Cargando…

Vitellogenin Receptor (VgR) Mediates Oocyte Maturation and Ovarian Development in the Pacific White Shrimp (Litopenaeus vannamei)

Oocyte maturation and ovarian development are sequentially coordinated events critical to reproduction. In the ovaries of adult oviparous animals such as birds, bony fish, insects, and crustaceans, vitellogenin receptor (VgR) is a plasma membrane receptor that specifically mediates vitellogenin (Vg)...

Descripción completa

Detalles Bibliográficos
Autores principales: Ruan, Yao, Wong, Nai-Kei, Zhang, Xin, Zhu, Chunhua, Wu, Xiaofen, Ren, Chunhua, Luo, Peng, Jiang, Xiao, Ji, Jiatai, Wu, Xugan, Hu, Chaoqun, Chen, Ting
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7243368/
https://www.ncbi.nlm.nih.gov/pubmed/32499719
http://dx.doi.org/10.3389/fphys.2020.00485
_version_ 1783537416609464320
author Ruan, Yao
Wong, Nai-Kei
Zhang, Xin
Zhu, Chunhua
Wu, Xiaofen
Ren, Chunhua
Luo, Peng
Jiang, Xiao
Ji, Jiatai
Wu, Xugan
Hu, Chaoqun
Chen, Ting
author_facet Ruan, Yao
Wong, Nai-Kei
Zhang, Xin
Zhu, Chunhua
Wu, Xiaofen
Ren, Chunhua
Luo, Peng
Jiang, Xiao
Ji, Jiatai
Wu, Xugan
Hu, Chaoqun
Chen, Ting
author_sort Ruan, Yao
collection PubMed
description Oocyte maturation and ovarian development are sequentially coordinated events critical to reproduction. In the ovaries of adult oviparous animals such as birds, bony fish, insects, and crustaceans, vitellogenin receptor (VgR) is a plasma membrane receptor that specifically mediates vitellogenin (Vg) transport into oocytes. Accumulation of Vg drives sexual maturation of the female crustaceans by acting as a pivotal regulator of nutritional accumulation within oocytes, a process known as vitellogenesis. However, the mechanisms by which VgR mediates vitellogenesis are still not fully understood. In this study, we first identified a unique VgR (Lv-VgR) and characterized its genomic organization and protein structural domains in Litopenaeus vannamei, a predominant cultured shrimp species worldwide. This newly identified Lv-VgR phylogenetically forms a group with VgRs from other crustacean species within the arthropod cluster. Duplicated LBD/EGFD regions are found exclusively among arthropod VgRs but not in paralogs from vertebrates and nematodes. In terms of expression patterns, Lv-VgR transcripts are specifically expressed in ovaries of female shrimps, which increases progressively during ovarian development, and rapidly declines toward embryonic development. The cellular and subcellular locations were For analyzed by in situ hybridization and immunofluorescence, respectively. The Lv-VgR mRNA was found to be expressed in the oocytes of ovaries, and Lv-VgR protein was found to localize in the cell membrane of maturing oocytes while accumulation of the ligand Vg protein assumed an even cytoplasmic distribution. Silencing of VgR transcript expression by RNAi was effective for stunting ovarian development. This present study has thus provided new insights into the regulatory roles of VgR in crustacean ovarian development.
format Online
Article
Text
id pubmed-7243368
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-72433682020-06-03 Vitellogenin Receptor (VgR) Mediates Oocyte Maturation and Ovarian Development in the Pacific White Shrimp (Litopenaeus vannamei) Ruan, Yao Wong, Nai-Kei Zhang, Xin Zhu, Chunhua Wu, Xiaofen Ren, Chunhua Luo, Peng Jiang, Xiao Ji, Jiatai Wu, Xugan Hu, Chaoqun Chen, Ting Front Physiol Physiology Oocyte maturation and ovarian development are sequentially coordinated events critical to reproduction. In the ovaries of adult oviparous animals such as birds, bony fish, insects, and crustaceans, vitellogenin receptor (VgR) is a plasma membrane receptor that specifically mediates vitellogenin (Vg) transport into oocytes. Accumulation of Vg drives sexual maturation of the female crustaceans by acting as a pivotal regulator of nutritional accumulation within oocytes, a process known as vitellogenesis. However, the mechanisms by which VgR mediates vitellogenesis are still not fully understood. In this study, we first identified a unique VgR (Lv-VgR) and characterized its genomic organization and protein structural domains in Litopenaeus vannamei, a predominant cultured shrimp species worldwide. This newly identified Lv-VgR phylogenetically forms a group with VgRs from other crustacean species within the arthropod cluster. Duplicated LBD/EGFD regions are found exclusively among arthropod VgRs but not in paralogs from vertebrates and nematodes. In terms of expression patterns, Lv-VgR transcripts are specifically expressed in ovaries of female shrimps, which increases progressively during ovarian development, and rapidly declines toward embryonic development. The cellular and subcellular locations were For analyzed by in situ hybridization and immunofluorescence, respectively. The Lv-VgR mRNA was found to be expressed in the oocytes of ovaries, and Lv-VgR protein was found to localize in the cell membrane of maturing oocytes while accumulation of the ligand Vg protein assumed an even cytoplasmic distribution. Silencing of VgR transcript expression by RNAi was effective for stunting ovarian development. This present study has thus provided new insights into the regulatory roles of VgR in crustacean ovarian development. Frontiers Media S.A. 2020-05-15 /pmc/articles/PMC7243368/ /pubmed/32499719 http://dx.doi.org/10.3389/fphys.2020.00485 Text en Copyright © 2020 Ruan, Wong, Zhang, Zhu, Wu, Ren, Luo, Jiang, Ji, Wu, Hu and Chen. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Ruan, Yao
Wong, Nai-Kei
Zhang, Xin
Zhu, Chunhua
Wu, Xiaofen
Ren, Chunhua
Luo, Peng
Jiang, Xiao
Ji, Jiatai
Wu, Xugan
Hu, Chaoqun
Chen, Ting
Vitellogenin Receptor (VgR) Mediates Oocyte Maturation and Ovarian Development in the Pacific White Shrimp (Litopenaeus vannamei)
title Vitellogenin Receptor (VgR) Mediates Oocyte Maturation and Ovarian Development in the Pacific White Shrimp (Litopenaeus vannamei)
title_full Vitellogenin Receptor (VgR) Mediates Oocyte Maturation and Ovarian Development in the Pacific White Shrimp (Litopenaeus vannamei)
title_fullStr Vitellogenin Receptor (VgR) Mediates Oocyte Maturation and Ovarian Development in the Pacific White Shrimp (Litopenaeus vannamei)
title_full_unstemmed Vitellogenin Receptor (VgR) Mediates Oocyte Maturation and Ovarian Development in the Pacific White Shrimp (Litopenaeus vannamei)
title_short Vitellogenin Receptor (VgR) Mediates Oocyte Maturation and Ovarian Development in the Pacific White Shrimp (Litopenaeus vannamei)
title_sort vitellogenin receptor (vgr) mediates oocyte maturation and ovarian development in the pacific white shrimp (litopenaeus vannamei)
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7243368/
https://www.ncbi.nlm.nih.gov/pubmed/32499719
http://dx.doi.org/10.3389/fphys.2020.00485
work_keys_str_mv AT ruanyao vitellogeninreceptorvgrmediatesoocytematurationandovariandevelopmentinthepacificwhiteshrimplitopenaeusvannamei
AT wongnaikei vitellogeninreceptorvgrmediatesoocytematurationandovariandevelopmentinthepacificwhiteshrimplitopenaeusvannamei
AT zhangxin vitellogeninreceptorvgrmediatesoocytematurationandovariandevelopmentinthepacificwhiteshrimplitopenaeusvannamei
AT zhuchunhua vitellogeninreceptorvgrmediatesoocytematurationandovariandevelopmentinthepacificwhiteshrimplitopenaeusvannamei
AT wuxiaofen vitellogeninreceptorvgrmediatesoocytematurationandovariandevelopmentinthepacificwhiteshrimplitopenaeusvannamei
AT renchunhua vitellogeninreceptorvgrmediatesoocytematurationandovariandevelopmentinthepacificwhiteshrimplitopenaeusvannamei
AT luopeng vitellogeninreceptorvgrmediatesoocytematurationandovariandevelopmentinthepacificwhiteshrimplitopenaeusvannamei
AT jiangxiao vitellogeninreceptorvgrmediatesoocytematurationandovariandevelopmentinthepacificwhiteshrimplitopenaeusvannamei
AT jijiatai vitellogeninreceptorvgrmediatesoocytematurationandovariandevelopmentinthepacificwhiteshrimplitopenaeusvannamei
AT wuxugan vitellogeninreceptorvgrmediatesoocytematurationandovariandevelopmentinthepacificwhiteshrimplitopenaeusvannamei
AT huchaoqun vitellogeninreceptorvgrmediatesoocytematurationandovariandevelopmentinthepacificwhiteshrimplitopenaeusvannamei
AT chenting vitellogeninreceptorvgrmediatesoocytematurationandovariandevelopmentinthepacificwhiteshrimplitopenaeusvannamei