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BCOR Mutations and Unstoppable Root Growth: a Commentary on Oculofaciocardiodental Syndrome: Novel BCOR Mutations and Expression in Dental Cells

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BCOR Mutations and Unstoppable Root Growth: a Commentary on Oculofaciocardiodental Syndrome: Novel BCOR Mutations and Expression in Dental Cells Journal of Human Genetics (2014) 59, 297–299 & 2014 The Japan Society of Human Genetics All rights reserved 1434-5161/14 www.nature.com/jhg COMMENTARY BCOR mutations and unstoppable root growth: a commentary on oculofaciocardiodental syndrome: novel BCOR mutations and expression in dental cells Piranit Nik Kantaputra Journal of Human Genetics (2014) 59, 297–299; doi:10.1038/jhg.2014.31; published online 1 May 2014 OFCD SYNDROME AND cases the roots of the mandibular permanent development Bcor in mesenchyme has ROBERT J GORLIN canines were reaching the lower border of crucial roles in cellular events, such as r Robert J Gorlin, a dental geneticist, mandible and the roots of the maxillary apoptosis and cellular differentiation.5,6 Dhad a key role in delineating oculofa- permanent ones were reaching the floors of It is important to note that BCL-6 is not ciocardiodental (OFCD) syndrome (OFCD, the orbits (Figures 1a and b). This expressed in tooth primordium in early MCOPS2; OMIM 300166), a rare disorder striking feature appears to be unique embryogenesis.7 This implies that the role with some very interesting things to teach us to the best of my knowledge, it has of Bcor in tooth development is BCL-6- about the regulation of development. This is not been found in any genetic or nongenetic independent5,8 and the dental phenotypes an X-linked dominant disorder with male disorders. Dr Gorlin later coined the found in patients affected with BCOR lethality. Female patients show: (1) ocular name Oculo-Facio-Cardio-Dental syndrome mutations are not associated with BCL-6. abnormalities: congenital cataract (80%), emphasizing the major affected organs of the It is possible that BCOR is likely to be microphthalmia or secondary glaucoma, syndrome,1 and always thought that it was targeted to DNA by other transcription (2) facial abnormalities: long narrow facies, telling us something important about repressors.3 In addition, the ankylin repeats pointed nose with cartilages separated at development, a belief that is being amply of BCOR, which are involved in protein– the tip, high-nasal bridge and cleft palate, confirmed. protein interactions support the possibility (3) cardiac abnormalities: atrial septal that BCOR interacts with other proteins not defect, ventricular septal defect and mitral associated with Bcl-6. Bcor is highly expressed OFCD SYNDROME AND BCOR valve prolapse, and (4) dental abnormal- in the tongue during early development but, MUTATIONS ities: radiculomegaly, delayed dentition, interestingly, patients with BCOR mutations Since then, we have learned much more hypodontia, delayed exfoliation of primary have never been reported to have tongue about this condition. OFCD syndrome is teeth, root dilaceration and hyperdontia.1 anomalies.5 Besides radiculomegaly and caused by mutations in the BCL-6 corepres- The consistent characteristic feature sor (BCOR)gene.2 BCOR is ubiquitously hyperdontia, all other defects in OFCD of this syndrome appears to be expressed in human tissues during early syndrome appear to be ‘deficiency’ defects radiculomegaly of permanent teeth, development and the encoded BCOR protein such as cardiac septal defects, hypodontia especially the maxillary and mandibular functions as a transcriptional corepressor. It and cleft palate. Continuous root growth permanent canines. lacks a DNA-binding domain and interacts and hyperdontia appear to be the opposite. I was a student of Professor Gorlin from with the DNA-binding transcriptional There must be mechanisms that control 1989 to 1991. I still remember how excited repressor BCL-6 via Poxvirus and zinc human organ sizes, including the closure he was about the long-rooted permanent finger domain3 and the transcriptional of anterior and posterior neuropores. canines he saw in patients with OFCD regulator AF9.4 It is not surprising that This control mechanism appears to syndrome. He told me that in a number of BCOR mutations are associated with malfunction in the teeth of patients dental anomalies, including hypodontia, with OFCD syndrome. That is why hyperdontia and radiculomegaly since Bcor the tooth roots do not close and keep PN Kantaputra is at Center of Excellence in Medical is expressed in both dental epithelium growing. In the normal situation BCOR Genetics Research, Chiang Mai University, Chiang Mai, might have roles in regulating the root to Thailand; Craniofacial Genetics Laboratory, Faculty of and the mesenchyme during the early 5 Dentistry, Chiang Mai University, Chiang Mai, Thailand; stages of tooth development. Knockdown stop growing; thus its mutations lead to Division of Pediatric Dentistry, Department of Orthodon- experiments of Bcor expression in dental continuously growing roots, imitating tics and Pediatric Dentistry, Faculty of Dentistry, Chiang mesenchymal cells using the lentivirus- rodent incisors. Mai University, Chiang Mai, Thailand; DENTALAND CLINIC, Chiang Mai University, Chiang Mai, Thailand mediated RNA interference approach have In this issue of Journal of Human Genetics E-mail: [email protected] demonstrated that during early tooth the group led by Professor Keiji Moriyama Commentary 298 Bcor is strongly expressed in the dental papilla cells and dental follicle cells that are attached to the cervical loops at the bell stage. This pattern of Bcor expression indicates the crucial role of Bcor in root development.5 What controls the length of the root is still a mystery. In the normal situation the stem cell niche disappears, HERS invaginates and apical root closure commences.11 In the permanent teeth, apical root closure takes place B3 years after the teeth erupt into the oral cavity. In the primary teeth the interval is approximately 1.5 years. The stem cell population at the base of the tooth is the source of cells to replace all mesenchymal and epithelium-derived tooth cells.12 In patients with BCOR mutations this does not appear to happen, indicating that the regulation in reducing the number of stem cells does not function properly. BCOR MUTATIONS AND DISRUPTION OF EPIGENETIC MECHANISMS The abnormal root growth in patients with OFCD syndrome has been demonstrated to be caused by the increase of the osteo– dentinogenic potential of mesenchymal stem cells (MSCs) secondary to BCOR muta- tions.13 BCOR mutations result in abnormal activation of AP-2a, a repressive target of Figure 1 (a) Very long root of mandibular permanent canine. (b) Panoramic radiograph of a patient BCOR which is a key factor that mediates the affected with OFCD. The roots of maxillary permanent canines reach the floors of orbits. The roots of increased osteo–dentinogenic capacity of the mandibular permanent canine reach the lower border of the mandible (arrow heads). Note very MSCs. In the normal situation BCOR com- large mandibular canals (arrows). (Figures from Gorlin Slide Collection.) A full color version of this plex works as a negative regulator of osteo– figure is available at the Journal of Human Genetics journal online. dentinogenic capacity of MSCs. It maintains tissue homeostasis and gene silencing reports two novel BCOR mutations, a BCOR MUTATIONS AND UNSTOPPABLE through epigenetic mechanisms. BCOR nonsense and a frameshift mutation in two ROOT GROWTH mutations have been demonstrated to Japanese patients affected with OFCD syn- There are exciting studies that add to our increase histone H3K4 and H3K36 methyla- drome along with studies of expression understanding of the mechanisms behind un- tion in MSCs, and subsequently reactivating aimed at understanding why the tooth stoppable root growth in OFCD, and I would transcription of silenced target genes.13 roots in patients with OFCD syndrome like to review some developmental background kept growing.9 They studied the periodontal to place them within a broader context. BCOR AND POLYCOMB REPRESSIVE ligament (PDL) cells surrounding the Development of the tooth root requires the COMPLEX-1 apical 1/3 and apical pulp cells, which proliferation of the Hertwig epithelial root Besides the nonsense-mediated mRNA decay are tissues in the area of the growing sheath (HERS), a transient epithelial double mechanism, the polycomb repressive com- root. They found that BCOR is highly layer of flat, cuboidal cells which grows from plex (PRC) might have a role in nonstop root expressed in the mesenchyme and the the cervical loop of the dental organ between growth in patients with OFCD syndrome. It expression of the mutant PDL cells was the dental follicle and the dental pulp, out- has been demonstrated that polycomb com- higher than that of the mutant dental lining the shape of the future tooth root.10,11 plex group (PcG) proteins have roles in the pulp cells. The mutant PDL appeared to HERS elongates and subsequently breaks up maintenance of embryonic and adult stem have unstable transcripts and proliferated into epithelial cords at the very beginning of cells, control of cell proliferation, cancer faster than wild-type cells. In addition cementogenesis to allow the ingression of development, genomic imprinting and they also demonstrated that the higher mesenchymal cells of the dental follicles to X-chromosome inactivation. The role of rate of nonsense-mediated mRNA decay trespass the epithelial barrier and secrete PcG complexes is to maintain the transcrip- in PDL led to insufficient function of cementum on to the dentinal surface of the tional repression of target genes by binding BCOR to repress target genes, resulting in root. Finally HERS collapses into the to the chromatin and inducing higher-order the promotion of cell proliferation and epithelial rests of Malassez.11 The epithelial chromatin structures.14 It is hypothesized subsequently led to ‘nonstop’ root growth. diaphragm at the most apical portion of that Bcor, which forms a complex with This phenotype appears to be the result of HERS stays intact as it is not involved in PRC1,6 has an important role in root haploinsufficiency.9 the ingression of mesenchymal cells.10 formation, especially in controlling the final Journal of Human Genetics Commentary 299 root length. PRC1 complex regulates the few mechanisms.
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