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      Molecular Features and Expression Patterns of Vitellogenin Receptor in Calliptamus italicus (Orthoptera: Acrididae)

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          Abstract

          Vitellogenin receptor (VgR) mediates the intake of vitellin via oocytes, thus exerting an important role in vitellogenesis. In this study, reverse transcription-polymerase chain reaction (RT-PCR) and rapid-amplification of cDNA ends techniques were adopted to clone the CiVgR gene, namely the VgR gene of Calliptamus italicus, i.e., Orthopteran. The full length of CiVgR was 5,589 bp, and the open reading frame was estimated to be 5,265 bp, which encoded 1,754 amino acids (aa). Sequence alignment analysis showed that CiVgR belonged to the superfamily of low-density lipoprotein receptor genes, which contained several conserved domains, including ligand-binding domains, epidermal growth factor precursor homology domains, transmembrane domains, and cytoplasmic domains. However, no O-linked sugar domain was identified. Phylogenetic analysis showed that CiVgR had the closest genetic relationship to Blattarias. RT-PCR showed that CiVgR was only specifically expressed in the ovarian tissue of females. quantitative real time polymerase chain reaction showed that the transcription of CiVgR already appeared in the fourth-instar nymph of C. italicus, which gradually increased after adult emergence, peaked at the previtellogenesis stage, and then started to decrease. The expression pattern of CiVgR was closely associated with vitellogenesis. The findings of this study further our understanding of the molecular mechanisms involved in the reproduction of C. italicus, and provide new ideas to control this insect.

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          Regulatory Pathways Controlling Female Insect Reproduction

          The synthesis of vitellogenin and its uptake by maturing oocytes during egg maturation are essential for successful female reproduction. These events are regulated by the juvenile hormones and ecdysteroids and by the nutritional signaling pathway regulated by neuropeptides. Juvenile hormones act as gonadotropins, regulating vitellogenesis in most insects, but ecdysteroids control this process in Diptera and some Hymenoptera and Lepidoptera. The complex crosstalk between the juvenile hormones, ecdysteroids, and nutritional signaling pathways differs distinctly depending on the reproductive strategies adopted by various insects. Molecular studies within the past decade have revealed much about the relationships among, and the role of, these pathways with respect to regulation of insect reproduction. Here, we review the role of juvenile hormones, ecdysteroids, and nutritional signaling, along with that of microRNAs, in regulating female insect reproduction at the molecular level.
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            Accumulation of yolk proteins in insect oocytes.

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              Insect vitellogenin/lipophorin receptors: molecular structures, role in oogenesis, and regulatory mechanisms.

              Insect vitellogenin and lipophorin receptors (VgRs/LpRs) belong to the low-density lipoprotein receptor (LDLR) gene superfamily and play a critical role in oocyte development by mediating endocytosis of the major yolk protein precursors Vg and Lp, respectively. Precursor Vg and Lp are synthesized, in the majority of insects, extraovarially in the fat body and are internalized by competent oocytes through membrane-bound receptors (i.e., VgRs and LpRs, respectively). Structural analysis reveals that insect VgRs/LpRs and all other LDLR family receptors share a group of five structural domains: clusters of cysteine-rich repeats constituting the ligand-binding domain (LBD), epidermal growth factor (EGF)-precursor homology domain that mediates the acid-dependent dissociation of ligands, an O-linked sugar domain of unknown function, a transmembrane domain anchoring the receptor in the plasma membrane, and a cytoplasmic domain that mediates the clustering of the receptor into the coated pits. The sequence analysis indicates that insect VgRs harbor two LBDs with five repeats in the first and eight repeats in the second domain as compared to LpRs which have a single 8-repeat LBD. Moreover, the cytoplasmic domain of all insect VgRs contains a LI internalization signal instead of the NPXY motif found in LpRs and in the majority of other LDLR family receptors. The exception is that of Solenopsis invicta VgR, which also contains an NPXY motif in addition to LI signal. Cockroach VgRs still harbor another motif, NPTF, which is also believed to be a functional internalization signal. The expression studies clearly demonstrate that insect VgRs are ovary-bound receptors of the LDLR family as compared to LpRs, which are transcribed in a wide range of tissues including ovary, fat body, midgut, brain, testis, Malpighian tubules, and muscles. VgR/LpR mRNA and the protein were detected in the germarium, suggesting that the genes involved in receptor-endocytotic machinery are specifically expressed long before they are functionally required.
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                Author and article information

                Contributors
                Role: Subject Editor
                Journal
                J Insect Sci
                J. Insect Sci
                jis
                Journal of Insect Science
                Oxford University Press (US )
                1536-2442
                November 2019
                08 December 2019
                08 December 2019
                : 19
                : 6
                : 15
                Affiliations
                International Research Center for the Collaborative Containment of Cross-Border Pests in Central Asia, College of Life Sciences, Xinjiang Normal University , Urumqi, China
                Author notes
                Corresponding author, e-mail: wanghanguoxi@ 123456163.com
                Article
                iez119
                10.1093/jisesa/iez119
                6899333
                31812980
                6989417d-dd4d-448b-a90f-17b2d1c36c17
                © The Author(s) 2019. Published by Oxford University Press on behalf of Entomological Society of America.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence ( http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 21 October 2019
                : 14 November 2019
                Page count
                Pages: 8
                Funding
                Funded by: Tianshan Youth Project
                Award ID: 2017Q024
                Funded by: Xinjiang Uygur Autonomous Region, the University scientific research Project
                Award ID: XJEDU2017M023
                Funded by: Xinjiang Uygur Autonomous Region, the Project of Key Laboratory of Xinjiang Normal University
                Award ID: XJTSWZ-2018-02
                Funded by: International S&T Cooperation Project of China (ISTCP)
                Award ID: 2016YFE0203100
                Award ID: 2015DFR30290
                Funded by: University Innovation Team Project of Xinjiang Uygur Autonomous Region
                Award ID: XJEDU2017T007
                Categories
                Molecular Entomological Genetics

                Entomology
                calliptamus italicus,vitellogenin receptor,vitellin,gene clone,sequence analysis
                Entomology
                calliptamus italicus, vitellogenin receptor, vitellin, gene clone, sequence analysis

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