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Egfr signaling promotes juvenile hormone biosynthesis in the German cockroach

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 regul...

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Autores principales: Li, Zhaoxin, Zhou, Caisheng, Chen, Yumei, Ma, Wentao, Cheng, Yunlong, Chen, Jinxin, Bai, Yu, Luo, Wei, Li, Na, Du, Erxia, Li, Sheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9749228/
https://www.ncbi.nlm.nih.gov/pubmed/36514097
http://dx.doi.org/10.1186/s12915-022-01484-z
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author Li, Zhaoxin
Zhou, Caisheng
Chen, Yumei
Ma, Wentao
Cheng, Yunlong
Chen, Jinxin
Bai, Yu
Luo, Wei
Li, Na
Du, Erxia
Li, Sheng
author_facet Li, Zhaoxin
Zhou, Caisheng
Chen, Yumei
Ma, Wentao
Cheng, Yunlong
Chen, Jinxin
Bai, Yu
Luo, Wei
Li, Na
Du, Erxia
Li, Sheng
author_sort Li, Zhaoxin
collection PubMed
description 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01484-z.
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spelling pubmed-97492282022-12-15 Egfr signaling promotes juvenile hormone biosynthesis in the German cockroach Li, Zhaoxin Zhou, Caisheng Chen, Yumei Ma, Wentao Cheng, Yunlong Chen, Jinxin Bai, Yu Luo, Wei Li, Na Du, Erxia Li, Sheng BMC Biol Research Article 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01484-z. BioMed Central 2022-12-13 /pmc/articles/PMC9749228/ /pubmed/36514097 http://dx.doi.org/10.1186/s12915-022-01484-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Li, Zhaoxin
Zhou, Caisheng
Chen, Yumei
Ma, Wentao
Cheng, Yunlong
Chen, Jinxin
Bai, Yu
Luo, Wei
Li, Na
Du, Erxia
Li, Sheng
Egfr signaling promotes juvenile hormone biosynthesis in the German cockroach
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 Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9749228/
https://www.ncbi.nlm.nih.gov/pubmed/36514097
http://dx.doi.org/10.1186/s12915-022-01484-z
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