Polarized Sonic Hedgehog Protein Localization and a Shift in the Expression of Region-Specific Molecules Is Associated With the Secondary Palate Development in the Veiled Chameleon

. 2020 ; 8 () : 572. [epub] 20200728

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32850780

Secondary palate development is characterized by the formation of two palatal shelves on the maxillary prominences, which fuse in the midline in mammalian embryos. However, in reptilian species, such as turtles, crocodilians, and lizards, the palatal shelves of the secondary palate develop to a variable extent and morphology. While in most Squamates, the palate is widely open, crocodilians develop a fully closed secondary palate. Here, we analyzed developmental processes that underlie secondary palate formation in chameleons, where large palatal shelves extend horizontally toward the midline. The growth of the palatal shelves continued during post-hatching stages and closure of the secondary palate can be observed in several adult animals. The massive proliferation of a multilayered oral epithelium and mesenchymal cells in the dorsal part of the palatal shelves underlined the initiation of their horizontal outgrowth, and was decreased later in development. The polarized cellular localization of primary cilia and Sonic hedgehog protein was associated with horizontal growth of the palatal shelves. Moreover, the development of large palatal shelves, supported by the pterygoid and palatine bones, was coupled with the shift in Meox2, Msx1, and Pax9 gene expression along the rostro-caudal axis. In conclusion, our results revealed distinctive developmental processes that contribute to the expansion and closure of the secondary palate in chameleons and highlighted divergences in palate formation across amniote species.

Zobrazit více v PubMed

Abramyan J., Leung K. J., Richman J. M. (2014). Divergent palate morphology in turtles and birds correlates with differences in proliferation and BMP2 expression during embryonic development. J. Exp. Zool. B Mol. Dev. Evol. 322 73–85. 10.1002/jez.b.22547 PubMed DOI PMC

Abramyan J., Richman J. M. (2015). Recent insights into the morphological diversity in the amniote primary and secondary palates. Dev. Dyn. 244 1457–1468. 10.1002/dvdy.24338 PubMed DOI PMC

Anderson C. V., Deban S. M. (2010). Ballistic tongue projection in chameleons maintains high performance at low temperature. Proc. Natl. Acad. Sci. U.S.A. 107 5495–5499. 10.1073/pnas.0910778107 PubMed DOI PMC

Anderson C. V., Deban S. M. (2012). Thermal effects on motor control and in vitro muscle dynamics of the ballistic tongue apparatus in chameleons. J. Exp. Biol. 215 4345–4357. 10.1242/jeb.078881 PubMed DOI

Andrews R. M. (2007). Effects of temperature on embryonic development of the veiled chameleon, Chamaeleo calyptratus. Comp. Biochem. Physiol. A. Mol. Integr. Physiol 148 698–706. 10.1016/j.cbpa.2007.08.026 PubMed DOI

Andrews R. M., Donoghue S. (2004). Effects of temperature and moisture on embryonic diapause of the veiled chameleon (Chamaeleo calyptratus). J. Exp. Zool. A Comp. Exp. Biol. 301 629–635. 10.1002/jez.a.56 PubMed DOI

Brugmann S. A., Allen N. C., James A. W., Mekonnen Z., Madan E., Helms J. A. (2010). A primary cilia-dependent etiology for midline facial disorders. Hum. Mol. Genet. 19 1577–1592. 10.1093/hmg/ddq030 PubMed DOI PMC

Buchtová M., Zahradněček O., Balková S., Tucker A. S. (2013). Odontogenesis in the veiled chameleon (Chamaeleo calyptratus). Arch. Oral. Biol. 58 118–133. 10.1016/j.archoralbio.2012.10.019 PubMed DOI

Bush J. O., Jiang R. (2012). Palatogenesis: morphogenetic and molecular mechanisms of secondary palate development. Development 139 231–243. 10.1242/dev.067082 PubMed DOI PMC

Crompton A. (1995). Masticatory Function in Nonmammalian Cynodonts and Early Mammals. Functional Morphology in Vertebrate Paleontology. Cambridge: Cambridge University Press.

Daza J. D., Mapps A. A., Lewis P. J., Thies M. L., Bauer A. M. (2015). Peramorphic traits in the tokay gecko skull. J. Morphol. 276 915–928. 10.1002/jmor.20389 PubMed DOI

Diaz J. R. E., Trainor P. A. (2019). An Integrative View of Lepidosaur Cranial Anatomy, Development and Diversification. Heads, Jaws and Muscles Anatomical, Functional and Developmental Diversity in Chordate Evolution. Cham: Springer.

Diaz R. E., Anderson C. V., Baumann D. P., Kupronis R., Jewell D., Piraquive C., et al. (2015). The veiled chameleon (Chamaeleo calyptratus Duméril and Duméril 1851): a model for studying reptile body plan development and evolution. Cold Spring Harb. Protoc. 2015 889–894. PubMed

Diaz R. E., Shylo N. A., Roellig D., Bronner M., Trainor P. A. (2019). Filling in the phylogenetic gaps: induction, migration, and differentiation of neural crest cells in a squamate reptile, the veiled chameleon (Chamaeleo calyptratus). Dev. Dyn. 248 709–727. 10.1002/dvdy.38 PubMed DOI

Diaz R. E., Trainor P. A. (2015). Hand/foot splitting and the ’re-evolution’ of mesopodial skeletal elements during the evolution and radiation of chameleons. BMC Evol. Biol. 15:184. 10.1186/s12862-015-0464-4 PubMed DOI PMC

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. J. Anat. 229 356–368. 10.1111/joa.12490 PubMed DOI PMC

Duldulao N. A., Lee S., Sun Z. (2009). Cilia localization is essential for in vivo functions of the Joubert syndrome protein Arl13b/Scorpion. Development 136 4033–4042. 10.1242/dev.036350 PubMed DOI PMC

Ferguson M. W. (1981a). Review: the value of the American alligator (Alligator mississippiensis) as a model for research in craniofacial development. J. Craniofac. Genet. Dev. Biol. 1 123–144. PubMed

Ferguson M. W. (1981b). The structure and development of the palate in Alligator mississippiensis. Arch. Oral. Biol. 26 427–443. 10.1016/0003-9969(81)90041-8 PubMed DOI

Ferguson M. W. (1987). Palate development: mechanisms and malformations. Ir. J. Med. Sci. 156 309–315. 10.1007/bf02951261 PubMed DOI

Ferguson M. W. (1988). Palate development. Development 103(Suppl), 41–60. PubMed

Grbic D., Saenko S. V., Randriamoria T. M., Debry A., Raselimanana A. P., Milinkovitch M. C. (2015). Phylogeography and support vector machine classification of colour variation in panther chameleons. Mol. Ecol. 24 3455–3466. 10.1111/mec.13241 PubMed DOI PMC

Greene R. M., Pratt R. M. (1976). Developmental aspects of secondary palate formation. J. Embryol. Exp. Morphol. 36 225–245. PubMed

Hampl M., Cela P., Szabo-Rogers H. L., Bosakova M. K., Dosedelova H., Krejci P., et al. (2017). Role of primary cilia in odontogenesis. J. Dent. Res. 96 965–974. 10.1177/0022034517713688 PubMed DOI PMC

Hanken J., Thorogood P. (1993). Evolution and development of the vertebrate skull: the role of pattern formation. Trends Ecol. Evol. 8 9–15. 10.1016/0169-5347(93)90124-8 PubMed DOI

Haycraft C. J., Banizs B., Aydin-Son Y., Zhang Q., Michaud E. J., Yoder B. K. (2005). Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet. 1:e53. 10.1371/journal.pgen.0010053 PubMed DOI PMC

Hedges S. B. (2012). Amniote phylogeny and the position of turtles. BMC Biol. 10:64. 10.1186/1741-7007-10-64 PubMed DOI PMC

Hernández-Jaimes C., Jerez A., Ramírez-Pinilla M. P. (2012). Embryonic development of the skull of the Andean lizard Ptychoglossus bicolor (Squamata, Gymnophthalmidae). J. Anat. 221 285–302. 10.1111/j.1469-7580.2012.01549.x PubMed DOI PMC

Herrel A., Redding C. L., Meyers J. J., Nishikawa K. C. (2014). The scaling of tongue projection in the veiled chameleon, Chamaeleo calyptratus. Zoology 117 227–236. 10.1016/j.zool.2014.01.001 PubMed DOI

Huangfu D., Anderson K. V. (2005). Cilia and Hedgehog responsiveness in the mouse. Proc. Natl. Acad. Sci. U.S.A. 102 11325–11330. 10.1073/pnas.0505328102 PubMed DOI PMC

Huangfu D., Liu A., Rakeman A. S., Murcia N. S., Niswander L., Anderson K. V. (2003). Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426 83–87. 10.1038/nature02061 PubMed DOI

Iordansky N. (2016). Functional relationships in the jaw apparatus of the chameleons and the evolution of adaptive complexes. Zool. Z. 95 1173–1181.

Iwabe N., Hara Y., Kumazawa Y., Shibamoto K., Saito Y., Miyata T., et al. (2005). Sister group relationship of turtles to the bird-crocodilian clade revealed by nuclear DNA-coded proteins. Mol. Biol. Evol. 22 810–813. 10.1093/molbev/msi075 PubMed DOI

Jankowski R. (2013). The Complex Formation of the Secondary Palate and Nose in Evolution, The Evo-Devo Origin of the Nose, Anterior Skull Base and Midface. Cham: Springer, 41–61.

Jin J. Z., Ding J. (2006). Analysis of Meox-2 mutant mice reveals a novel postfusion-based cleft palate. Dev. Dyn. 235 539–546. 10.1002/dvdy.20641 PubMed DOI

Jin J. Z., Ding J. (2015). Strain-dependent gene expression during mouse embryonic palate development. J. Dev. Biol. 3 2–10. 10.3390/jdb3010002 PubMed DOI PMC

Johnson M. L. (1933). The time and order of appearance of ossification centers in the albino mouse. Am. J. Anat. 52 241–271. 10.1002/aja.1000520203 DOI

Jones M. E., Werneburg I., Curtis N., Penrose R., O’higgins P., Fagan M. J., et al. (2012). The head and neck anatomy of sea turtles (Cryptodira: Chelonioidea) and skull shape in testudines. PLoS One 7:e47852. 10.1371/journal.pone.0047852 PubMed DOI PMC

Kanazawa E., Mochizuki K. (1974). The time and order of appearance of ossification centers in the hamster before birth. Jikken Dobutsu 23 113–122. 10.1538/expanim1957.23.3_113 PubMed DOI

Kimmel C. B., Sidlauskas B., Clack J. A. (2009). Linked morphological changes during palate evolution in early tetrapods. J. Anat. 215 91–109. 10.1111/j.1469-7580.2009.01108.x PubMed DOI PMC

Krmpotić-Nemanić J., Vinter I., Marusić A. (2006). Relations of the pterygoid hamulus and hard palate in children and adults: anatomical implications for the function of the soft palate. Ann. Anat. 188 69–74. 10.1016/j.aanat.2005.05.005 PubMed DOI

Le Pabic P., Ng C., Schilling T. F. (2014). Fat-Dachsous signaling coordinates cartilage differentiation and polarity during craniofacial development. PLoS Genet. 10:e1004726. 10.1371/journal.pgen.1004726 PubMed DOI PMC

Li J., Johnson C. A., Smith A. A., Hunter D. J., Singh G., Brunski J. B., et al. (2016). Linking suckling biomechanics to the development of the palate. Sci. Rep. 6:20419. PubMed PMC

Mo R., Freer A. M., Zinyk D. L., Crackower M. A., Michaud J., Heng H. H., et al. (1997). Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development 124 113–123. PubMed

Mohamed R. (2018). Anatomical and radiographic study on the skull and mandible of the common opossum. Vet. Sci. 5:44. 10.3390/vetsci5020044 PubMed DOI PMC

Namkoong B. (2015). The Molecular Determinants of Cranial Skeletal Development and Evolution. Dissertation Thesis, Harvard University, Cambridge, MA.

Ollonen J., Da Silva F. O., Mahlow K., Di-Poï N. (2018). Skull development, ossification pattern, and adult shape in the emerging lizard model organism. Front. Physiol. 9:278. 10.3389/fphys.2018.00278 PubMed DOI PMC

Pinto B. J., Card D. C., Castoe T. A., Diaz R. E., Nielsen S. V., Trainor P. A., et al. (2019). The transcriptome of the veiled chameleon (Chamaeleo calyptratus): a resource for studying the evolution and development of vertebrates. Dev. Dyn. 248 702–708. 10.1002/dvdy.20 PubMed DOI

Presley R., Steel F. L. (1978). The pterygoid and ectopterygoid in mammals. Anat. Embryol. 154 95–110. 10.1007/bf00317957 PubMed DOI

Rice R., Connor E., Rice D. P. (2006). Expression patterns of Hedgehog signalling pathway members during mouse palate development. Gene Expr. Patterns 6 206–212. 10.1016/j.modgep.2005.06.005 PubMed DOI

Richman J. M., Buchtová M., Boughner J. C. (2006). Comparative ontogeny and phylogeny of the upper jaw skeleton in amniotes. Dev. Dyn. 235 1230–1243. 10.1002/dvdy.20716 PubMed DOI

Rieppel O. (1993). Studies on skeleton formation in reptiles. v. Patterns of ossification in the skeleton of Alligator mississippiensis DAUDIN (Reptilia, Crocodylia). Zool. J. Linn. Soc. 109 301–325. 10.1111/j.1096-3642.1993.tb02537.x DOI

Rieppel O., Crumly C. (2009). Paedomorphosis and skull structure in Malagasy chamaeleons (Reptilia: Chamaeleoninae). J. Zool. 243 351–380. 10.1111/j.1469-7998.1997.tb02788.x DOI

Romer A. S. (1956). Osteology of the Reptiles. Chicago, IL: University of Chicago Press.

Schock E. N., Chang C. F., Youngworth I. A., Davey M. G., Delany M. E., Brugmann S. A. (2016). Utilizing the chicken as an animal model for human craniofacial ciliopathies. Dev. Biol. 415 326–337. 10.1016/j.ydbio.2015.10.024 PubMed DOI PMC

Sheil C. A. (2005). Skeletal development of Macrochelys temminckii (Reptilia: Testudines: Chelydridae). J. Morphol. 263 71–106. 10.1002/jmor.10290 PubMed DOI

Shi J., Zhao Y., Galati D., Winey M., Klymkowsky M. W. (2014). Chibby functions in Xenopus ciliary assembly, embryonic development, and the regulation of gene expression. Dev. Biol. 395 287–298. 10.1016/j.ydbio.2014.09.008 PubMed DOI PMC

Sperber G. H., Sperber S. M., Guttmann G. D. (eds) (2012). Craniofacial Embryogenetics and Development, 2nd Edn Shelton: PMPH USA Ltd.

Stower M. J., Diaz R. E., Fernandez L. C., Crother M. W., Crother B., Marco A., et al. (2015). Bi-modal strategy of gastrulation in reptiles. Dev. Dyn. 29 1144–1157. 10.1002/dvdy.24300 PubMed DOI

Tamarin A. (1982). The formation of the primitive choanae and the junction of the primary and secondary palates in the mouse. Am. J. Anat. 165 319–337. 10.1002/aja.1001650308 PubMed DOI

Tokita M., Chaeychomsri W., Siruntawineti J. (2013). Developmental basis of toothlessness in turtles: insight into convergent evolution of vertebrate morphology. Evolution 67 260–273. 10.1111/j.1558-5646.2012.01752.x PubMed DOI

Tolley K. A., Herrel A. (2015). The Biology of Chameleons. Berkeley, CA: University of California Press.

Wheatley D. N., Wang A. M., Strugnell G. E. (1996). Expression of primary cilia in mammalian cells. Cell Biol. Int. 20 73–81. 10.1006/cbir.1996.0011 PubMed DOI

Yu K., Ornitz D. M. (2011). Histomorphological study of palatal shelf elevation during murine secondary palate formation. Dev. Dyn. 240 1737–1744. 10.1002/dvdy.22670 PubMed DOI PMC

Zahradnicek O., Buchtova M., Dosedelova H., Tucker A. S. (2014). The development of complex tooth shape in reptiles. Front. Physiol. 5:74. 10.3389/fphys.2014.00074 PubMed DOI PMC

Zhang Z., Song Y., Zhao X., Zhang X., Fermin C., Chen Y. (2002). Rescue of cleft palate in Msx1-deficient mice by transgenic Bmp4 reveals a network of BMP and Shh signaling in the regulation of mammalian palatogenesis. Development 129 4135–4146. PubMed

Zheng Y., Wiens J. J. (2016). 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. 94 537–547. 10.1016/j.ympev.2015.10.009 PubMed DOI

Zhou J., Gao Y., Lan Y., Jia S., Jiang R. (2013). Pax9 regulates a molecular network involving Bmp4, Fgf10, Shh signaling and the Osr2 transcription factor to control palate morphogenesis. Development 140 4709–4718. 10.1242/dev.099028 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace