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Molecular Genetics of Tooth Agenesis

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Molecular Genetics of Tooth Agenesis View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Helsingin yliopiston digitaalinen arkisto Molecular Genetics of Tooth Agenesis Pekka Nieminen Department of Orthodontics Institute of Dentisty and Institute of Biotechnology and Department of Biological and Environmental Sciences Faculty of Biosciences University of Helsinki Finland Academic Dissertation To be discussed publicly with the permission of the Faculty of Biosciences of the University of Helsinki, in the Main Auditorium of the Institute of Dentistry on November 23rd 2007 at 12 noon. Helsinki 2007 Supervisors Sinikka Pirinen, DDS, PhD Professor emerita Department of Pedodontics and Orthodontics Institute of Dentistry, University of Helsinki, Finland Irma Thesleff, DDS, PhD Professor Developmental Biology Programme Institute of Biotechnology, University of Helsinki, Finland Reviewed by Jan Huggare, DDS, PhD Professor Department of Orthodontics Karolinska institutet Huddinge, Sweden Anu Wartiovaara, MD, PhD Professor FinMIT, Research Program of Molecular Neurology Biomedicum Helsinki Finland Opponent: Heiko Peters PhD, Reader University of Newcastle ISBN 978-952-10-4350-5 (nid.) ISBN 978-952-10-4351-2 (PDF) ISSN 1795-7079 Yliopistopaino Oy Helsinki 2007 Contents LIST OF ORIGINAL PUBLICATIONS 7 ABBREVIATIONS 8 SUMMARY 9 INTRODUCTION 10 REVIEW OF THE LITERATURE 11 OVERVIEW OF TOOTH DEVELOPMENT 11 Principles of development 11 Teeth and dentitions 13 Development of teeth 14 Commitment, morphogenesis and inductive interactions 19 Molecular regulation of tooth development 26 Reciprocal signaling and signaling centers 26 Transcription factors 27 MSX1 and PAX9 28 Initiation 29 Morphogenesis 32 Tooth replacement 34 TOOTH AGENESIS 36 Developmental anomalies 36 Developmental anomalies of teeth 37 Genetic traits of tooth number and shape 37 Supernumerary teeth 38 Tooth agenesis 39 Terminology 39 Diagnostic challenges 40 Prevalences 40 Patterns of agenesis 41 Tooth agenesis in syndromes 43 Dental anomalies associated with agenesis 43 Reduction of tooth size and morphology 44 Delayed development and eruption 45 Root abnormalities 46 Abnormal positions of teeth 47 Enamel defects 48 Etiology and pathogenesis of tooth agenesis 48 Environmental factors 48 Tooth size variation and heritability 50 Twin studies on agenesis 50 Segregation analyses in families 51 Molecular genetics 52 4 Pathogenesis of tooth agenesis 53 Tooth agenesis and cancer 56 HUMAN GENETICS AND GENE DEFECTS 57 The human genome 57 Variation 58 From genotypes to phenotypes 59 Gene identification 60 AIMS 64 MATERIALS AND METHODS 65 Subjects 65 DNA isolation 66 Genotyping 67 Linkage analysis (I, IV) 68 Sequencing (II) 68 FISH Analysis (III) 68 Gene expression data collection (V) 69 WWW implementation (V) 69 RESULTS AND DISCUSSION 70 MSX1 and PAX9 in dominantly inherited severe tooth agenesis (pub- lications II and III) 70 Attempts to unravel the genetic basis of common tooth agenesis (incisor and premolar hypodontia) (publications I, IV) 74 Construction of the gene expression database (publication V) 78 GENERAL DISCUSSION 80 Uncovering the genetic background of tooth agenesis 80 Implications for the pathogenetic mechanisms of tooth agenesis 82 CONCLUDING REMARKS 85 ACKNOWLEDGEMENTS 86 REFERENCES 88 5 6 List of original publications This thesis is based on the following original articles, which are referred to in the text by their roman numerals. In addition, some unpublished data are also presented. I Nieminen P, Arte S, Pirinen S, Peltonen L, and Thesleff I (1995). Gene defect in hy- podontia - exclusion of MSX1 and MSX2 as candidate genes. Human Genetics 96, 305-308. II Nieminen P, Arte S, Tanner D, Paulin L, Alaluusua S, Thesleff I, and Pirinen S (2001). Identification of a nonsense mutation in the PAX9 gene in molar oligodontia. European Journal of Human Genetics 9, 743-746. III Nieminen P, Kotilainen J, Aalto Y, Knuutila S, Pirinen S, and Thesleff I (2003). MSX1 gene is deleted in Wolf-Hirschhorn syndrome patients with oligodontia. Jour- nal of Dental Research 82 , 1012-1016. IV Nieminen P, Arte S, Luonsi E, Pirinen S, Peltonen L, and Thesleff I. A genome-wide search for hypodontia locus in families, manuscript. V Nieminen P, Pekkanen M, Åberg T, and Thesleff I (1998). A graphical www- database on gene expression in tooth. European Journal of Oral Sciences 106, 7-11. 7 ABBREVIATIONS ADULT acro-dermato-ungual-lacrimal-tooth syndrome AEC ankyloblepharon-ectodermal dysplasia-clefting syndrome AI amelogenesis imperfecta APC adenomatous polyposis coli BMP/Bmp bone morphogenetic protein CLPED cleft lip/palate-ectodermal dysplasia syndrome DKK1/Dkk1 dickkopf-1 DLX/Dlx distalless homeobox homolog DNA deoxyribonucleid acid E embryonic day EDA/Eda anhidrotic ectodermal dysplasia EDAR/Edar EDA receptor EDA-ID anhidrotic ectodermal dysplasia with immunodeficiency EEC ectrodactyly-ectodermal dysplasia-clefting syndrome EGF/Egf epidermal growth factor ERS epithelial cell rests of Malassez FAP familial adenomatous polyposis coli FGF/Fgf fibroblast growth factor FGFR/Fgfr fibroblast growth factor receptor HERS Hertwig’s epithelial root sheath IP incontinentia pigmenti LEF1/Lef1 lymphoid enhancer factor 1 LMS limb-mammary syndrome mRNA messenger RNA MSX/Msx muscle segment homeobox homolog NMD nonsense mediated decay OL-EDA-ID anhidrotic ectodermal dysplasia-immunodeficiency-osteopetrosis- lymphoedema. PAX/Pax paired box family member PCR polymerase chain reaction RNA ribonucleic acid RUNX/Runx runt homolog SHH/Shh sonic heghehog SNP single nucleotide polymorphism SRA short root anomaly STRP short tandem repeat polymorphism TGFA transforming growth factor D TGFE/TgfE transforming growth factor E TNF/Tnf tumor necrosis factor 8 SUMMARY Tooth agenesis is one of the most common developmental anomalies in man. The common forms, in which one or a few teeth are absent, may cause cosmetic or occlusal harm, while severe forms which are relatively rare require clinical attention to support and maintain the dental function. Observation of tooth agenesis and especially the severe forms is also impor- tant for diagnosis of malformation syndromes. Some external factors like pollutants or cancer therapy may cause developmental defects and agenesis in dentition. However, twin and family studies have shown the predominant role of inheritance in the etiology of agenesis. Furthermore, studies on inherited tooth agenesis as well as mouse null mutants have identified several of the genetic factors and helped to un- derstand the molecular mechanisms of tooth development. However, so far success has only been made in identifying the genes involved in syndromic or rare dominant forms of tooth agenesis, while the genes and defects responsible for the majority of cases of tooth agenesis, especially the common and less severe forms, are largely unknown. In this study, different types of tooth agenesis were studied. It was shown that a dominant nonsense mutation in PAX9 was responsible for severe agenesis (oligodontia) affecting espe- cially permanent molars in a Finnish family. In a study of tooth agenesis associated with Wolf-Hirschhorn syndrome, it was shown that severe tooth agenesis was present if the causative deletion in the short arm of chromosome 4 spanned the MSX1 locus. A conclusion from these studies was that severe tooth agenesis was caused by haploinsufficiency of these transcription factors. During this work several other gene defects in MSX1 and PAX9 have been identified by us and others, and according to an analysis of the associated phenotypes presented in this thesis, similar but significantly different agenesis phenotypes are associated with defects in MSX1 and PAX9, apparently reflecting distinctive roles for these two tran- scription factors during the development of human dentition. The original aim of this work was to identify gene defects that underlie the common incisor and premolar hypodontia. For this purpose, several candidate genes were first excluded. Af- ter a genome-wide search with seven families in which tooth agenesis was inherited in an autosomal dominant manner, a promising locus in chromosome 18 was identified for second premolar agenesis in one family. This finding was supported by results from other families. The results also implied existence of other loci both for second premolar agenesis and for incisor agenesis. On the other hand the results from this study did not lend support for com- prehensive involvement of the most obvious candidate genes in the etiology of incisor and premolar hypodontia. Rather, they suggest remarkable genetic heterogeneity of tooth agen- esis. Despite the increasing knowledge of the molecular background of tooth agenesis, the patho- logical and developmental mechanisms of tooth agenesis have only become clarified in a few cases. The available evidence suggests that human tooth agenesis usually is a conse- quence of quantitative defects which predispose to a failure to overcome a developmental threshold. However, the stages and causes may be different in the case of different genes. 9 INTRODUCTION Mammalian teeth develop as ectodermal organs bearing many similarities to other such or- gans like hair, feathers and mammary glands (Pispa and Thesleff, 2003). As such, teeth are serially homologous and the developmental mechanisms that produce different tooth types in an organized fashion have long been debated (Butler, 1939; Osborn, 1978; Weiss et al., 1998). The positioning of teeth, their intricate and species-specific morphologies, timing of development
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