Temperature-induced embryonic diapause in chickens is mediated by PKC-NF-κB-IRF1 signaling
Abstract Background Embryonic diapause (dormancy) is a state of temporary arrest of embryonic development that is triggered by unfavorable conditions and serves as an evolutionary strategy to ensure reproductive survival. Unlike maternally-controlled embryonic diapause in mammals, chicken embryonic...
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BMC
2023-03-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-023-01550-0 |
| _version_ | 1797863566203682816 |
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| author | Junxiao Ren Zhengzheng Hu Quanlin Li Shuang Gu Fangren Lan Xiqiong Wang Jianbo Li Junying Li Liwa Shao Ning Yang Congjiao Sun |
| author_facet | Junxiao Ren Zhengzheng Hu Quanlin Li Shuang Gu Fangren Lan Xiqiong Wang Jianbo Li Junying Li Liwa Shao Ning Yang Congjiao Sun |
| author_sort | Junxiao Ren |
| collection | DOAJ |
| description | Abstract Background Embryonic diapause (dormancy) is a state of temporary arrest of embryonic development that is triggered by unfavorable conditions and serves as an evolutionary strategy to ensure reproductive survival. Unlike maternally-controlled embryonic diapause in mammals, chicken embryonic diapause is critically dependent on the environmental temperature. However, the molecular control of diapause in avian species remains largely uncharacterized. In this study, we evaluated the dynamic transcriptomic and phosphoproteomic profiles of chicken embryos in pre-diapause, diapause, and reactivated states. Results Our data demonstrated a characteristic gene expression pattern in effects on cell survival-associated and stress response signaling pathways. Unlike mammalian diapause, mTOR signaling is not responsible for chicken diapause. However, cold stress responsive genes, such as IRF1, were identified as key regulators of diapause. Further in vitro investigation showed that cold stress-induced transcription of IRF1 was dependent on the PKC-NF-κB signaling pathway, providing a mechanism for proliferation arrest during diapause. Consistently, in vivo overexpression of IRF1 in diapause embryos blocked reactivation after restoration of developmental temperatures. Conclusions We concluded that embryonic diapause in chicken is characterized by proliferation arrest, which is the same with other spices. However, chicken embryonic diapause is strictly correlated with the cold stress signal and mediated by PKC-NF-κB-IRF1 signaling, which distinguish chicken diapause from the mTOR based diapause in mammals. |
| first_indexed | 2024-04-09T22:37:35Z |
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| id | doaj.art-d67154216653473e9c1e18c8ae594ccf |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-09T22:37:35Z |
| publishDate | 2023-03-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-d67154216653473e9c1e18c8ae594ccf2023-03-22T12:23:09ZengBMCBMC Biology1741-70072023-03-0121112010.1186/s12915-023-01550-0Temperature-induced embryonic diapause in chickens is mediated by PKC-NF-κB-IRF1 signalingJunxiao Ren0Zhengzheng Hu1Quanlin Li2Shuang Gu3Fangren Lan4Xiqiong Wang5Jianbo Li6Junying Li7Liwa Shao8Ning Yang9Congjiao Sun10Department of Animal Genetics and Breeding, College of Animal Science and Technology, China Agricultural UniversityDepartment of Animal Genetics and Breeding, College of Animal Science and Technology, China Agricultural UniversityDepartment of Animal Genetics and Breeding, College of Animal Science and Technology, China Agricultural UniversityDepartment of Animal Genetics and Breeding, College of Animal Science and Technology, China Agricultural UniversityDepartment of Animal Genetics and Breeding, College of Animal Science and Technology, China Agricultural UniversityDepartment of Animal Genetics and Breeding, College of Animal Science and Technology, China Agricultural UniversityDepartment of Animal Genetics and Breeding, College of Animal Science and Technology, China Agricultural UniversityDepartment of Animal Genetics and Breeding, College of Animal Science and Technology, China Agricultural UniversityDepartment of Animal Genetics and Breeding, College of Animal Science and Technology, China Agricultural UniversityDepartment of Animal Genetics and Breeding, College of Animal Science and Technology, China Agricultural UniversityDepartment of Animal Genetics and Breeding, College of Animal Science and Technology, China Agricultural UniversityAbstract Background Embryonic diapause (dormancy) is a state of temporary arrest of embryonic development that is triggered by unfavorable conditions and serves as an evolutionary strategy to ensure reproductive survival. Unlike maternally-controlled embryonic diapause in mammals, chicken embryonic diapause is critically dependent on the environmental temperature. However, the molecular control of diapause in avian species remains largely uncharacterized. In this study, we evaluated the dynamic transcriptomic and phosphoproteomic profiles of chicken embryos in pre-diapause, diapause, and reactivated states. Results Our data demonstrated a characteristic gene expression pattern in effects on cell survival-associated and stress response signaling pathways. Unlike mammalian diapause, mTOR signaling is not responsible for chicken diapause. However, cold stress responsive genes, such as IRF1, were identified as key regulators of diapause. Further in vitro investigation showed that cold stress-induced transcription of IRF1 was dependent on the PKC-NF-κB signaling pathway, providing a mechanism for proliferation arrest during diapause. Consistently, in vivo overexpression of IRF1 in diapause embryos blocked reactivation after restoration of developmental temperatures. Conclusions We concluded that embryonic diapause in chicken is characterized by proliferation arrest, which is the same with other spices. However, chicken embryonic diapause is strictly correlated with the cold stress signal and mediated by PKC-NF-κB-IRF1 signaling, which distinguish chicken diapause from the mTOR based diapause in mammals.https://doi.org/10.1186/s12915-023-01550-0DiapauseEmbryoCell proliferationCold stressPKC-NF-κB signaling |
| spellingShingle | Junxiao Ren Zhengzheng Hu Quanlin Li Shuang Gu Fangren Lan Xiqiong Wang Jianbo Li Junying Li Liwa Shao Ning Yang Congjiao Sun Temperature-induced embryonic diapause in chickens is mediated by PKC-NF-κB-IRF1 signaling BMC Biology Diapause Embryo Cell proliferation Cold stress PKC-NF-κB signaling |
| title | Temperature-induced embryonic diapause in chickens is mediated by PKC-NF-κB-IRF1 signaling |
| title_full | Temperature-induced embryonic diapause in chickens is mediated by PKC-NF-κB-IRF1 signaling |
| title_fullStr | Temperature-induced embryonic diapause in chickens is mediated by PKC-NF-κB-IRF1 signaling |
| title_full_unstemmed | Temperature-induced embryonic diapause in chickens is mediated by PKC-NF-κB-IRF1 signaling |
| title_short | Temperature-induced embryonic diapause in chickens is mediated by PKC-NF-κB-IRF1 signaling |
| title_sort | temperature induced embryonic diapause in chickens is mediated by pkc nf κb irf1 signaling |
| topic | Diapause Embryo Cell proliferation Cold stress PKC-NF-κB signaling |
| url | https://doi.org/10.1186/s12915-023-01550-0 |
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