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Coordinated labio-lingual asymmetries in dental and bone development create a symmetrical acrodont dentition

. 2020 Dec 16 ; 10 (1) : 22040. [epub] 20201216

Language English Country Great Britain, England Media electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Links

PubMed 33328503
PubMed Central PMC7745041
DOI 10.1038/s41598-020-78939-2
PII: 10.1038/s41598-020-78939-2
Knihovny.cz E-resources

Organs throughout the body develop both asymmetrically and symmetrically. Here, we assess how symmetrical teeth in reptiles can be created from asymmetrical tooth germs. Teeth of lepidosaurian reptiles are mostly anchored to the jaw bones by pleurodont ankylosis, where the tooth is held in place on the labial side only. Pleurodont teeth are characterized by significantly asymmetrical development of the labial and lingual sides of the cervical loop, which later leads to uneven deposition of hard tissue. On the other hand, acrodont teeth found in lizards of the Acrodonta clade (i.e. agamas, chameleons) are symmetrically ankylosed to the jaw bone. Here, we have focused on the formation of the symmetrical acrodont dentition of the veiled chameleon (Chamaeleo calyptratus). Intriguingly, our results revealed distinct asymmetries in morphology of the labial and lingual sides of the cervical loop during early developmental stages, both at the gross and ultrastructural level, with specific patterns of cell proliferation and stem cell marker expression. Asymmetrical expression of ST14 was also observed, with a positive domain on the lingual side of the cervical loop overlapping with the SOX2 domain. In contrast, micro-CT analysis of hard tissues revealed that deposition of dentin and enamel was largely symmetrical at the mineralization stage, highlighting the difference between cervical loop morphology during early development and differentiation of odontoblasts throughout later odontogenesis. In conclusion, the early asymmetrical development of the enamel organ seems to be a plesiomorphic character for all squamate reptiles, while symmetrical and precisely orchestrated deposition of hard tissue during tooth formation in acrodont dentitions probably represents a novelty in the Acrodonta clade.

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LeBlanc ARH, Brink KS, Cullen TM, Reisz RR. Evolutionary implications of tooth attachment versus tooth implantation: a case study using dinosaur, crocodilian, and mammalian teeth. J. Vertebr. Paleontol. 2017;37:19. doi: 10.1080/02724634.2017.1354006. DOI

Luan XH, Ito Y, Diekwisch TGH. Evolution and development of Hertwig's epithelial root sheath. Dev. Dyn. 2006;235:1167–1180. doi: 10.1002/dvdy.20674. PubMed DOI PMC

Bertin TJC, Thivichon-Prince B, LeBlanc ARH, Caldwell MW, Viriot L. Current perspectives on tooth implantation, attachment, and replacement in amniota. Front. Physiol. 2018;9:20. doi: 10.3389/fphys.2018.01630. PubMed DOI PMC

Gaenger, P. Evolution of tooth attachment in lower vertebrates to tetrapods. In Development, Function, and Evolution of Teeth (Teaford, M.F., Smith, M.M. & Ferguson, M.W.J.) 173–185 (Cambridge University Press, Cambridge, 2000).

Zahradnicek O, Horacek I, Tucker AS. Tooth development in a model reptile: functional and null generation teeth in the gecko Paroedura picta. J. Anat. 2012;221:195–208. doi: 10.1111/j.1469-7580.2012.01531.x. PubMed DOI PMC

Delgado S, Davit-Beal T, Allizard F, Sire JY. Tooth development in a scincid lizard, Chalcides viridanus (Squamata), with particular attention to enamel formation. Cell Tissue Res. 2005;319:71–89. doi: 10.1007/s00441-004-0950-2. PubMed DOI

Osborn JW. The ontogeny of tooth succession in Lacerta vivipara Jacquin (1787) Proc. R. Soc. Lond. B. Biol. Sci. 1971;179:261–289. doi: 10.1098/rspb.1971.0097. PubMed DOI

Juuri E, et al. Sox2 marks epithelial competence to generate teeth in mammals and reptiles. Development. 2013;140:1424–1432. doi: 10.1242/dev.089599. PubMed DOI PMC

Jenkins KM, Jones MEH, Zikmund T, Boyde A, Daza JD. A Review of tooth implantation among rhynchocephalians (Lepidosauria) J. Herpetol. 2017;51:300–306. doi: 10.1670/16-146. DOI

Buchtova M, Zahradnicek O, Balkova S, Tucker AS. Odontogenesis in the Veiled Chameleon (Chamaeleo calyptratus) Arch. Oral Biol. 2013;58:118–133. doi: 10.1016/j.archoralbio.2012.10.019. PubMed DOI

Harrison HS. The development and succession of teeth in Hatteria punctata. Q. J. Microsc. Sci. 1901;44:161–U113.

Haridy Y, LeBlanc ARH, Reisz RR. The Permian reptile Opisthodontosaurus carrolli: a model for acrodont tooth replacement and dental ontogeny. J. Anat. 2018;232:371–382. doi: 10.1111/joa.12754. PubMed DOI PMC

Salomies L, Eymann J, Khan I, Di-Poï N. The alternative regenerative strategy of bearded dragon unveils the key processes underlying vertebrate tooth renewal. Elife. 2019 doi: 10.7554/eLife.47702. PubMed DOI PMC

Simoes TR, Wilner E, Caldwell MW, Weinschutz LC, Kellner AWA. A stem acrodontan lizard in the Cretaceous of Brazil revises early lizard evolution in Gondwana. Nat. Commun. 2015;6:8. doi: 10.1038/ncomms9149. PubMed DOI PMC

Hedges SB. Amniote phylogeny and the position of turtles. BMC Biol. 2012;10:64. doi: 10.1186/1741-7007-10-64. PubMed DOI PMC

Zheng Y, Wiens JJ. Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Mol. Phylogenet. Evol. 2016;94:537–547. doi: 10.1016/j.ympev.2015.10.009. PubMed DOI

Sulcova ML, et al. Developmental mechanisms driving complex tooth shape in reptiles. Dev. Dynam. 2020 doi: 10.1002/dvdy.138. PubMed DOI

Diaz-Paniagua C, Cuadrado M. Influence of incubation conditions on hatching success, embryo development and hatchling phenotype of common chameleon (Chamaeleo chamaeleon) eggs. Amphibia-Reptilia. 2003;24:429–440. doi: 10.1163/156853803322763891. DOI

Diaz-Paniagua C. Effect of cold temperature on the length of incubation of Chamaeleo chamaeleon. Amphibia-Reptilia. 2007;28:387–392. doi: 10.1163/156853807781374782. DOI

Andrews RM. Effects of temperature on embryonic development of the veiled chameleon, Chamaeleo calyptratus. Comp. Biochem. Physiol. A. 2007;148:698–706. doi: 10.1016/j.cbpa.2007.08.026. PubMed DOI

Peterka M, Lesot H, Peterkova R. Body weight in mouse embryos specifies staging of tooth development. Connect. Tissue Res. 2002;43:186–190. doi: 10.1080/03008200290000673. PubMed DOI

Buchtova, M., Handrigan, G. R., Tucker, A. S., Lozanoff, S., Town, L., Fu, K., Diewert, V. M., Wicking, C. & Richman, J. M. Initiation and patterning of the snake dentition are dependent on Sonic hedgehog signaling. Dev. Biol.319(1), 132–145 (2008). PubMed

List K, et al. Epithelial integrity is maintained by a matriptase-dependent proteolytic pathway. Am. J. Pathol. 2009;175:1453–1463. doi: 10.2353/ajpath.2009.090240. PubMed DOI PMC

List K, et al. Matriptase/MT-SP1 is required for postnatal survival, epidermal barrier function, hair follicle development, and thymic homeostasis. Oncogene. 2002;21:3765–3779. doi: 10.1038/sj/onc/1205502. PubMed DOI

Oberst MD, et al. Characterization of matriptase expression in normal human tissues. J. Histochem. Cytochem. 2003;51:1017–1025. doi: 10.1177/002215540305100805. PubMed DOI

Zahradnicek O, Buchtova M, Dosedelova H, Tucker AS. The development of complex tooth shape in reptiles. Front. Physiol. 2014;5:7. doi: 10.3389/fphys.2014.00074. PubMed DOI PMC

Handrigan GR, Richman JM. Autocrine and paracrine Shh signaling are necessary for tooth morphogenesis, but not tooth replacement in snakes and lizards (Squamata) Dev. Biol. 2010;337:171–186. doi: 10.1016/j.ydbio.2009.10.020. PubMed DOI

Handrigan GR, Richman JM. Unicuspid and bicuspid tooth crown formation in squamates. J. Exp. Zool. B. 2011;316B:598–608. doi: 10.1002/jezmde.21438. PubMed DOI

Lesot H, et al. Initial features of the inner dental epithelium histo-morphogenesis in the first lower molar in mouse. Int. J. Dev. Biol. 1999;43:245–254. PubMed

Hu JKH, Mushegyan V, Klein OD. On the cutting edge of organ renewal: identification, regulation, and evolution of incisor stem cells. Genesis. 2014;52:79–92. doi: 10.1002/dvg.22732. PubMed DOI PMC

Green KJ, Jones JCR. Desmosomes and hemidesmosomes: Structure and function of molecular components. Faseb J. 1996;10:871–881. doi: 10.1096/fasebj.10.8.8666164. PubMed DOI

Ohshima H, Wartiovaara J, Thesleff I. Developmental regulation and ultrastructure of glycogen deposits during murine tooth morphogenesis. Cell Tissue Res. 1999;297:271–281. doi: 10.1007/s004410051355. PubMed DOI

Ida-Yonemochi H, et al. Glucose uptake mediated by glucose transporter 1 is essential for early tooth morphogenesis and size determination of murine molars. Dev. Biol. 2012;363:52–61. doi: 10.1016/j.ydbio.2011.12.020. PubMed DOI

Morita R, et al. Coordination of cellular dynamics contributes to tooth epithelium deformations. PLoS ONE. 2016;11:20. doi: 10.1371/journal.pone.0161336. PubMed DOI PMC

Arnold K, et al. Sox2(+) adult stem and progenitor cells are important for tissue regeneration and survival of mice. Cell Stem Cell. 2011;9:317–329. doi: 10.1016/j.stem.2011.09.001. PubMed DOI PMC

Buchtova M, Stembirek J, Glocova K, Matalova E, Tucker AS. Early regression of the dental lamina underlies the development of diphyodont dentitions. J. Dent. Res. 2012;91:491–498. doi: 10.1177/0022034512442896. PubMed DOI

Luo JF, Yan RC, He XB, He J. SOX2 inhibits cell proliferation and metastasis, promotes apoptotic by downregulating CCND1 and PARP in gastric cancer. Am. J. Transl. Res. 2018;10:639–647. PubMed PMC

Popa EM, Buchtova M, Tucker AS. Revitalising the rudimentary replacement dentition in the mouse. Development. 2019;146:11. doi: 10.1242/dev.171363. PubMed DOI

Jussila M, Yanezl XC, Thesleff I. Initiation of teeth from the dental lamina in the ferret. Differentiation. 2014;87:32–43. doi: 10.1016/j.diff.2013.11.004. PubMed DOI

Dosedelova H, et al. Age-related changes in the tooth-bone interface area of acrodont dentition in the chameleon. J. Anat. 2016;229:356–368. doi: 10.1111/joa.12490. PubMed DOI PMC

Grimes DT. Making and breaking symmetry in development, growth and disease. Development. 2019;146:12. doi: 10.1242/dev.170985. PubMed DOI PMC

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