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A New, Clinically Relevant Synthesis of an Old Concept archives of oral biology 54s (2009) s34–s44 available at www.sciencedirect.com journal homepage: www.intl.elsevierhealth.com/journals/arob Morphogenetic fields within the human dentition: A new, § clinically relevant synthesis of an old concept Grant Townsend a,e,*, Edward F. Harris b,e, Herve Lesot c,d,e, Francois Clauss c,d, Alan Brook e a School of Dentistry, The University of Adelaide, Adelaide, South Australia 5005, Australia b Department of Orthodontics, College of Dentistry, University of Tennessee, 875 Union Avenue, Memphis, TN 38163, USA c INSERM U595, Faculty of Medicine, 11, rue Humann, 67085 Strasbourg, France d Faculty of Dentistry, Louis Pasteur University, 67085 Strasbourg Cedex, France e International Collaborating Centre in Oro-facial Genetics and Development, The University of Liverpool, Liverpool L69 3GN, UK article info abstract Article history: This paper reviews the concept of morphogenetic fields within the dentition that was first Accepted 25 June 2008 proposed by Butler(Butler PM. Studies of the mammalian dentition. Differentiation of thepost- canine dentition. Proc Zool Soc Lond B 1939;109:1–36), then adapted for the human dentition by Keywords: Dahlberg (Dahlberg AA. The changing dentition of man. J Am Dent Assoc 1945;32:676–90; Dental development Dahlberg AA. The dentition of the American Indian. In: Laughlin WS, editor. The Physical Clone model Anthropology of the American Indian. New York: Viking Fund Inc.; 1951. p. 138–76). The clone Homeobox code theory of dental development, proposed by Osborn (Osborn JW. Morphogenetic gradients: Patterning fields versus clones. In: Butler PM, Joysey KA, editors Development, function and evolution of teeth. Hypodontia London: Academic Press, 1978. p. 171–201), is then considered before these two important Supernumeraries concepts are interpreted in the light of recent findings from molecular, cellular, genetic and Twins theoretical and anthropological investigation. Sharpe (Sharpe PT. Homeobox genes and orofacial development. Connect Tissue Res 1995;32:17–25) put forward the concept of an odontogenic homeobox code to explain how different tooth classes are initiated in different parts of the oral cavity in response to molecular cues and the expression of specific groups of homeobox genes. Recently, Mitsiadis and Smith (Mitsiadis TA, Smith MM. How do genes make teeth to order through development? J Exp Zool (Mol Dev Evol) 2006; 306B:177–82.) proposed that the field, clone and homeobox code models could all be incorporated into a single model to explain dental patterning. We agree that these three models should be viewed as comple- mentary rather than contradictory and propose that this unifying view can be extended into the clinical setting using findings on dental patterning in individuals with missing and extra teeth. The proposals are compatible with the unifying aetiological model developed by Brook (Brook AH. A unifying aetiological explanation for anomalies of tooth number and size. Archs Oral Biol 1984;29:373–78) based on human epidemiological and clinical findings. Indeed, this new synthesis can provide a sound foundation for clinical diagnosis, counselling and manage- ment of patients with various anomalies of dental development as well as suggesting hypoth- eses for future studies. # 2008 Elsevier Ltd. All rights reserved. § This Supplement arises from a series of papers given at an International Workshop on Oral Growth and Development held in Liverpool on November 26–28, 2007. * Corresponding author at: School of Dentistry, The University of Adelaide, Adelaide, South Australia 5005, Australia. Tel.: +61 8 83035968; fax: +61 8 83033444. E-mail address: [email protected] (G. Townsend). 0003–9969/$ – see front matter # 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.archoralbio.2008.06.011 archives of oral biology 54s (2009) s34–s44 S35 1. Field and clone theories premolars and molars. Each field was thought to have its strongest effect on the anterior or key tooth within a class. The The concept of a morphogenetic field emerged in the 19th more distally placed teeth, which generally develop later than century, though the molecular-genetic basis for patterned those more mesially placed, were observed to show greater series of skeletodental elements (e.g., vertebrae, ribs, teeth) phenotypic variation. Interestingly, Dahlberg2,3 did not define were unknown. Ordered form was a common observation in fields within the primary dentition and, without any com- numerous aspects of biology,8 but the governing principles, let ment, he added a premolar field to Butler’s1 three-field alone the causes, were virtually unknown.9 paradigm. In contrast, Butler19 later argues that premolars The accumulation of paleontological findings, along with represent modified anterior members of a permanent molar information on extant species, made it clear that the field, with the primary second molar displaying similar dentitions of higher vertebrates were (1) heterodont—com- morphology to the permanent first molar located directly posed of multiple tooth types, and (2) organised into distal to it. morphogenetic fields. For example, Bateson,10 amassed Osborn4 proposed that a single clone of pre-programmed extensive data on meristic variation, including dental exam- cells led to the development of all the teeth within a particular ples primarily of hypo- and hyperdontia. Bateson’s far-ranging class. For example, a molar clone of cells was postulated to compilations showed that the variable dental elements induce the dental lamina to initiate molar development. As the occurred at the later-forming end of a field and that these clone of cells grew distally, tooth buds were formed, terminal teeth were metrically and morphologically most surrounded by zones of inhibition that prevented other teeth variable within a field. developing until the migrating clone had moved on suffi- The Zeitgeist of developmental biology in the early 20th ciently. More recent work invokes a reaction-diffusion model century was strongly influenced by Spemann’s embryological in the region of a presumptive tooth, where activators induce organizing centers (Spemann11; De Robertis12). In 1934 Huxley placode formation while negative regulators are higher in and De Beer combined the study of morphology with the interplacodal regions, which prevents tooth formation and, morphogenetic field concept in their seminal work The thus, accounts for the orderly spacing of teeth.20 Elements of Experimental Embryology, which closely preceded The demonstration that isolated presumptive first molar Butler’s1 description of fields and morphogenetic variations in tissue explants could continue to grow and form all three the mammalian dentition. molar teeth in their normal sequence, provided strong Weiss13 was among the leaders to reaffirm the interpre- experimental support for the clone model.21 However, the tative value of the field concept. Butler1 postulated that clone model does not provide an explanation for how the morphogenetic fields can account for the way in which teeth dentition develops as a whole, with different tooth classes within a particular class formed meristic series, i.e., with each displaying different shapes. Furthermore, the inclusion of the tooth displaying similarities to others nearby because of the phrase ‘‘fields versus clones’’ in the title of Osborn’s original influence of a common field but with graded differences paper4 has led many to suppose that the field and clone because of its position. Currently these dental elements are models are competing, mutually exclusive concepts. Recent considered to result from the repetition of ‘developmental findings about the roles of signalling molecules and the modules’.14,15 Butler’s phylogenetic study of the mammalian expression of homeobox genes during dental development dentition was wholly observational, but he inferred several indicate that such a distinction is unwarranted.6 Indeed, the features of the changes that meshed well with the biological field and clone models can be viewed as complementary to features of field gradients, notably (a) a size gradient within each other. each field, (b) a gradient of morphological complexity, from the complex pole tooth to the simpler variable tooth, and (c) a gradient of variability, with less size and shape variability in 2. The odontogenic homeobox code the pole tooth and increasing variability away from the pole. Documenting such field gradients was important because the The odontogenic homeobox code model explains how dental observations substantiated that teeth exist within morpho- patterns can be generated from different domains of expression genetic gradients as defined by the criteria established by of homeobox genes in neural crest derived ectomesench- Huxley and De Beer16 and Weiss.14 The phylogenetic patterns yme.5,22 While the code was initially developed from studies of do not always match the ontogenetic situations, however; the mouse dentition in which there are only incisor and molar while incisors have lost teeth distally-to-mesially, the number teeth, it has been extended to explain how canines and of premolars has been reduced mesially-to-distally. premolars could also be produced by overlapping domains of Butler17 later suggested that teeth were evolving as a part of gene expression.22 Experimental studies have also shown that a system rather than as individual organs. He postulated two by modulating certain signalling molecules it is possible to alter different effects: a ‘meristic’ effect, influencing the
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