Wnt Signaling Pathway Linked to Intestinal Regeneration via Evolutionary Patterns and Gene Expression in the Sea Cucumber Apostichopus japonicus
Many echinoderms are regenerative species that exhibit exceptional regenerative capacity, and sea cucumber is a representative organism that could regenerate the whole intestine after evisceration. There are many signaling pathways participate in the regeneration process, but it is not clear which i...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-02-01
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| Series: | Frontiers in Genetics |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fgene.2019.00112/full |
| _version_ | 1818418985785360384 |
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| author | Jianbo Yuan Jianbo Yuan Jianbo Yuan Yi Gao Yi Gao Yi Gao Lina Sun Lina Sun Lina Sun Songjun Jin Songjun Jin Songjun Jin Xiaojun Zhang Xiaojun Zhang Xiaojun Zhang Chengzhang Liu Chengzhang Liu Chengzhang Liu Fuhua Li Fuhua Li Fuhua Li Jianhai Xiang Jianhai Xiang Jianhai Xiang |
| author_facet | Jianbo Yuan Jianbo Yuan Jianbo Yuan Yi Gao Yi Gao Yi Gao Lina Sun Lina Sun Lina Sun Songjun Jin Songjun Jin Songjun Jin Xiaojun Zhang Xiaojun Zhang Xiaojun Zhang Chengzhang Liu Chengzhang Liu Chengzhang Liu Fuhua Li Fuhua Li Fuhua Li Jianhai Xiang Jianhai Xiang Jianhai Xiang |
| author_sort | Jianbo Yuan |
| collection | DOAJ |
| description | Many echinoderms are regenerative species that exhibit exceptional regenerative capacity, and sea cucumber is a representative organism that could regenerate the whole intestine after evisceration. There are many signaling pathways participate in the regeneration process, but it is not clear which is essential for the intestinal regeneration. In this study, we performed genome-wide comprehensive analyses on these regeneration-related signaling pathways, and found the Wnt signaling pathway was one of the most conservative pathways among regenerative species. Additionally, among these signaling pathways, we found that the Wnt signaling pathway was the only one under positive selection in regenerative echinoderms, and the only one enriched by differentially expressed genes during the intestinal regeneration. Thus, it suggests both coding sequence and gene expression of the Wnt signaling pathway have been shaped by natural selection to provide the genetic architecture for intestinal regeneration. Wnt7, Fz7, and Dvl are the three positively selected genes and also happen to be three upstream genes in the Wnt signaling pathway. They are all significantly upregulated at the early stages of regeneration, which may contribute significantly to the early activation of Wnt signaling and the initiation of intestinal regeneration. Expression knockdown of Wnt7 and Dvl by RNA interference significantly inhibit intestinal extension, implying that they are essential for intestinal regeneration. As an important regeneration-related gene, the downstream gene c-Myc is also conserved and highly expressed during the whole regeneration stages, which may make the Wnt/c-Myc signaling to be an important way to promote intestinal regeneration. Therefore, it is reasonable to conclude that the Wnt signaling pathway is the chosen one to play an important role in intestinal regeneration of sea cucumbers, or even in the regeneration of other echinoderms. |
| first_indexed | 2024-12-14T12:31:23Z |
| format | Article |
| id | doaj.art-fc11e3cc87874558a917bcd28fdecf12 |
| institution | Directory Open Access Journal |
| issn | 1664-8021 |
| language | English |
| last_indexed | 2024-12-14T12:31:23Z |
| publishDate | 2019-02-01 |
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| series | Frontiers in Genetics |
| spelling | doaj.art-fc11e3cc87874558a917bcd28fdecf122022-12-21T23:01:11ZengFrontiers Media S.A.Frontiers in Genetics1664-80212019-02-011010.3389/fgene.2019.00112396513Wnt Signaling Pathway Linked to Intestinal Regeneration via Evolutionary Patterns and Gene Expression in the Sea Cucumber Apostichopus japonicusJianbo Yuan0Jianbo Yuan1Jianbo Yuan2Yi Gao3Yi Gao4Yi Gao5Lina Sun6Lina Sun7Lina Sun8Songjun Jin9Songjun Jin10Songjun Jin11Xiaojun Zhang12Xiaojun Zhang13Xiaojun Zhang14Chengzhang Liu15Chengzhang Liu16Chengzhang Liu17Fuhua Li18Fuhua Li19Fuhua Li20Jianhai Xiang21Jianhai Xiang22Jianhai Xiang23CAS Key Laboratory of Experimental Marine Biology and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology and Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaCenter for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaCAS Key Laboratory of Experimental Marine Biology and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology and Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaCenter for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaCAS Key Laboratory of Experimental Marine Biology and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology and Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaCenter for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaCAS Key Laboratory of Experimental Marine Biology and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology and Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaCenter for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaCAS Key Laboratory of Experimental Marine Biology and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology and Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaCenter for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaCAS Key Laboratory of Experimental Marine Biology and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology and Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaCenter for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaCAS Key Laboratory of Experimental Marine Biology and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology and Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaCenter for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaCAS Key Laboratory of Experimental Marine Biology and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology and Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaCenter for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaMany echinoderms are regenerative species that exhibit exceptional regenerative capacity, and sea cucumber is a representative organism that could regenerate the whole intestine after evisceration. There are many signaling pathways participate in the regeneration process, but it is not clear which is essential for the intestinal regeneration. In this study, we performed genome-wide comprehensive analyses on these regeneration-related signaling pathways, and found the Wnt signaling pathway was one of the most conservative pathways among regenerative species. Additionally, among these signaling pathways, we found that the Wnt signaling pathway was the only one under positive selection in regenerative echinoderms, and the only one enriched by differentially expressed genes during the intestinal regeneration. Thus, it suggests both coding sequence and gene expression of the Wnt signaling pathway have been shaped by natural selection to provide the genetic architecture for intestinal regeneration. Wnt7, Fz7, and Dvl are the three positively selected genes and also happen to be three upstream genes in the Wnt signaling pathway. They are all significantly upregulated at the early stages of regeneration, which may contribute significantly to the early activation of Wnt signaling and the initiation of intestinal regeneration. Expression knockdown of Wnt7 and Dvl by RNA interference significantly inhibit intestinal extension, implying that they are essential for intestinal regeneration. As an important regeneration-related gene, the downstream gene c-Myc is also conserved and highly expressed during the whole regeneration stages, which may make the Wnt/c-Myc signaling to be an important way to promote intestinal regeneration. Therefore, it is reasonable to conclude that the Wnt signaling pathway is the chosen one to play an important role in intestinal regeneration of sea cucumbers, or even in the regeneration of other echinoderms.https://www.frontiersin.org/article/10.3389/fgene.2019.00112/fullsea cucumberintestinal regenerationWnt signaling pathwaypositive selectionnatural selection |
| spellingShingle | Jianbo Yuan Jianbo Yuan Jianbo Yuan Yi Gao Yi Gao Yi Gao Lina Sun Lina Sun Lina Sun Songjun Jin Songjun Jin Songjun Jin Xiaojun Zhang Xiaojun Zhang Xiaojun Zhang Chengzhang Liu Chengzhang Liu Chengzhang Liu Fuhua Li Fuhua Li Fuhua Li Jianhai Xiang Jianhai Xiang Jianhai Xiang Wnt Signaling Pathway Linked to Intestinal Regeneration via Evolutionary Patterns and Gene Expression in the Sea Cucumber Apostichopus japonicus Frontiers in Genetics sea cucumber intestinal regeneration Wnt signaling pathway positive selection natural selection |
| title | Wnt Signaling Pathway Linked to Intestinal Regeneration via Evolutionary Patterns and Gene Expression in the Sea Cucumber Apostichopus japonicus |
| title_full | Wnt Signaling Pathway Linked to Intestinal Regeneration via Evolutionary Patterns and Gene Expression in the Sea Cucumber Apostichopus japonicus |
| title_fullStr | Wnt Signaling Pathway Linked to Intestinal Regeneration via Evolutionary Patterns and Gene Expression in the Sea Cucumber Apostichopus japonicus |
| title_full_unstemmed | Wnt Signaling Pathway Linked to Intestinal Regeneration via Evolutionary Patterns and Gene Expression in the Sea Cucumber Apostichopus japonicus |
| title_short | Wnt Signaling Pathway Linked to Intestinal Regeneration via Evolutionary Patterns and Gene Expression in the Sea Cucumber Apostichopus japonicus |
| title_sort | wnt signaling pathway linked to intestinal regeneration via evolutionary patterns and gene expression in the sea cucumber apostichopus japonicus |
| topic | sea cucumber intestinal regeneration Wnt signaling pathway positive selection natural selection |
| url | https://www.frontiersin.org/article/10.3389/fgene.2019.00112/full |
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