广西师范大学学报（自然科学版） ›› 2024, Vol. 42 ›› Issue (2): 183-191.doi: 10.16088/j.issn.1001-6600.2023031501

• • 上一篇    下一篇

青鳉gsdf调控Igf2bp2/Igf2bp3-m6A阅读器在雌雄生殖细胞的差异表达

王光幸, 郭振华, 杨继辉, 李雅园, 李新闻, 关桂君*   

  1. 上海海洋大学 水产与生命学院, 上海 201306
  • 收稿日期:2023-03-15 修回日期:2023-05-15 发布日期:2024-04-22
  • 通讯作者: 关桂君(1965—), 女, 浙江镇海人, 上海海洋大学教授, 博士。 E-mail: gjguan@shou.edu.cn
  • 基金资助:
    国家重点研发计划(2018YFD0900601)

Medaka gsdf Regulates Differential Expression of Igf2bp2/Igf2bp3-m6A Reader in Male and Female Germ Cells

WANG Guangxing, GUO Zhenhua, YANG Jihui, LI Yayuan, LI Xinwen, GUAN Guijun*   

  1. College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China
  • Received:2023-03-15 Revised:2023-05-15 Published:2024-04-22

PDF (PC)

10

摘要： 青鳉gsdf敲除导致生殖细胞异常增殖,产生XY巨大精巢或XY巨大卵巢。正常精巢、卵巢及gsdf缺失型XY巨大精巢或巨大卵巢的mRNA转录组比对分析和qPCR验证结果显示,igf2bp2表达可能受gsdf信号调控。脊椎动物igf2bp2的分子结构高度进化保守,igf2bp2 mRNA在胚胎发育各时期均有表达,在成体精巢表达量最高,提示igf2bp2可能在早期胚胎发育、性别分化及精子生成发育中起重要作用。免疫荧光检测显示XY精巢的抗Igf2bp2免疫反应信号强于XX卵巢、gsdf缺失型XY精巢和XY卵巢。不同于gsdf缺失激活igf2bp3的表达,gsdf缺失反而减弱igf2bp2表达。Gsdf对igf2bp2和igf2bp3的正负调控影响其介导的m6A甲基腺苷修饰,以及其靶向的mRNA转录后修饰和翻译,这一分子调控机制可能在脊椎动物性别分化和精子生成过程中普遍存在。

关键词: 青鳉, 生殖细胞, 性别分化, 调控, 转录生长因子-β

Abstract: Knockout of gonadal soma-derived factor (gsdf), led to the abnormal proliferation of germ cells and sexual reversal of XY males to females. Differences in transcriptome data of wild-type XY testis, XX ovary, and gsdf-deficient XY giant testis or XY giant ovary showed that the expression level of igf2bp2 (insulin-like growth factor 2 mRNA binding protein 2) was significantly higher in wild-type XY sperms than that in wild-type XX ovary and gsdf-deficient XY sperms and XY ovary, and confirmed by RT-qPCR, suggesting that igf2bp2 expression may be regulated by gsdf signal. The molecular structure of vertebrate igf2bp2 was highly homology evolutionary conserved. RT-qPCR showed that igf2bp2 mRNA was highly expressed in early embryogenesis, especially in the stage of gastrulation. The expression of igf2bp2 was in early embryogenesis and predominant testis in adulthood, suggesting that igf2bp2 may play an important role in early embryonic development, sex differentiation and spermatogenesis. Immunofluorescence assay revealed that the signal of positive reaction of anti-Igf2bp2 antibody in wild-type XY testis was stronger than that of XX ovary, gsdf-deficient XY testis or XY ovary. The presence or absence of gsdf signaling was positively correlated with igf2bp2 expression during gonadal developmental differentiation in medaka, thus may potentially promote igf2bp2 expression, which was opposite to the inhibition of igf2bp3 expression. gsdf-regulatory role of igf2bp2/igf2bp3 expression during medaka spermatogenesis may be a conserved molecular mechanism in vertebrate gonadal differentiation and spermatogenesis.

Key words: medaka, germ cell, sexual differentiation, modulating control, transforming growth factor-β

中图分类号:  S917.4

[1] DAVID C J, MASSAGUÉ J. Contextual determinants of TGFβ action in development, immunity and cancer[J]. Nature Reviews Molecular Cell Biology, 2018, 19(7): 419-435.DOI: 10.1038/s41580-018-0007-0.
[2] DERYNCK R, BUDI E H. Specificity, versatility, and control of TGF-β family signaling[J]. Science Signaling, 2019, 12(570): eaav5183.DOI: 10.1126/scisignal.aav5183.
[3] MORIKAWA M, DERYNCK R, MIYAZONO K. TGF-β and the TGF-β family: context-dependent roles in cell and tissue physiology[J].Cold Spring Harbor Perspectives in Biology, 2016, 8(5): a021873. DOI: 10.1101/cshperspect.a021873.
[4] KANEKO H, IJIRI S, KOBAYASHI T, et al. Gonadal soma-derived factor (gsdf), a TGF-beta superfamily gene, induces testis differentiation in the teleost fish Oreochromis niloticus[J]. Molecular and Cellular Endocrinology, 2015, 415: 87-99.DOI: 10.1016/j.mce.2015.08.008.
[5] 亢逸, 关桂君, 洪云汉. 用模式生物青鳉概观硬骨鱼性别决定及性分化研究进展[J]. 遗传, 2017, 39(6): 441-454. DOI: 10.16288/j.yczz.17-140.
[6] ZHANG X, GUAN G J, LI M Y, et al. Autosomal gsdf acts as a male sex initiator in the fish medaka[J]. Scientific Reports, 2016, 6: 19738. DOI: 10.1038/srep19738.
[7] 郭海燕, 李茜, 关桂君. 青鳉gsdf下游因子zc4h2在脑-性腺中的表达分析[J]. 基因组学与应用生物学, 2022, 41(4): 720-730.DOI:10.13417/j.gab.041.000720.
[8] 李雅园, 王光幸, 李新闻,等. 青鳉nup58的表达及其在性别分化中的潜在作用[J]. 广西师范大学学报(自然科学版), 2024, 42(1): 190-201.DOI:10.16088/j.issn.1001-6600.2023012701.
[9] NISHIMURA T, TANAKA M. Gonadal development in fish[J]. Sexual Development, 2014, 8(5): 252-261.DOI: 10.1159/000364924.
[10] WU X W, ZHANG Y Q, XU S M, et al. Loss of Gsdf leads to a dysregulation of Igf2bp3-mediated oocyte development in medaka[J]. General and Comparative Endocrinology, 2019, 277: 122-129.DOI: 10.1016/j.ygcen.2019.04.001.
[11] DAI N. The diverse functions of IMP2/IGF2BP2 in metabolism[J]. Trends in Endocrinology and Metabolism, 2020, 31(9): 670-679.DOI: 10.1016/j.tem.2020.05.007.
[12] KORN S M, ULSHÖEFER C J, SCHNEIDER T, et al. Structures and target RNA preferences of the RNA-binding protein family of IGF2BPs: an overview[J]. Structure, 2021, 29(8): 787-803. DOI: 10.1016/j.str.2021.05.001.
[13] YISRAELI J K. VICKZ proteins: a multi-talented family of regulatory RNA-binding proteins[J]. Biology of the Cell, 2005, 97(1): 87-96.DOI: 10.1042/BC20040151.
[14] LI M Y, RONG X Z, LU L, et al. IGF-2 mRNA binding protein 2 regulates primordial germ cell development in zebrafish[J]. General and Comparative Endocrinology, 2021, 313: 113875.DOI: 10.1016/j.ygcen.2021.113875.
[15] GALLARDO T D, JOHN G B, SHIRLEY L, et al. Genomewide discovery and classification of candidate ovarian fertility genes in the mouse[J]. Genetics, 2007, 177(1): 179-194.DOI: 10.1534/genetics.107.074823.
[16] LI X, LI X W, LI W H, et al. Sex-specific meiosis responses to Gsdf in medaka (Oryzias latipes)[J]. The FEBS Journal, 2023, 290(10): 2760-2779. DOI: 10.1111/febs.16701.
[17] BAI G, ZHAI X X, LIU L L, et al. The molecular characteristics in different procedures of spermatogenesis[J]. Gene, 2022, 826: 146405.DOI: 10.1016/j.gene.2022.146405.
[18] TANG C, XIE Y M, YU T, et al. m6A-dependent biogenesis of circular RNAs in male germ cells[J]. Cell Research, 2020, 30(3): 211-228.DOI: 10.1038/s41422-020-0279-8.
[19] HAMMER N A, HANSEN T V O, BYSKOV A G, et al. Expression of IGF-II mRNA-binding proteins (IMPs) in gonads and testicular cancer[J]. Reproduction, 2005, 130(2): 203-212. DOI: 10.1530/rep.1.00664.
[20] 郭韶珂,裴杰,王兴东,等.m6A修饰及其生殖调控功能研究进展[J].中国畜牧杂志,2022,58(1):21-27.DOI:10.19556/j.0258-7033.20210106-05.
[21] TANG C, KLUKOVICH R, PENG H Y, et al. ALKBH5-dependent m6A demethylation controls splicing and stability of long 3′-UTR mRNAs in male germ cells[J]. Proceedings of the National Academy of Sciences of the United States of America, 2018, 115(2): E325-E333.DOI: 10.1073/pnas.1717794115.
[22] ZHANG X T, CHANG Y Y, ZHAI W Y, et al. A potential role for the Gsdf-eEF1α complex in inhibiting germ cell proliferation: a protein-interaction analysis in medaka (Oryzias latipes) from a proteomics perspective[J]. Molecular & Cellular Proteomics, 2021, 20: 100023.DOI: 10.1074/mcp.RA120.002306.
[23] LIU H B, MUHAMMAD T, GUO Y S, et al. RNA-binding protein IGF2BP2/IMP2 is a critical maternal activator in early zygotic genome activation[J]. Advanced Science, 2019, 6(15): 1900295.DOI: 10.1002/advs.201900295.
[24] DeCHIARA T M, ROBERTSON E J, EFSTRATIADIS A. Parental imprinting of the mouse insulin-like growth factor II gene[J]. Cell, 1991, 64(4): 849-859.DOI: 10.1016/0092-8674(91)90513-x.
[25] WOODS K A, CAMACHO-HÜBNER C, SAVAGE M O, et al. Intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene[J]. New England Journal of Medicine, 1996, 335(18): 1363-1367.DOI: 10.1056/NEJM199610313351805.
[26] TENUTA M, CARLOMAGNO F, CANGIANO B, et al. Somatotropic-testicular axis: a crosstalk between GH/IGF-I and gonadal hormones during development, transition, and adult age[J]. Andrology, 2021, 9(1): 168-184.DOI: 10.1111/andr.12918.
[27] McGLADE E A, HERRERA G G, STEPHENS K K, et al. Cell-type specific analysis of physiological action of estrogen in mouse oviducts[J]. The FASEB Journal, 2021, 35(5): e21563.DOI: 10.1096/fj.202002747R.
[28] CANNARELLA R, MANCUSO F, ARATO I, et al. Sperm-carried IGF2 downregulated the expression of mitogens produced by Sertoli cells: a paracrine mechanism for regulating spermatogenesis?[J]. Frontiers in Endocrinology, 2022, 13: 1010796.DOI: 10.3389/fendo.2022.1010796.
[29] DAI N, ZHAO L P, WRIGHTING D, et al. IGF2BP2/IMP2-deficient mice resist obesity through enhanced translation of Ucp1 mRNA and other mRNAs encoding mitochondrial proteins[J]. Cell Metabolism, 2015, 21(4): 609-621.DOI: 10.1016/j.cmet.2015.03.006.
[30] LAGGAI S, KESSLER S M, BOETTCHER S, et al. The IGF2 mRNA binding protein p62/IGF2BP2-2 induces fatty acid elongation as a critical feature of steatosis[J]. Journal of Lipid Research, 2014, 55(6): 1087-1097.DOI: 10.1194/jlr.M045500.
[31] SIMPSON A, PETNGA W, MACAULAY V M, et al. Insulin-like growth factor (IGF) pathway targeting in cancer: role of the IGF axis and opportunities for future combination studies[J]. Targeted Oncology, 2017, 12(5): 571-597.DOI:10.1007/s11523-017-0514-5.
[1] 王辉, 冯平. 苦味受体的非味觉功能研究进展[J]. 广西师范大学学报（自然科学版）, 2024, 42(1): 18-27.
[2] 李雅园, 王光幸, 李新闻, 郭振华, 关桂君. 青鳉nup58的表达及其在性别分化中的潜在作用[J]. 广西师范大学学报（自然科学版）, 2024, 42(1): 168-179.
[3] 武霞, 许艺兰, 文露婷, 黄姻, 覃俊奇, 周康奇, 杜雪松, 陈忠, 潘贤辉, 宾石玉. 全州禾花鲤色素细胞组成、分布及色素含量观测[J]. 广西师范大学学报（自然科学版）, 2022, 40(6): 222-229.
[4] 庞冰冰, 叶丰彩, 李钰艳, 尚常花. 微藻类胡萝卜素合成与代谢调控研究进展[J]. 广西师范大学学报（自然科学版）, 2021, 39(6): 13-23.
[5] 刘伟铭, 陈纲梅, 林观荣, 李静宁. 高速公路收费站与衔接信号交叉口协调控制研究[J]. 广西师范大学学报（自然科学版）, 2019, 37(4): 16-26.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
[1] 王宁, 刘敏. 径向基函数方法在原子核质量预言中的应用[J]. 广西师范大学学报（自然科学版）, 2012, 30(3): 59 -63 .
[2] 阿尧林, 王耀辉, 董金超, 李剑锋. 原位拉曼光谱研究电催化反应过程[J]. 广西师范大学学报（自然科学版）, 2022, 40(5): 183 -198 .
[3] 吴海锋, 张瑾, 陆祖军, 尚常花. 酱香型白酒大曲细菌与蛋白酶研究进展[J]. 广西师范大学学报（自然科学版）, 2022, 40(5): 398 -405 .
[4] 董淑龙, 马姜明, 辛文杰. 景观视觉评价研究进展与趋势——基于CiteSpace的知识图谱分析[J]. 广西师范大学学报（自然科学版）, 2023, 41(5): 1 -13 .
[5] 莫丽丽, 周子豪, 李定宏, 曾文龙, 武正军, 黄锦龙, 孙涛. 克氏原螯虾8种代谢物对其引诱效果研究[J]. 广西师范大学学报（自然科学版）, 2023, 41(5): 143 -151 .
[6] 袁静静, 郑宇钊, 徐晨枫, 殷婷婕. 非内吞依赖型生物大分子药物胞质递送策略研究进展[J]. 广西师范大学学报（自然科学版）, 2024, 42(1): 1 -8 .
[7] 涂广升, 孔咏骏, 宋哲超, 叶康. 密文域可逆信息隐藏研究进展及技术难点分析[J]. 广西师范大学学报（自然科学版）, 2024, 42(2): 1 -15 .
[8] 杨杨阳, 朱震霆, 杨翠萍, 李世豪, 张舒, 范秀磊, 万蕾. 基于文献计量学分析的剩余污泥厌氧消化预处理研究进展[J]. 广西师范大学学报（自然科学版）, 2024, 42(2): 16 -29 .
[9] 许伦辉, 李金龙, 李若南, 陈俊宇. 基于动态生成对抗网络的路网缺失交通数据修复[J]. 广西师范大学学报（自然科学版）, 2024, 42(2): 30 -40 .
[10] 杨海, 谢亚琴. 基于Floyd算法的5G基站区域储能分配策略[J]. 广西师范大学学报（自然科学版）, 2024, 42(2): 41 -54 .
版权所有 © 广西师范大学学报（自然科学版）编辑部
地址：广西桂林市三里店育才路15号　邮编：541004
电话：0773-5857325　E-mail: gxsdzkb@mailbox.gxnu.edu.cn
本系统由北京玛格泰克科技发展有限公司设计开发