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      Evidence for a transcellular route for vitellogenin transport in the telotrophic ovary of Podisus nigrispinus (Hemiptera: Pentatomidae)

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          Abstract

          Vitellogenin is the main yolk precursor protein in insect oocytes. It is synthesized in the fat body and released into the hemolymph. To reach the oocyte surface, vitellogenin must cross a single layer of follicular epithelium cells. The transport of vitellogenin across the follicular epithelium has been suggested to occur through the enlarged intercellular spaces (patency) by a paracellular route or by endocytosis by follicular cells and release onto oocyte surface in a transcelluar route. In this study, we investigated whether vitellogenin transport in the meroistic telotrophic ovary of Podisus nigrispinus (Hemiptera) occurs via a paracellular or transcellular route. Light and transmission electron microscopies showed that short cell–cell contacts with well-developed occluding septate junctions were present in follicular cells with patency. Immunofluorescence microscopy revealed the presence of vitellogenin receptors in the plasma membrane and of vitellogenin in the cytoplasm of follicular cells. Data suggest that cell–cell contacts serve as a barrier to large vitellogenin molecules and that this protein is transported via a transcellular route of receptor-mediated endocytosis.

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          Accumulation of yolk proteins in insect oocytes.

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            Social exploitation of vitellogenin.

            Vitellogenin is a female-specific glucolipoprotein yolk precursor produced by all oviparous animals. Vitellogenin expression is under hormonal control, and the protein is generally synthesized directly before yolk deposition. In the honeybee (Apis mellifera), vitellogenin is not only synthesized by the reproductive queen, but also by the functionally sterile workers. In summer, the worker population consists of a hive bee group performing a multitude of tasks including nursing inside the nest, and a forager group specialized in collecting nectar, pollen, water, and propolis. Vitellogenin is synthesized in large quantities by hive bees. When hive bees develop into foragers, their juvenile hormone titers increase, and this causes cessation of their vitellogenin production. This inverse relationship between vitellogenin synthesis and juvenile hormone is opposite to the norm in insects, and the underlying proximate processes and life-history reasons are still not understood. Here we document an alternative use of vitellogenin by showing that it is a source for the proteinaceous royal jelly that is produced by the hive bees. Hive bees use the jelly to feed larvae, queen, workers, and drones. This finding suggests that the evolution of a brood-rearing worker class and a specialized forager class in an advanced eusocial insect society has been directed by an alternative utilization of yolk protein.
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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
                jeserrao@ufv.br
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                11 November 2019
                11 November 2019
                2019
                : 9
                : 16441
                Affiliations
                [1 ]ISNI 0000 0000 8338 6359, GRID grid.12799.34, Department of General Biology, , Universidade Federal de Viçosa, ; 36570-000 Viçosa, Brazil
                [2 ]ISNI 0000 0000 8338 6359, GRID grid.12799.34, Departament of Entomology, , Universidade Federal de Viçosa, ; 36570-000 Viçosa, Brazil
                Author information
                http://orcid.org/0000-0003-4353-7011
                http://orcid.org/0000-0002-0477-4252
                Article
                52789
                10.1038/s41598-019-52789-z
                6848487
                31712640
                3cabdfce-9454-43f5-b623-0e8bab000212
                © The Author(s) 2019

                Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 28 August 2018
                : 23 October 2019
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                © The Author(s) 2019

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                electron microscopy,entomology
                Uncategorized
                electron microscopy, entomology

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