Tooth-bone attachment tissue is produced by cells with a mixture of odontoblastic and osteoblastic features in reptiles

. 2026 Feb ; 248 (2) : 251-268. [epub] 20251119

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid41261944

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

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.

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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

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