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)...
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| Published in | Frontiers in physiology Vol. 11; p. 485 |
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| Main Authors | , , , , , , , , , , , |
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| Abstract | 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.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. |
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| AbstractList | 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. 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. 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.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. |
| Author | Zhang, Xin Wu, Xiaofen Jiang, Xiao Ruan, Yao Ren, Chunhua Wong, Nai-Kei Wu, Xugan Luo, Peng Hu, Chaoqun Zhu, Chunhua Chen, Ting Ji, Jiatai |
| AuthorAffiliation | 7 Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture, Shanghai Ocean University , Shanghai , China 4 College of Fisheries, Guangdong Ocean University , Zhanjiang , China 6 Guangdong Haimao Investment Co., Ltd. , Zhanjiang , China 5 Institution of South China Sea Ecology and Environmental Engineering (ISEE), Chinese Academy of Sciences , Guangzhou , China 1 CAS Key Laboratory of Tropical Marine Bio-resources and Ecology (LMB), Guangdong Provincial Key Laboratory of Applied Marine Biology (LAMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences , Guangzhou , China 2 University of Chinese Academy of Sciences , Beijing , China 3 National Clinical Research Center for Infectious Diseases, Shenzhen Third People’s Hospital, The Second Hospital Affiliated to Southern University of Science and Technology , Shenzhen , China |
| AuthorAffiliation_xml | – name: 3 National Clinical Research Center for Infectious Diseases, Shenzhen Third People’s Hospital, The Second Hospital Affiliated to Southern University of Science and Technology , Shenzhen , China – name: 2 University of Chinese Academy of Sciences , Beijing , China – name: 6 Guangdong Haimao Investment Co., Ltd. , Zhanjiang , China – name: 1 CAS Key Laboratory of Tropical Marine Bio-resources and Ecology (LMB), Guangdong Provincial Key Laboratory of Applied Marine Biology (LAMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences , Guangzhou , China – name: 4 College of Fisheries, Guangdong Ocean University , Zhanjiang , China – name: 7 Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture, Shanghai Ocean University , Shanghai , China – name: 5 Institution of South China Sea Ecology and Environmental Engineering (ISEE), Chinese Academy of Sciences , Guangzhou , China |
| Author_xml | – sequence: 1 givenname: Yao surname: Ruan fullname: Ruan, Yao – sequence: 2 givenname: Nai-Kei surname: Wong fullname: Wong, Nai-Kei – sequence: 3 givenname: Xin surname: Zhang fullname: Zhang, Xin – sequence: 4 givenname: Chunhua surname: Zhu fullname: Zhu, Chunhua – sequence: 5 givenname: Xiaofen surname: Wu fullname: Wu, Xiaofen – sequence: 6 givenname: Chunhua surname: Ren fullname: Ren, Chunhua – sequence: 7 givenname: Peng surname: Luo fullname: Luo, Peng – sequence: 8 givenname: Xiao surname: Jiang fullname: Jiang, Xiao – sequence: 9 givenname: Jiatai surname: Ji fullname: Ji, Jiatai – sequence: 10 givenname: Xugan surname: Wu fullname: Wu, Xugan – sequence: 11 givenname: Chaoqun surname: Hu fullname: Hu, Chaoqun – sequence: 12 givenname: Ting surname: Chen fullname: Chen, Ting |
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| Copyright | Copyright © 2020 Ruan, Wong, Zhang, Zhu, Wu, Ren, Luo, Jiang, Ji, Wu, Hu and Chen. Copyright © 2020 Ruan, Wong, Zhang, Zhu, Wu, Ren, Luo, Jiang, Ji, Wu, Hu and Chen. 2020 Ruan, Wong, Zhang, Zhu, Wu, Ren, Luo, Jiang, Ji, Wu, Hu and Chen |
| Copyright_xml | – notice: Copyright © 2020 Ruan, Wong, Zhang, Zhu, Wu, Ren, Luo, Jiang, Ji, Wu, Hu and Chen. – notice: Copyright © 2020 Ruan, Wong, Zhang, Zhu, Wu, Ren, Luo, Jiang, Ji, Wu, Hu and Chen. 2020 Ruan, Wong, Zhang, Zhu, Wu, Ren, Luo, Jiang, Ji, Wu, Hu and Chen |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 This article was submitted to Aquatic Physiology, a section of the journal Frontiers in Physiology These authors have contributed equally to this work Edited by: Silvia Franzellitti, University of Bologna, Italy Reviewed by: Simon G. Webster, Bangor University, United Kingdom; Alejandro S. Mechaly, CONICET Instituto de Investigaciones en Biodiversidad y Biotecnología (INBIOTEC), Argentina |
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| Title | Vitellogenin Receptor (VgR) Mediates Oocyte Maturation and Ovarian Development in the Pacific White Shrimp (Litopenaeus vannamei) |
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