Tooth-bone attachment tissue is produced by cells with a mixture of odontoblastic and osteoblastic features in reptiles
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
22-02794S
Grantová Agentura České Republiky
NW24-10-00204
Ministerstvo Zdravotnictví Ceské Republiky
CZ.02.01.01/00/22_008/0004593
Ministerstvo Školství, Mládeže a Tělovýchovy
CZ.02.1.01/0.0/0.0/15_003/0000460
Ministerstvo Školství, Mládeže a Tělovýchovy
CZ.02.1.01/0.0/0.0/16_019/0000728
Ministerstvo Školství, Mládeže a Tělovýchovy
LM2023050
Ministerstvo Školství, Mládeže a Tělovýchovy
PubMed
41261944
PubMed Central
PMC12779411
DOI
10.1111/joa.70059
Knihovny.cz E-zdroje
- Klíčová slova
- Calbindin1, Runx2, acrodont dentition, odontoblasts, osteoblasts, reptiles, teeth,
- MeSH
- ještěři * anatomie a histologie MeSH
- odontoblasty * cytologie MeSH
- osteoblasty * cytologie MeSH
- zuby * cytologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Teeth are anchored in the jaw in a highly variable manner across vertebrates. In mammals and crocodiles, the teeth are cushioned inside bony sockets by periodontal ligaments, whereas most squamate reptiles have teeth firmly attached to the jawbone. Here, we analyzed the development of the attachment tissue in the veiled chameleon, a species with firm acrodont tooth attachment, to reveal the cellular processes establishing ankylosis and to determine the cell types contributing to the attachment. The tooth-bearing bones formed pedicles with edges fusing to the dentine via an attachment tissue produced by morphologically distinct cells exhibiting both osteoblastic and odontoblastic features. These cells were RUNX2-positive, suggesting their potential to differentiate into hard-tissue-producing cells. However, in contrast to the osteoblasts of the bony pedicles, tooth-bone interface (TBI) cells expressed elevated levels of Na+-/K+-ATPase and thus resembled odontoblasts. TBI cells were visible only temporarily, and after tooth-bone fusion they were removed by apoptosis and phagocytosis. Dynamic deposition of the hard matrix continued on both sides of the TBI and during the posthatching stages through the participation of osteoblasts. Overall, our findings demonstrate both odontoblast- and osteoblast-like characteristics of cells producing the attachment tissue at the TBI during development in chameleons, highlighting the existence of a transient intermediate cell population, which we call ankyloblasts.
Central European Institute of Technology Brno University of Technology Brno Czech Republic
Department of Experimental Biology Faculty of Science Masaryk University Brno Czech Republic
Department of Histology and Embryology Faculty of Medicine Masaryk University Brno Czech Republic
Department of Neuroimmunology Center for Brain Research Medical University of Vienna Vienna Austria
Department of Physiology and Pharmacology Karolinska Institutet Stockholm Sweden
Zobrazit více v PubMed
Alfaqeeh, S.A. , Gaete, M. & Tucker, A.S. (2013) Interactions of the tooth and bone during development. Journal of Dental Research, 92, 1129–1135. Available from: 10.1177/0022034513510321 PubMed DOI
Beresford, W.A. (1981) Chondroid bone, secondary cartilage, and metaplasia. Baltimore: Urban & Schwarzenberg.
Berggård, T. , Miron, S. , Önnerfjord, P. , Thulin, E. , Akerfeldt, K.S. , Enghild, J.J. et al. (2002) Calbindin D28k exhibits properties characteristic of a Ca PubMed DOI
Bertin, T.J.C. , Thivichon‐Prince, B. , LeBlanc, A.R.H. , Caldwell, M.W. & Viriot, L. (2018) Current perspectives on tooth implantation, attachment, and replacement in amniota. Frontiers in Physiology, 9, 1630. Available from: 10.3389/fphys.2018.01630 PubMed DOI PMC
Bertonnier‐Brouty, L. , Viriot, L. , Joly, T. & Charles, C. (2021) Gene expression patterns associated with dental replacement in the rabbit, a new model for the mammalian dental replacement mechanisms. Developmental Dynamics, 250, 1494–1504. Available from: 10.1002/dvdy.335 PubMed DOI
Buchtová, M. , Zahradníček, O. , Balková, S. & Tucker, A.S. (2013) Odontogenesis in the veiled chameleon ( PubMed DOI
Budney, L.A. , Caldwell, M.W. & Albino, A. (2006) Tooth socket histology in the cretaceous Snake Dinilysia, with a review of amniote dental attachment tissues. Journal of Vertebrate Paleontology, 26(1), 138–145.
Caldwell, M.W. (2007) Ontogeny, anatomy and attachment of the dentition in mosasaurs (Mosasauridae: Squamata). Zoological Journal of the Linnean Society, 149, 687–700.
Caldwell, M.W. , Budney, L.A. , Lamoureux, D.O. , Caldwell, M.W. , Budneyl, L.A. & Lamoureux2, D.O. (2003) Histology of tooth attachment tissues in the late cretaceous Mosasaurid Platecarpus. Source: Journal of Vertebrate Paleontology, 23(3), 622–630. Available from: 10.1671/0272-4634(2003)023 DOI
Camilleri, S. & McDonald, F. (2006) Runx2 and dental development. European Journal of Oral Sciences, 114, 361–373. Available from: 10.1111/j.1600-0722.2006.00399.x PubMed DOI
Cole, A.G. & Hall, B.K. (2004) The nature and significance of invertebrate cartilages revisited: distribution and histology of cartilage and cartilage‐like tissues within the Metazoa. Zoology, 107, 261–273. Available from: 10.1016/j.zool.2004.05.001 PubMed DOI
Couve, E. , Osorio, R. & Schmachtenberg, O. (2013) The amazing odontoblast: activity, autophagy, and aging. Journal of Dental Research, 92(9), 765–772. Available from: 10.1177/0022034513495874 PubMed DOI
Delgado, S. , Davit‐Beal, T. , Allizard, F. & Sire, J.‐Y. (2005) Tooth development in a scincid lizard, PubMed DOI
Diekwisch, T.G.H. (2001) Developmental biology of cementum. The International Journal of Developmental Biology, 45(5–6), 695–706. PubMed
Domon, T. , Sugaya, K. , Yawaka, Y. , Osanai, M. , Hanaizumi, Y. , Takahashi, S. et al. (1994) Electron microscopic and histochemical studies of the mononuclear odontoclast of the human. The Anatomical Record, 240, 42–51. Available from: 10.1002/ar.1092400105 PubMed DOI
Dosedělová, H. , Štěpánková, K. , Zikmund, T. , Lesot, H. , Kaiser, J. , Novotný, K. et al. (2016) Age‐related changes in the tooth–bone interface area of acrodont dentition in the chameleon. Journal of Anatomy, 229, 356–368. Available from: 10.1111/joa.12490 PubMed DOI PMC
D'Souza, R.N. , Åberg, T. , Gaikwad, J. , Cavender, A. , Owen, M. , Karsenty, G. et al. (1999) Cbfa1 is required for epithelial‐mesenchymal interactions regulating tooth development in mice. Development (Cambridge, England), 126, 2911–2920. Available from: 10.1242/dev.126.13.2911 PubMed DOI
Ducy, P. , Zhang, R. , Geoffroy, V. , Ridall, A.L. & Karsenty, G. (1997) Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell, 89(5), 747–754. Available from: 10.1016/s0092-8674(00)80257-3 PubMed DOI
Edmund, A.G. (1960) Tooth replacement phenomena in the lower vertebrates. Toronto: Royal Ontario Museum. Available from: 10.5962/bhl.title.52196 DOI
Edmund, A.G. (1969) In: Gans, C. (Ed.) Biology of the Reptilia, Part 1: Morphology A. London: London Academic Press.
Fuenzalida, M. , Illanes, J. , Lemus, R. , Guerrero, A. , Oyarzn, A. , Acua, O. et al. (1999) Microscopic and histochemical study of odontoclasts in physiologic resorption of teeth of the polyphyodont lizard, PubMed DOI
Gaengler, P. (2000) Evolution of tooth attachment in lower vertebrates to tetrapods. In: Development, function and evolution of teeth. Cambridge: Cambridge University Press, pp. 173–185. Available from: 10.1017/CBO9780511542626.012 DOI
Garcia, M.A. , Nelson, W.J. & Chavez, N. (2018) Cell–cell junctions organize structural and signaling networks. Cold Spring Harbor Perspectives in Biology, 10(4), a029181. Available from: 10.1101/cshperspect.a029181 PubMed DOI PMC
Gonzalez Lopez, M. , Huteckova, B. , Lavicky, J. , Zezula, N. , Rakultsev, V. , Fridrichova, V. et al. (2023) Spatiotemporal monitoring of hard tissue development reveals unknown features of tooth and bone development. Science Advances, 2, eadi0482. Available from: 10.1126/sciadv.adi0482 PubMed DOI PMC
Hallett, S.A. , Ono, W. & Ono, N. (2021) The hypertrophic chondrocyte: to be or not to be. Histology and Histopathology, 10, 1021–1036. PubMed PMC
Handrigan, G.R. , Leung, K.J. & Richman, J.M. (2010) Identification of putative dental epithelial stem cells in a lizard with life‐long tooth replacement. Development, 137, 3545–3549. Available from: 10.1242/dev.052415 PubMed DOI
Handrigan, G.R. & Richman, J.M. (2010) Autocrine and paracrine shh signaling are necessary for tooth morphogenesis, but not tooth replacement in snakes and lizards (Squamata). Developmental Biology, 337, 171–186. Available from: 10.1016/j.ydbio.2009.10.020 PubMed DOI
Henriquez, J.I. , Flibotte, S. , Fu, K. & Richman, J.M. (2025) Molecular profiling of odontoclasts during physiological tooth replacement. Journal of Dental Research, 104, 561–571. Available from: 10.1177/00220345241304756 PubMed DOI PMC
Holness, C.L. & Simmons, D.L. (1993) Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood, 81(6), 1607–1613. PubMed
Howes, R.I. (1979) Root morphogenesis in ectopically transplanted pleurodont teeth of the iguana. Cells, Tissues, Organs, 103, 400–408. Available from: 10.1159/000145042 PubMed DOI
Huysseune, A. & Sire, J.‐Y. (1997) Structure and development of teeth in three Armoured catfish, DOI
Jiang, H. , Sodek, J. , Karsenty, G. , Thomas, H. , Ranly, D. & Chen, J. (1999) Expression of core binding factor Osf2/Cbfa‐1 and bone sialoprotein in tooth development. Mechanisms of Development, 81, 169–173. Available from: 10.1016/S0925-4773(98)00232-9 PubMed DOI
Kavková, M. , Šulcová, M. , Dumková, J. , Zahradníček, O. , Kaiser, J. , Tucker, A.S. et al. (2020) Coordinated labio‐lingual asymmetries in dental and bone development create a symmetrical acrodont dentition. Scientific Reports, 10(1), 22040. Available from: 10.1038/s41598-020-78939-2 PubMed DOI PMC
Kawasaki, K. (2009) The SCPP gene repertoire in bony vertebrates and graded differences in mineralized tissues. Development Genes and Evolution, 219, 147–157. Available from: 10.1007/s00427-009-0276-x PubMed DOI PMC
Kawasaki, K. , Keating, J.N. , Nakatomi, M. , Welten, M. , Mikami, M. , Sasagawa, I. et al. (2021) Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans. IScience, 24(1), 102023. Available from: 10.1016/j.isci.2020.102023 PubMed DOI PMC
Kodama, J. , Wilkinson, K.J. , Iwamoto, M. , Otsuru, S. & Enomoto‐Iwamoto, M. (2022) The role of hypertrophic chondrocytes in regulation of the cartilage‐to‐bone transition in fracture healing. Bone Reports, 17, 101616. Available from: 10.1016/j.bonr.2022.101616 PubMed DOI PMC
Komori, T. , Yagi, H. & Nomura, S. (1997) Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell, 89(5), 755–764. Available from: 10.1016/s0092-8674(00)80258-5 PubMed DOI
LeBlanc, A.R.H. , Brink, K.S. , Cullen, T.M. & Reisz, R.R. (2017) Evolutionary implications of tooth attachment versus tooth implantation: a case study using dinosaur, crocodilian, and mammal teeth. Journal of Vertebrate Paleontology, 37(5), e1354006. Available from: 10.1080/02724634.2017.1354006 DOI
LeBlanc, A.R.H. , Lamoureux, D.O. & Caldwell, M.W. (2017) Mosasaurs and snakes have a periodontal ligament: timing and extent of calcification, not tissue complexity, determines tooth attachment mode in reptiles. Journal of Anatomy, 231, 869–885. Available from: 10.1111/joa.12686 PubMed DOI PMC
LeBlanc, A.R.H. , Palci, A. , Anthwal, N. , Tucker, A.S. , Araújo, R. , Pereira, M.F.C. et al. (2023) A conserved tooth resorption mechanism in modern and fossil snakes. Nature Communications, 14(1), 742. Available from: 10.1038/s41467-023-36422-2 PubMed DOI PMC
LeBlanc, A.R.H. , Paparella, I. , Lamoureux, D.O. , Doschak, M.R. & Caldwell, M.W. (2021) Tooth attachment and pleurodont implantation in lizards: histology, development, and evolution. Journal of Anatomy, 238, 1156–1178. Available from: 10.1111/joa.13371 PubMed DOI PMC
LeBlanc, A.R.H. , Reisz, R.R. , Brink, K.S. & Abdala, F. (2016) Mineralized periodontia in extinct relatives of mammals shed light on the evolutionary history of mineral homeostasis in periodontal tissue maintenance. Journal of Clinical Periodontology, 43(4), 323–332. Available from: 10.1111/jcpe.12508 PubMed DOI
Lian, J.B. , Stein, G.S. , Javed, A. , Van Wijnen, A.J. , Stein, J.L. , Montecino, M. et al. (2006) Networks and hubs for the transcriptional control of osteoblastogenesis. Reviews in Endocrine and Metabolic Disorders, 7(1–2), 1–16. Available from: 10.1007/s11154-006-9001-5 PubMed DOI
Listgarten, M.A. & Shapiro, I.M. (1974) Fine structure and composition of coronal cementum in Guinea‐pig molars. Archives of Oral Biology, 19(8), 679–696. Available from: 10.1016/0003-9969(74)90137-X PubMed DOI
Liu, M. , Reed, D.A. , Cecchini, G.M. , Lu, X. , Ganjawalla, K. , Gonzales, C.S. et al. (2016) Varanoid tooth eruption and implantation modes in a late cretaceous mosasaur. Frontiers in Physiology, 7, 145. Available from: 10.3389/fphys.2016.00145 PubMed DOI PMC
Liu, W. , Selever, J. , Murali, D. , Sun, X. , Brugger, S.M. , Ma, L. et al. (2005) Threshold‐specific requirements for Bmp4 in mandibular development. Developmental Biology, 283, 282–293. Available from: 10.1016/j.ydbio.2005.04.019 PubMed DOI
Luan, X. , Walker, C. , Dangaria, S. , Ito, Y. , Druzinsky, R. , Jarosius, K. et al. (2009) The mosasaur tooth attachment apparatus as paradigm for the evolution of the gnathostome periodontium. Evolution and Development, 11, 247–259. Available from: 10.1111/j.1525-142X.2009.00327.x PubMed DOI PMC
Luckett, W.P. (1993) Ontogenetic staging of the mammalian dentition, and its value for assessment of homology and heterochrony. Journal of Mammalian Evolution, 1, 269–282. Available from: 10.1007/BF01041667 DOI
McIntosh, J.E. , Anderton, X. , Flores‐De‐Jacoby, L. , Carlson, D.S. , Shuler, C.F. & Diekwisch, T.G.H. (2002) Caiman periodontium as an intermediate between basal vertebrate ankylosis‐type attachment and mammalian ‘true’ periodontium. Microscopy Research and Technique, 59, 449–459. Available from: 10.1002/jemt.10222 PubMed DOI
Meunier, F.J. (2015) New data on the attachment of teeth in the angler fish
Oddie, G.W. , Schenk, G. , Angel, N.Z. , Walsh, N. , Guddat, L.W. , De, J. et al. (2000) Structure, function, and regulation of tartrate‐resistant acid phosphatase. Bone, 27(5), 575–584. Available from: 10.1016/s8756-3282(00)00368-9 PubMed DOI
Otto, F. , Thornell, A.P. , Crompton, T. , Denzel, A. , Gilmour, K.C. & Rosewell, I.R. (1997) Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell, 89(5), 765–771. Available from: 10.1016/s0092-8674(00)80259-7 PubMed DOI
Palone, M. , Casella, S. , Bastianoni, D. , Siciliani, G. & Lombardo, L. (2020) Lower incisor extraction therapy in a complex case with an ankylosed tooth in an adult patient: a case report. International Orthodontics, 18, 850–862. Available from: 10.1016/j.ortho.2020.08.006 PubMed DOI
Pautke, C. , Tischer, T. , Vogt, S. , Haczek, C. , Deppe, H. , Neff, A. et al. (2007) New advances in fluorochrome sequential labelling of teeth using seven different fluorochromes and spectral image analysis. Journal of Anatomy, 210, 117–121. Available from: 10.1111/j.1469-7580.2006.00660.x PubMed DOI PMC
Pautke, C. , Vogt, S. , Tischer, T. , Wexel, G. , Deppe, H. , Milz, S. et al. (2005) Polychrome labeling of bone with seven different fluorochromes: enhancing fluorochrome discrimination by spectral image analysis. Bone, 37, 441–445. Available from: 10.1016/j.bone.2005.05.008 PubMed DOI
Peyer, B. (1968) In: Zangerl, R. (Ed.) Comparative Odontology. Chicago: University of Chicago Press.
Rieppel, O. (2001) Tooth implantation and replacement in Sauropterygia. PalZ, 75, 207–217. Available from: 10.1007/BF02988014 DOI
Rieppel, O. & Kearney, M. (2005) Tooth replacement in the late cretaceous mosasaur Clidastes. Journal of Herpetology, 39(4), 688–692.
Rosa, J.T. , Witten, P.E. & Huysseune, A. (2021) Cells at the edge: the dentin–bone Interface in zebrafish teeth. Frontiers in Physiology, 12, 723210. Available from: 10.3389/fphys.2021.723210 PubMed DOI PMC
Sahara, N. , Ashizawa, Y. , Nakamura, K. , Deguchi, T. & Suzuki, K. (1998) Ultrastructural features of odontoclasts that resorb enamel in human deciduous teeth prior to shedding. Anatomical Record, 252, 215–228. Available from: 10.1002/(SICI)1097-0185(199810)252:2<215::AID-AR7>3.0.CO;2-1 PubMed DOI
Tan, W.H. , Witten, P.E. , Winkler, C. , Au, D.W.T. & Huysseune, A. (2017) Telomerase expression in medaka ( PubMed DOI
Tong, A. , Chow, Y.L. , Xu, K. , Hardiman, R. , Schneider, P. & Tan, S.S. (2020) Transcriptome analysis of ankylosed primary molars with infraocclusion. International Journal of Oral Science, 12(1), 7. Available from: 10.1038/s41368-019-0070-1 PubMed DOI PMC
Westergaard, B. & Ferguson, M.W.J. (1986) Development of the dentition in DOI
Westergaard, B. & Ferguson, M.W.J. (1987) Development of the dentition in PubMed DOI
Wu, X. , Hu, J. , Li, G. , Li, Y. , Li, Y. , Zhang, J. et al. (2020) Biomechanical stress regulates mammalian tooth replacement via the integrin β1‐RUNX2‐Wnt pathway. The EMBO Journal, 39(3), e102374. Available from: 10.15252/embj.2019102374 PubMed DOI PMC
Zaher, H. & Rieppel, O. (1999) Tooth implantation and replacement in squamates, with special reference to mosasaur lizards and snakes. American Museum Novitates, 3271, 1–19.
Zhu, D. , Li, G. , Fang, H. & Gao, Y. (2024) Emerging role of hypertrophic chondrocytes in tissue regeneration and fracture healing: a narrative review. European Cells and Materials, 47, 219–237. Available from: 10.22203/eCM.v047a14 DOI