Genome-wide identification and spatiotemporal expression analysis of cadherin superfamily members in echinoderms
Abstract Background Cadherins are calcium-dependent transmembrane cell–cell adhesion proteins that are essential for metazoan development. They consist of three subfamilies: classical cadherins, which bind catenin, protocadherins, which contain 6–7 calcium-binding repeat domains, and atypical cadher...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-12-01
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| Series: | EvoDevo |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13227-023-00219-7 |
| _version_ | 1797376937102934016 |
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| author | Macie M. Chess William Douglas Josiah Saunders Charles A. Ettensohn |
| author_facet | Macie M. Chess William Douglas Josiah Saunders Charles A. Ettensohn |
| author_sort | Macie M. Chess |
| collection | DOAJ |
| description | Abstract Background Cadherins are calcium-dependent transmembrane cell–cell adhesion proteins that are essential for metazoan development. They consist of three subfamilies: classical cadherins, which bind catenin, protocadherins, which contain 6–7 calcium-binding repeat domains, and atypical cadherins. Their functions include forming adherens junctions, establishing planar cell polarity (PCP), and regulating cell shape, proliferation, and migration. Because they are basal deuterostomes, echinoderms provide important insights into bilaterian evolution, but their only well-characterized cadherin is G-cadherin, a classical cadherin that is expressed by many embryonic epithelia. We aimed to better characterize echinoderm cadherins by conducting phylogenetic analyses and examining the spatiotemporal expression patterns of cadherin-encoding genes during Strongylocentrotus purpuratus development. Results Our phylogenetic analyses conducted on two echinoid, three asteroid, and one crinoid species identified ten echinoderm cadherins, including one deuterostome-specific ortholog, cadherin-23, and an echinoderm-specific atypical cadherin that possibly arose in an echinoid-asteroid ancestor. Catenin-binding domains in dachsous-2 orthologs were found to be a deuterostome-specific innovation that was selectively lost in mouse, while those in Fat4 orthologs appeared to be Ambulacraria-specific and were selectively lost in non-crinoid echinoderms. The identified suite of echinoderm cadherins lacks vertebrate-specific innovations but contains two proteins that are present in protostomes and absent from mouse. The spatiotemporal expression patterns of four embryonically expressed cadherins (fat atypical cadherins 1 and 4, dachsous-2, and protocadherin-9) were dynamic and mirrored the expression pattern of Frizzled 5/8, a non-canonical Wnt PCP pathway receptor protein essential for archenteron morphogenesis. Conclusions The echinoderm cadherin toolkit is more similar to that of an ancient bilaterian predating protostomes and deuterostomes than it is to the suite of cadherins found in extant vertebrates. However, it also appears that deuterostomes underwent several cadherin-related innovations. Based on their similar spatiotemporal expression patterns and orthologous relationships to PCP-related and tumor-suppressing proteins, we hypothesize that sea urchin cadherins may play a role in regulating the shape and growth of embryonic epithelia and organs. Future experiments will examine cadherin expression in non-echinoid echinoderms and explore the functions of cadherins during echinoderm development. |
| first_indexed | 2024-03-08T19:46:42Z |
| format | Article |
| id | doaj.art-cc68e3024b5c4e11b3b1df2e1e1500f7 |
| institution | Directory Open Access Journal |
| issn | 2041-9139 |
| language | English |
| last_indexed | 2024-03-08T19:46:42Z |
| publishDate | 2023-12-01 |
| publisher | BMC |
| record_format | Article |
| series | EvoDevo |
| spelling | doaj.art-cc68e3024b5c4e11b3b1df2e1e1500f72023-12-24T12:21:27ZengBMCEvoDevo2041-91392023-12-0114111510.1186/s13227-023-00219-7Genome-wide identification and spatiotemporal expression analysis of cadherin superfamily members in echinodermsMacie M. Chess0William Douglas1Josiah Saunders2Charles A. Ettensohn3Department of Biological Sciences, Carnegie Mellon UniversityDepartment of Biological Sciences, Carnegie Mellon UniversityDepartment of Biological Sciences, Carnegie Mellon UniversityDepartment of Biological Sciences, Carnegie Mellon UniversityAbstract Background Cadherins are calcium-dependent transmembrane cell–cell adhesion proteins that are essential for metazoan development. They consist of three subfamilies: classical cadherins, which bind catenin, protocadherins, which contain 6–7 calcium-binding repeat domains, and atypical cadherins. Their functions include forming adherens junctions, establishing planar cell polarity (PCP), and regulating cell shape, proliferation, and migration. Because they are basal deuterostomes, echinoderms provide important insights into bilaterian evolution, but their only well-characterized cadherin is G-cadherin, a classical cadherin that is expressed by many embryonic epithelia. We aimed to better characterize echinoderm cadherins by conducting phylogenetic analyses and examining the spatiotemporal expression patterns of cadherin-encoding genes during Strongylocentrotus purpuratus development. Results Our phylogenetic analyses conducted on two echinoid, three asteroid, and one crinoid species identified ten echinoderm cadherins, including one deuterostome-specific ortholog, cadherin-23, and an echinoderm-specific atypical cadherin that possibly arose in an echinoid-asteroid ancestor. Catenin-binding domains in dachsous-2 orthologs were found to be a deuterostome-specific innovation that was selectively lost in mouse, while those in Fat4 orthologs appeared to be Ambulacraria-specific and were selectively lost in non-crinoid echinoderms. The identified suite of echinoderm cadherins lacks vertebrate-specific innovations but contains two proteins that are present in protostomes and absent from mouse. The spatiotemporal expression patterns of four embryonically expressed cadherins (fat atypical cadherins 1 and 4, dachsous-2, and protocadherin-9) were dynamic and mirrored the expression pattern of Frizzled 5/8, a non-canonical Wnt PCP pathway receptor protein essential for archenteron morphogenesis. Conclusions The echinoderm cadherin toolkit is more similar to that of an ancient bilaterian predating protostomes and deuterostomes than it is to the suite of cadherins found in extant vertebrates. However, it also appears that deuterostomes underwent several cadherin-related innovations. Based on their similar spatiotemporal expression patterns and orthologous relationships to PCP-related and tumor-suppressing proteins, we hypothesize that sea urchin cadherins may play a role in regulating the shape and growth of embryonic epithelia and organs. Future experiments will examine cadherin expression in non-echinoid echinoderms and explore the functions of cadherins during echinoderm development.https://doi.org/10.1186/s13227-023-00219-7CadherinCateninDeuterostome evolutionEchinodermProtocadherinSea urchin development |
| spellingShingle | Macie M. Chess William Douglas Josiah Saunders Charles A. Ettensohn Genome-wide identification and spatiotemporal expression analysis of cadherin superfamily members in echinoderms EvoDevo Cadherin Catenin Deuterostome evolution Echinoderm Protocadherin Sea urchin development |
| title | Genome-wide identification and spatiotemporal expression analysis of cadherin superfamily members in echinoderms |
| title_full | Genome-wide identification and spatiotemporal expression analysis of cadherin superfamily members in echinoderms |
| title_fullStr | Genome-wide identification and spatiotemporal expression analysis of cadherin superfamily members in echinoderms |
| title_full_unstemmed | Genome-wide identification and spatiotemporal expression analysis of cadherin superfamily members in echinoderms |
| title_short | Genome-wide identification and spatiotemporal expression analysis of cadherin superfamily members in echinoderms |
| title_sort | genome wide identification and spatiotemporal expression analysis of cadherin superfamily members in echinoderms |
| topic | Cadherin Catenin Deuterostome evolution Echinoderm Protocadherin Sea urchin development |
| url | https://doi.org/10.1186/s13227-023-00219-7 |
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