail [email protected] Introduction The Dental Lamina In contrast to the reduced monophyodont rodent Knowledge about the origin, development and fate of dentition in which only incisors and molars are present, the dental lamina is critical to our understanding of how the diphyodont human dentition exhibits all four tooth supernumerary teeth arise. In humans, the primitive oral classes at maturity. The deciduous complement of 20 cavity or stomatodeum becomes apparent around day 25 teeth consists in each quadrant two incisors, one canine of development and is demarcated laterally by the first pair and two molars that are shed during childhood while of branchial (pharyngeal) arches [Krause and Jordan, 1965; the permanent or secondary dentition consists of 32 Nanci, 2003]. The latter consist of an external layer of ec- teeth, namely, two incisors, one canine, two premolars toderm, an intermediate layer of lateral plate mesoderm and three molars in each quadrant. Molecular and ge- and an internal layer of endoderm. Microscopically, the netic studies performed in the past two decades have stomatodeum is lined by a two- to three-cell layer of epi- shown that the patterning of dentition is a highly com- thelial cells that overlies a layer of embryonic connective plex process that provides a valuable developmental tissue derived from cranial neural crest ectomesenchyme. model for studying genes that control three-dimension- Around day 37 of embryonic development, the presump- al patterning and morphogenesis. Taken together, these tive maxilla and mandible become visible as each is cov- advances have improved our understanding that the ered by a continuous layer of thickened epithelium, called precise control of the number, position, size and shape the primary epithelial band. Shortly after, this band of tis- of teeth within the maxilla and mandible requires sig- sue divides into two distinct structures, the vestibular lam- naling between odontogenic (tooth-specific) epithelium ina and the dental lamina. While both structures are com- and mesenchyme. Such interactions involve diffusible posed of highly proliferative cells that rapidly grow into morphogens and nuclear transcription factors that op- surrounding ectomesenchyme, cells of the vestibular lam- erate within parallel signaling pathways to give rise to ina enlarge and undergo programmed cell death to form a an exquisitely patterned dentition. That such a complex cleft (the space between the cheek and the arch). In con- process frequently goes awry is not surprising, and pat- trast, the dental lamina remains proliferative, extending terning defects in human dentition occur often and are outgrowths into the ectomesenchyme but only at future characterized by alterations in the number, size and sites of odontogenesis. The epithelial outgrowth or tooth shape of teeth. The importance of the genetic control of bud then progresses from the cap to the bell stages of mor- the patterning of human dentition is underscored by the phogenesis but remains attached to the dental lamina findings that mutations in genes that encode the tran- through a stalk-like extension called the lateral lamina. scription factors PAX9 and MSX1 lead to non-syndrom- During the bell stage and prior to the differentiation of ic tooth agenesis or the congenital absence of teeth, odontoblasts and ameloblasts, the dental lamina and the among the most commonly inherited disorders in hu- lateral lamina that connects the tooth organ to the overly- mans [hypodontia (OMIM 106600)]. Another condi- ing oral epithelium fragment into small clusters of cells. tion affecting the patterning of dentition is the presence These cells normally undergo programmed cell death but of supernumerary teeth, a relatively rare condition that sometimes persist to form structures called epithelial is characterized by the presence of more than the nor- pearls. The formation of eruption cysts from these epithe- mal complement of 20 deciduous and 32 permanent lial remnants is known to interfere with the normal erup- teeth. In contrast to advances made in our understand- tion pathway of the underlying tooth organ [Moskow and ing of the genetic etiology of tooth agenesis and its un- Bloom, 1983; Pindborg, 1970]. Thus far, studies on the fate derlying molecular mechanisms, not as much has been of the dental lamina have been limited to histologic and reported about the genetic and molecular defects that ultrastructural analyses that suggest that the sequence of lead to supernumerary tooth development. The objec- events leading to its degeneration is initiated by underlying tives of this review are to survey classical literature con- mesenchyme [Khaejornbut et al., 1991]. cerning the etiology, frequency and classification of su- The primary dental lamina that gives rise to the decidu- pernumerary teeth, to highlight molecular insights ous dentition is also responsible for the formation of the gained from the use of genetically engineered mouse succedaneous (permanent) incisors, canines and premo- models, and to propose new research opportunities in lars. These develop as lingual extensions of the dental lam- human molecular genetics. ina and are clearly visible in a coronal section through a developing human jaw. The three permanent molars that Supernumerary Teeth Cells Tissues Organs 2007;186:60–69 61 Fig. 1. Panel describing the dental complications and the sequence graph showing that the majority of permanent teeth are unerupt- of treatment for a 17-year-old male affected by CCD. a, b Pan- ed. d Surgical exposure and extraction of all supernumerary teeth oramic radiograph and tracing. CI = Central incisor; L = lateral and deciduous teeth with the exception of the right deciduous incisor; C = canine; P = premolar; 6 = permanent first molar; 7 = second molar, which was not extracted for orthodontic anchor- permanent second molar; 8 = permanent third molar; D = decid- age. e Intraoral view of mandibular arch, showing lip bumper ap- uous first molar; E = deciduous second molar. The presence of pliance. Orthodontic traction, through bonded attachments with multiple supernumerary teeth creates several problems. Note that chains, will be applied to promote eruption of the remaining the only permanent teeth which have erupted are the maxillary teeth. A series of orthodontic interventions are planned to restore left central incisor and all first molars. Multiple retained decidu- normal occlusion. ous teeth are also present. c Preoperative intraoral frontal photo- do not have deciduous predecessors develop from an out- Supernumerary Teeth in Humans growth of the primary dental lamina backward into the jaw ectomesenchyme. There is relatively little known about the Supernumerary teeth exist in excess of the normal genetic factors that control the fate of the dental lamina. complement of deciduous
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