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      Mechanism of hyperproteinemia-induced damage to female reproduction in a genetic silkworm model

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          Summary

          Hyperproteinemia is a metabolic disorder characterized by abnormally elevated plasma protein concentrations (PPC) in humans and animals. Here, a genetic silkworm model with high PPC was employed to investigate the effect of elevated PPC on female reproduction. Transcriptomic analysis revealed that high PPC induces downregulation of the ovarian development-related genes and disrupts ovarian sugar metabolism. Biochemical and endocrinal analyses revealed that high PPC increases trehalose and glucose levels in hemolymph and glycogen content in the fat body through activation of the gluconeogenic pathway and inhibition of the Insulin/Insulin-like growth factor signaling pathway-the serine/threonine kinase (IIS-AKT) pathway, thus disrupting characteristic metabolic homeostasis of sugar in the ovary. These resulted in ovarian developmental delay as well as reduced number and poor quality of eggs. Insulin supplementation effectively increased egg numbers by lowering blood sugar. These collective results provide new insights into the mechanisms by which high PPC negatively affects female reproduction and support the potential therapeutic effects of insulin.

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          Highlights

          • •

            A heritable silkworm model of hyperproteinemia with impaired reproduction is reported

          • •

            High PPC disturbs ovarian sugar metabolism by inducing hyperglycemia

          • •

            Insulin can effectively reduce female reproductive damage caused by high PPC

          Abstract

          Physiology; Molecular biology; Omics; Transcriptomics

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          Most cited references38

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          Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar

          G L Miller (1959)
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            Obesity and time to pregnancy.

            Matthew Longnecker, Richard MacLehose, D Law (2007)
            Obesity may reduce fecundity. We examined the obesity-fecundity association in relation to menstrual cycle regularity, parity, smoking habits and age to gain insight into mechanisms and susceptible subgroups. Data were provided by 7327 pregnant women enrolled in the Collaborative Perinatal Project at 12 study centres in the United States from 1959 to 1965. Prepregnancy body mass index (BMI) was analysed continuously and categorically [underweight ( or=30.0 kg/m2)]. Adjusted fecundability odds ratios (FORs) were estimated using Cox proportional hazards modelling for discrete time data. Fecundity was reduced for overweight [OR=0.92, 95% confidence interval (95% CI): 0.84, 1.01] and obese (OR=0.82, 95% CI: 0.72, 0.95) women compared with optimal weight women and was more evident for obese primiparous women (OR=0.66, 95% CI: 0.49, 0.89). Fecundity remained reduced for overweight and obese women with normal menstrual cycles. Neither smoking habits nor age modified the association. Obesity was associated with reduced fecundity for all subgroups of women and persisted for women with regular cycles. Our results suggest that weight loss could increase fecundity for overweight and obese women, regardless of menstrual cycle regularity, parity, smoking habits and age.
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              Advances in silkworm studies accelerated by the genome sequencing of Bombyx mori.

              Qingyou Xia, Sheng-gong Li, Qili Feng (2013)
              Significant progress has been achieved in silkworm (Bombyx mori) research since the last review on this insect was published in this journal in 2005. In this article, we review the new and exciting progress and discoveries that have been made in B. mori during the past 10 years, which include the construction of a fine genome sequence and a genetic variation map, the evolution of genomes, the advent of functional genomics, the genetic basis of silk production, metamorphic development, immune response, and the advances in genetic manipulation. These advances, which were accelerated by the genome sequencing project, have promoted B. mori as a model organism not only for lepidopterans but also for general biology.
              Article 0 comments Cited 67 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Shi-Qing Xu
                Journal
                Journal ID (nlm-ta): iScience
                Journal ID (iso-abbrev): iScience
                Title: iScience
                Publisher: Elsevier
                ISSN (Electronic): 2589-0042
                Publication date PMC-release: 09 September 2023
                Publication date Collection: 20 October 2023
                Publication date (Electronic): 09 September 2023
                Volume: 26
                Issue: 10
                Electronic Location Identifier: 107860
                Affiliations
                [1 ]School of Biology and Basic Medical Sciences, Suzhou Medical College, Soochow University, Suzhou 215123, China
                [2 ]Institute of Agricultural Biotechnology & Ecology (IABE), Soochow University, Suzhou 215123, China
                Author notes
                [∗ ]Corresponding author szsqxu@ 123456suda.edu.cn
                [3]

                These authors contributed equally

                [4]

                Lead contact

                Article
                Publisher Item ID: S2589-0042(23)01937-5 Publisher ID: 107860
                DOI: 10.1016/j.isci.2023.107860
                PMC ID: 10518704
                PubMed ID: 37752953
                SO-VID: 6be1093f-3650-40fd-bbdb-5019d1c3a9e1
                Copyright © © 2023 The Author(s)
                License:

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                Date received : 16 May 2023
                Date revision received : 11 August 2023
                Date accepted : 6 September 2023
                Categories
                Subject: Article

                Keywords: physiology,molecular biology,omics,transcriptomics
                Data availability:
                Keywords: physiology, molecular biology, omics, transcriptomics

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