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      A Novel igf3 Gene in Common Carp ( Cyprinus carpio): Evidence for Its Role in Regulating Gonadal Development

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          Abstract

          Since the insulin-like growth factor 3 ( igf3) gene was recently discovered in fish ovary, its function in the gonads has received much attention. In this study, we isolated two igf3 subtypes from common carp ( Cyprinus carpio), which comprised full-length cDNA of 707 and 1153 nucleotides encoding 205 and 198 amino acids (aa), respectively. The Igf3 aa sequence had the highest gene homology of 72% with the corresponding sequence in zebrafish ( Danio rerio). Phylogenetic tree construction revealed that the C. carpio igf3 gene was first clustered with D. rerio and then with other teleost species. Igf3 mRNA was widely expressed, with expression being highest in the gonads and blood. In the gonad development stage, igf3a mRNA expression was highest in the maturity and recession stage of the ovary, and decline phase of the testis, while igf3b was highest in the recession and fully mature periods of the ovaries and testes, respectively. Western blotting of testis protein samples showed two bands of approximately 21 kDa and 34 kDa corresponding to the calculated molecular mass of the two Igf3 subtypes; no signal was detected in the ovary. The Igf3 protein was localized in the ovary granulosa cells and testis spermatogonium and spermatids. 17β-Ethinylestradiol treatment increased both ovary and testis igf3 mRNA expression. These findings suggest that Igf3 may play an important role in C. carpio gonadal development.

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          Influences of the environment on the endocrine and paracrine fish growth hormone-insulin-like growth factor-I system.

          Insulin-like growth factor-I (IGF-I) is a key component of the complex system that regulates differentiation, development, growth and reproduction of fishes. The IGF-I gene is mainly expressed in the liver that represents the principal source of endocrine IGF-I but also in numerous other organs where the hormone most probably acts in an autocrine-paracrine manner. The primary stimulus for synthesis and release of IGF-I is growth hormone (GH) from the anterior pituitary. Thus, in analogy to mammals, it is usual to speak of a fish 'GH-IGF-I axis'. The GH-IGF-I system is affected by changes in the environment and probably represents a target of endocrine disrupting compounds (EDC) that impair many physiological processes in fishes. Thus, the review deals with the influences of changes in different environmental factors, such as food availability, temperature, photoperiod, season, salinity and EDCs, on GH gene expression in pituitary, IGF-I gene expression in liver and extrahepatic sites and the physiological effects resulting from the evoked alterations in endocrine and local IGF-I. Environmental influences certainly interact with each other but for convenience of the reader they will be dealt with in separate sections. Current trends in GH-IGF-I research are analysed and future focuses are suggested at the end of the sections.
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            Fsh Stimulates Spermatogonial Proliferation and Differentiation in Zebrafish via Igf3.

            Growth factors modulate germ line stem cell self-renewal and differentiation behavior. We investigate the effects of Igf3, a fish-specific member of the igf family. Fsh increased in a steroid-independent manner the number and mitotic index of single type A undifferentiated spermatogonia and of clones of type A differentiating spermatogonia in adult zebrafish testis. All 4 igf gene family members in zebrafish are expressed in the testis but in tissue culture only igf3 transcript levels increased in response to recombinant zebrafish Fsh. This occurred in a cAMP/protein kinase A-dependent manner, in line with the results of studies on the igf3 gene promoter. Igf3 protein was detected in Sertoli cells. Recombinant zebrafish Igf3 increased the mitotic index of type A undifferentiated and type A differentiating spermatogonia and up-regulated the expression of genes related to spermatogonial differentiation and entry into meiosis, but Igf3 did not modulate testicular androgen release. An Igf receptor inhibitor blocked these effects of Igf3. Importantly, the Igf receptor inhibitor also blocked Fsh-induced spermatogonial proliferation. We conclude that Fsh stimulated Sertoli cell production of Igf3, which promoted via Igf receptor signaling spermatogonial proliferation and differentiation and their entry into meiosis. Because previous work showed that Fsh also released spermatogonia from an inhibitory signal by down-regulating anti-Müllerian hormone and by stimulating androgen production, we can now present a model, in which Fsh orchestrates the activity of stimulatory (Igf3, androgens) and inhibitory (anti-Müllerian hormone) signals to promote spermatogenesis.
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              Evolution of Ancient Functions in the Vertebrate Insulin-Like Growth Factor System Uncovered by Study of Duplicated Salmonid Fish Genomes

              Whole-genome duplication (WGD) was experienced twice by the vertebrate ancestor (2 rounds; 2R), again by the teleost fish ancestor (3R) and most recently in certain teleost lineages (4R). Consequently, vertebrate gene families are often expanded in 3R and 4R genomes. Arguably, many types of “functional divergence” present across 2R gene families will exceed that between 3R/4R paralogs of genes comprising 2R families. Accordingly, 4R offers a form of replication of 2R. Examining whether this concept has implications for molecular evolutionary research, we studied insulin-like growth factor (IGF) binding proteins (IGFBPs), whose six 2R family members carry IGF hormones and regulate interactions between IGFs and IGF1-receptors (IGF1Rs). Using phylogenomic approaches, we resolved the complete IGFBP repertoire of 4R-derived salmonid fishes (19 genes; 13 more than human) and established evolutionary relationships/nomenclature with respect to WGDs. Traits central to IGFBP action were determined for all genes, including atomic interactions in IGFBP–IGF1/IGF2 complexes regulating IGF–IGF1R binding. Using statistical methods, we demonstrate that attributes of these protein interfaces are overwhelming a product of 2R IGFBP family membership, explain 49–68% of variation in IGFBP mRNA concentration in several different tissues, and strongly predict the strength and direction of IGFBP transcriptional regulation under differing nutritional states. The results support a model where vertebrate IGFBP family members evolved divergent structural attributes to provide distinct competition for IGFs with IGF1Rs, predisposing different functions in the regulation of IGF signaling. Evolution of gene expression then acted to ensure the appropriate physiological production of IGFBPs according to their structural specializations, leading to optimal IGF-signaling according to nutritional-status and the endocrine/local mode of action. This study demonstrates that relatively recent gene family expansion can facilitate inference of functional evolution within ancient genetic systems.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                21 December 2016
                2016
                : 11
                : 12
                : e0168874
                Affiliations
                [1 ]Wuxi Fisheries College, Nanjing Agricultural University, Wuxi, Jiangsu, China
                [2 ]Freshwater Fisheries Research Centre of Chinese Academy of Fishery Sciences, Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture, Wuxi, Jiangsu, China
                Chinese Academy of Sciences, CHINA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: ZJD.

                • Data curation: FBS LMW.

                • Formal analysis: FBS LMW.

                • Funding acquisition: ZJD LMW.

                • Investigation: WBZ JJF JJD.

                • Methodology: ZJD.

                • Project administration: ZJD.

                • Resources: LMW ZJD.

                • Supervision: ZJD.

                • Validation: FBS LMW WBZ JJF JJD.

                • Visualization: FBS LMW.

                • Writing – original draft: FBS LMW.

                • Writing – review & editing: FBS LMW WBZ JJF JJD ZJD.

                Article
                PONE-D-16-31618
                10.1371/journal.pone.0168874
                5176323
                28002497
                18c2f0ad-50c9-496a-9733-f97afc02aba6
                © 2016 Song et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 8 August 2016
                : 7 December 2016
                Page count
                Figures: 8, Tables: 2, Pages: 17
                Funding
                Funded by: National Nonprofit Institute Research Grant of CATAS-TCGRI
                Award ID: 2015JBFR01
                Award Recipient :
                Funded by: Chinese Earmarked Fund for Modern Agro-Industry Technology Research System
                Award ID: CARS-46
                Award Recipient :
                Funded by: National Science and Technology Pillar Program during the Twelfth Five-year Plan Period
                Award ID: 2012BAD26B02
                Award Recipient :
                The National Nonprofit Institute Research Grant of CATAS-TCGRI (2015JBFR01) supported the study design and preparation of the manuscript; the Chinese Earmarked Fund for Modern Agro-Industry Technology Research System (CARS-46) supported the research and data analysis; the National Science & Technology Pillar Program during the Twelfth Five-year Plan Period (2012BAD26B02) supported the materials.
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