Egfr signaling promotes juvenile hormone biosynthesis in the German cockroach
Abstract Background In insects, an interplay between the activities of distinct hormones, such as juvenile hormone (JH) and 20-hydroxyecdysone (20E), regulates the progression through numerous life history hallmarks. As a crucial endocrine factor, JH is mainly synthesized in the corpora allata (CA)...
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| Format: | Article |
| Language: | English |
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BMC
2022-12-01
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| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-022-01484-z |
| _version_ | 1811196620757270528 |
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| author | Zhaoxin Li Caisheng Zhou Yumei Chen Wentao Ma Yunlong Cheng Jinxin Chen Yu Bai Wei Luo Na Li Erxia Du Sheng Li |
| author_facet | Zhaoxin Li Caisheng Zhou Yumei Chen Wentao Ma Yunlong Cheng Jinxin Chen Yu Bai Wei Luo Na Li Erxia Du Sheng Li |
| author_sort | Zhaoxin Li |
| collection | DOAJ |
| description | Abstract Background In insects, an interplay between the activities of distinct hormones, such as juvenile hormone (JH) and 20-hydroxyecdysone (20E), regulates the progression through numerous life history hallmarks. As a crucial endocrine factor, JH is mainly synthesized in the corpora allata (CA) to regulate multiple physiological and developmental processes, including molting, metamorphosis, and reproduction. During the last century, significant progress has been achieved in elucidating the JH signal transduction pathway, while less progress has been made in dissecting the regulatory mechanism of JH biosynthesis. Previous work has shown that receptor tyrosine kinase (RTK) signaling regulates hormone biosynthesis in both insects and mammals. Here, we performed a systematic RNA interference (RNAi) screening to identify RTKs involved in regulating JH biosynthesis in the CA of adult Blattella germanica females. Results We found that the epidermal growth factor receptor (Egfr) is required for promoting JH biosynthesis in the CA of adult females. The Egf ligands Vein and Spitz activate Egfr, followed by Ras/Raf/ERK signaling, and finally activation of the downstream transcription factor Pointed (Pnt). Importantly, Pnt induces the transcriptional expression of two key enzyme-encoding genes in the JH biosynthesis pathway: juvenile hormone acid methyltransferase (JHAMT) and methyl farnesoate epoxidase (CYP15A1). Dual-luciferase reporter assay shows that Pnt is able to activate a promoter region of Jhamt. In addition, electrophoretic mobility shift assay confirms that Pnt directly binds to the − 941~ − 886 nt region of the Jhamt promoter. Conclusions This study reveals the detailed molecular mechanism of Egfr signaling in promoting JH biosynthesis in the German cockroach, shedding light on the intricate regulation of JH biosynthesis during insect development. |
| first_indexed | 2024-04-12T01:01:57Z |
| format | Article |
| id | doaj.art-14885b3ec5ce4ce1baa966e7d419d7b2 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-12T01:01:57Z |
| publishDate | 2022-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-14885b3ec5ce4ce1baa966e7d419d7b22022-12-22T03:54:25ZengBMCBMC Biology1741-70072022-12-0120111610.1186/s12915-022-01484-zEgfr signaling promotes juvenile hormone biosynthesis in the German cockroachZhaoxin Li0Caisheng Zhou1Yumei Chen2Wentao Ma3Yunlong Cheng4Jinxin Chen5Yu Bai6Wei Luo7Na Li8Erxia Du9Sheng Li10Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityAbstract Background In insects, an interplay between the activities of distinct hormones, such as juvenile hormone (JH) and 20-hydroxyecdysone (20E), regulates the progression through numerous life history hallmarks. As a crucial endocrine factor, JH is mainly synthesized in the corpora allata (CA) to regulate multiple physiological and developmental processes, including molting, metamorphosis, and reproduction. During the last century, significant progress has been achieved in elucidating the JH signal transduction pathway, while less progress has been made in dissecting the regulatory mechanism of JH biosynthesis. Previous work has shown that receptor tyrosine kinase (RTK) signaling regulates hormone biosynthesis in both insects and mammals. Here, we performed a systematic RNA interference (RNAi) screening to identify RTKs involved in regulating JH biosynthesis in the CA of adult Blattella germanica females. Results We found that the epidermal growth factor receptor (Egfr) is required for promoting JH biosynthesis in the CA of adult females. The Egf ligands Vein and Spitz activate Egfr, followed by Ras/Raf/ERK signaling, and finally activation of the downstream transcription factor Pointed (Pnt). Importantly, Pnt induces the transcriptional expression of two key enzyme-encoding genes in the JH biosynthesis pathway: juvenile hormone acid methyltransferase (JHAMT) and methyl farnesoate epoxidase (CYP15A1). Dual-luciferase reporter assay shows that Pnt is able to activate a promoter region of Jhamt. In addition, electrophoretic mobility shift assay confirms that Pnt directly binds to the − 941~ − 886 nt region of the Jhamt promoter. Conclusions This study reveals the detailed molecular mechanism of Egfr signaling in promoting JH biosynthesis in the German cockroach, shedding light on the intricate regulation of JH biosynthesis during insect development.https://doi.org/10.1186/s12915-022-01484-zEgfr signalingPntJHJHAMTTranscriptional regulation |
| spellingShingle | Zhaoxin Li Caisheng Zhou Yumei Chen Wentao Ma Yunlong Cheng Jinxin Chen Yu Bai Wei Luo Na Li Erxia Du Sheng Li Egfr signaling promotes juvenile hormone biosynthesis in the German cockroach BMC Biology Egfr signaling Pnt JH JHAMT Transcriptional regulation |
| title | Egfr signaling promotes juvenile hormone biosynthesis in the German cockroach |
| title_full | Egfr signaling promotes juvenile hormone biosynthesis in the German cockroach |
| title_fullStr | Egfr signaling promotes juvenile hormone biosynthesis in the German cockroach |
| title_full_unstemmed | Egfr signaling promotes juvenile hormone biosynthesis in the German cockroach |
| title_short | Egfr signaling promotes juvenile hormone biosynthesis in the German cockroach |
| title_sort | egfr signaling promotes juvenile hormone biosynthesis in the german cockroach |
| topic | Egfr signaling Pnt JH JHAMT Transcriptional regulation |
| url | https://doi.org/10.1186/s12915-022-01484-z |
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