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
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 vari...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-07-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fcell.2020.00572/full |
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| author | Marek Hampl Marek Hampl Jana Dumkova Michaela Kavkova Hana Dosedelova Anna Bryjova Oldrich Zahradnicek Oldrich Zahradnicek Martin Pyszko Milos Macholan Tomas Zikmund Jozef Kaiser Marcela Buchtova Marcela Buchtova |
| author_facet | Marek Hampl Marek Hampl Jana Dumkova Michaela Kavkova Hana Dosedelova Anna Bryjova Oldrich Zahradnicek Oldrich Zahradnicek Martin Pyszko Milos Macholan Tomas Zikmund Jozef Kaiser Marcela Buchtova Marcela Buchtova |
| author_sort | Marek Hampl |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-22T02:48:34Z |
| format | Article |
| id | doaj.art-234b1861cbcd4812849c026852a1f656 |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-12-22T02:48:34Z |
| publishDate | 2020-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-234b1861cbcd4812849c026852a1f6562022-12-21T18:41:27ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2020-07-01810.3389/fcell.2020.00572536750Polarized Sonic Hedgehog Protein Localization and a Shift in the Expression of Region-Specific Molecules Is Associated With the Secondary Palate Development in the Veiled ChameleonMarek Hampl0Marek Hampl1Jana Dumkova2Michaela Kavkova3Hana Dosedelova4Anna Bryjova5Oldrich Zahradnicek6Oldrich Zahradnicek7Martin Pyszko8Milos Macholan9Tomas Zikmund10Jozef Kaiser11Marcela Buchtova12Marcela Buchtova13Laboratory of Molecular Morphogenesis, Institute of Animal Physiology and Genetics, Czech Academy of Sciences, Brno, CzechiaDepartment of Experimental Biology, Faculty of Science, Masaryk University, Brno, CzechiaDepartment of Histology and Embryology, Faculty of Medicine, Masaryk University, Brno, CzechiaLaboratory of Computed Tomography, Central European Institute of Technology, Brno University of Technology, Brno, CzechiaLaboratory of Molecular Morphogenesis, Institute of Animal Physiology and Genetics, Czech Academy of Sciences, Brno, CzechiaInstitute of Vertebrate Biology, Czech Academy of Sciences, Brno, CzechiaDepartment of Developmental Biology, Institute of Experimental Medicine, Czech Academy of Sciences, Prague, CzechiaDepartment of Radiation Dosimetry, Nuclear Physics Institute, Czech Academy of Sciences, Prague, CzechiaDepartment of Anatomy, Histology, and Embryology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Brno, CzechiaLaboratory of Mammalian Evolutionary Genetics, Institute of Animal Physiology and Genetics, Czech Academy of Sciences, Brno, CzechiaLaboratory of Computed Tomography, Central European Institute of Technology, Brno University of Technology, Brno, CzechiaLaboratory of Computed Tomography, Central European Institute of Technology, Brno University of Technology, Brno, CzechiaLaboratory of Molecular Morphogenesis, Institute of Animal Physiology and Genetics, Czech Academy of Sciences, Brno, CzechiaDepartment of Experimental Biology, Faculty of Science, Masaryk University, Brno, CzechiaSecondary 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.https://www.frontiersin.org/article/10.3389/fcell.2020.00572/fullsecondary palateSHHprimary ciliaskeletogenesischameleonreptile |
| spellingShingle | Marek Hampl Marek Hampl Jana Dumkova Michaela Kavkova Hana Dosedelova Anna Bryjova Oldrich Zahradnicek Oldrich Zahradnicek Martin Pyszko Milos Macholan Tomas Zikmund Jozef Kaiser Marcela Buchtova Marcela Buchtova 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 Frontiers in Cell and Developmental Biology secondary palate SHH primary cilia skeletogenesis chameleon reptile |
| title | 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 |
| title_full | 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 |
| title_fullStr | 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 |
| title_full_unstemmed | 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 |
| title_short | 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 |
| title_sort | 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 |
| topic | secondary palate SHH primary cilia skeletogenesis chameleon reptile |
| url | https://www.frontiersin.org/article/10.3389/fcell.2020.00572/full |
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