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Dynamics expression of DmFKBP12/Calstabin during embryonic early development of Drosophila melanogaster

BACKGROUND: Calcium signaling are conserved from invertebrates to vertebrates and plays critical roles in many molecular mechanisms of embryogenesis and postnatal development. As a critical component of the signaling pathway, the RyR medicated calcium-induced calcium release signaling system, has be...

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Autores principales: Feng, Rui, Zhou, Xin, Zhang, Wei, Pu, Tao, Sun, Yuting, Yang, Rong, Wang, Dan, Zhang, Xiaofei, Gao, Yingfeng, Cai, Zhenlu, Liang, Yu, Yu, Qiuxia, Wu, Yajun, Lei, Xinjuan, Liang, Zhijia, Jones, Odell, Wang, Liyang, Xu, Mengmeng, Sun, Yanping, Isaacs, William B., Ma, Jianjie, Xu, Xuehong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6325743/
https://www.ncbi.nlm.nih.gov/pubmed/30637096
http://dx.doi.org/10.1186/s13578-019-0270-6
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author Feng, Rui
Zhou, Xin
Zhang, Wei
Pu, Tao
Sun, Yuting
Yang, Rong
Wang, Dan
Zhang, Xiaofei
Gao, Yingfeng
Cai, Zhenlu
Liang, Yu
Yu, Qiuxia
Wu, Yajun
Lei, Xinjuan
Liang, Zhijia
Jones, Odell
Wang, Liyang
Xu, Mengmeng
Sun, Yanping
Isaacs, William B.
Ma, Jianjie
Xu, Xuehong
author_facet Feng, Rui
Zhou, Xin
Zhang, Wei
Pu, Tao
Sun, Yuting
Yang, Rong
Wang, Dan
Zhang, Xiaofei
Gao, Yingfeng
Cai, Zhenlu
Liang, Yu
Yu, Qiuxia
Wu, Yajun
Lei, Xinjuan
Liang, Zhijia
Jones, Odell
Wang, Liyang
Xu, Mengmeng
Sun, Yanping
Isaacs, William B.
Ma, Jianjie
Xu, Xuehong
author_sort Feng, Rui
collection PubMed
description BACKGROUND: Calcium signaling are conserved from invertebrates to vertebrates and plays critical roles in many molecular mechanisms of embryogenesis and postnatal development. As a critical component of the signaling pathway, the RyR medicated calcium-induced calcium release signaling system, has been well studied along with their regulator FK506-binding protein 12 (FKBP12/Calstabin). Lack of FKBP12 is known to result in lethal cardiac dysfunction in mouse. However, precisely how FKBP12 is regulated and effects calcium signaling in Drosophila melanogaster remains largely unknown. RESULTS: In this study, we identified both temporal and localization changes in expression of DmFKBP12, a translational and transcriptional regulator of Drosophila RyR (DmRyR) and FKBP12, through embryonic development. DmFKBP12 is first expressed at the syncytial blastoderm stage and undergoes increased expression during the cellular blastoderm and early gastrulation stages. At late gastrulation, DmFKBP12 expression begins to decline until it reaches homeostasis, which it then maintains throughout the rest of development. Throughout these described changes in expression, DmFKBP12 mRNA remain stable, which indicates that protein dynamics are attributed to regulation at the mRNA to protein translation level. In addition to temporal changes in expression, dynamic expression profiles during Drosophila development also revealed DmFKBP12 localization. Although DmFKBP12 is distributed evenly between the anterior to posterior poles of the blastoderm egg, the protein is expressed more strongly in the cortex of the early Drosophila gastrula with the highest concentration found in the basement membrane of the cellular blastoderm. Fertilized egg, through the profile as under-membrane cortex distribution concentering onto basement at cellular blastoderm, to the profile as three-gem layer localization in primitive neuronal and digestion architecture of early Drosophila gastrula. By late gastrulation, DmFKBP12 is no longer identified in the yolk or lumen of duct structures and has relocated to the future brain (suboesophageal and supraesophageal ganglions), ventral nervous system, and muscular system. Throughout these changes in distribution, in situ DmFKBP12 mRNA monitoring detected equal distribution of DmFKBP12 mRNA, once again indicating that regulation of DmFKBP12 occurs at the translational level in Drosophila development. CONCLUSION: As a critical regulator of the DmRyR-FKBP complex, DmFKBP12 expression in Drosophila fluctuates temporally and geographically with the formation of organ systems. These finding indicate that DmFKBP12 and RyR associated calcium signaling plays an essential role in the successful development of Drosophila melanogaster. Further study on the differences between mammalian RyR-FKBP12 and Drosophila DmRyR-FKBP12 can be exploited to develop safe pesticides. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13578-019-0270-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-63257432019-01-11 Dynamics expression of DmFKBP12/Calstabin during embryonic early development of Drosophila melanogaster Feng, Rui Zhou, Xin Zhang, Wei Pu, Tao Sun, Yuting Yang, Rong Wang, Dan Zhang, Xiaofei Gao, Yingfeng Cai, Zhenlu Liang, Yu Yu, Qiuxia Wu, Yajun Lei, Xinjuan Liang, Zhijia Jones, Odell Wang, Liyang Xu, Mengmeng Sun, Yanping Isaacs, William B. Ma, Jianjie Xu, Xuehong Cell Biosci Research BACKGROUND: Calcium signaling are conserved from invertebrates to vertebrates and plays critical roles in many molecular mechanisms of embryogenesis and postnatal development. As a critical component of the signaling pathway, the RyR medicated calcium-induced calcium release signaling system, has been well studied along with their regulator FK506-binding protein 12 (FKBP12/Calstabin). Lack of FKBP12 is known to result in lethal cardiac dysfunction in mouse. However, precisely how FKBP12 is regulated and effects calcium signaling in Drosophila melanogaster remains largely unknown. RESULTS: In this study, we identified both temporal and localization changes in expression of DmFKBP12, a translational and transcriptional regulator of Drosophila RyR (DmRyR) and FKBP12, through embryonic development. DmFKBP12 is first expressed at the syncytial blastoderm stage and undergoes increased expression during the cellular blastoderm and early gastrulation stages. At late gastrulation, DmFKBP12 expression begins to decline until it reaches homeostasis, which it then maintains throughout the rest of development. Throughout these described changes in expression, DmFKBP12 mRNA remain stable, which indicates that protein dynamics are attributed to regulation at the mRNA to protein translation level. In addition to temporal changes in expression, dynamic expression profiles during Drosophila development also revealed DmFKBP12 localization. Although DmFKBP12 is distributed evenly between the anterior to posterior poles of the blastoderm egg, the protein is expressed more strongly in the cortex of the early Drosophila gastrula with the highest concentration found in the basement membrane of the cellular blastoderm. Fertilized egg, through the profile as under-membrane cortex distribution concentering onto basement at cellular blastoderm, to the profile as three-gem layer localization in primitive neuronal and digestion architecture of early Drosophila gastrula. By late gastrulation, DmFKBP12 is no longer identified in the yolk or lumen of duct structures and has relocated to the future brain (suboesophageal and supraesophageal ganglions), ventral nervous system, and muscular system. Throughout these changes in distribution, in situ DmFKBP12 mRNA monitoring detected equal distribution of DmFKBP12 mRNA, once again indicating that regulation of DmFKBP12 occurs at the translational level in Drosophila development. CONCLUSION: As a critical regulator of the DmRyR-FKBP complex, DmFKBP12 expression in Drosophila fluctuates temporally and geographically with the formation of organ systems. These finding indicate that DmFKBP12 and RyR associated calcium signaling plays an essential role in the successful development of Drosophila melanogaster. Further study on the differences between mammalian RyR-FKBP12 and Drosophila DmRyR-FKBP12 can be exploited to develop safe pesticides. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13578-019-0270-6) contains supplementary material, which is available to authorized users. BioMed Central 2019-01-08 /pmc/articles/PMC6325743/ /pubmed/30637096 http://dx.doi.org/10.1186/s13578-019-0270-6 Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Feng, Rui
Zhou, Xin
Zhang, Wei
Pu, Tao
Sun, Yuting
Yang, Rong
Wang, Dan
Zhang, Xiaofei
Gao, Yingfeng
Cai, Zhenlu
Liang, Yu
Yu, Qiuxia
Wu, Yajun
Lei, Xinjuan
Liang, Zhijia
Jones, Odell
Wang, Liyang
Xu, Mengmeng
Sun, Yanping
Isaacs, William B.
Ma, Jianjie
Xu, Xuehong
Dynamics expression of DmFKBP12/Calstabin during embryonic early development of Drosophila melanogaster
title Dynamics expression of DmFKBP12/Calstabin during embryonic early development of Drosophila melanogaster
title_full Dynamics expression of DmFKBP12/Calstabin during embryonic early development of Drosophila melanogaster
title_fullStr Dynamics expression of DmFKBP12/Calstabin during embryonic early development of Drosophila melanogaster
title_full_unstemmed Dynamics expression of DmFKBP12/Calstabin during embryonic early development of Drosophila melanogaster
title_short Dynamics expression of DmFKBP12/Calstabin during embryonic early development of Drosophila melanogaster
title_sort dynamics expression of dmfkbp12/calstabin during embryonic early development of drosophila melanogaster
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6325743/
https://www.ncbi.nlm.nih.gov/pubmed/30637096
http://dx.doi.org/10.1186/s13578-019-0270-6
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