Igf2bp3 maintains maternal RNA stability and ensures early embryo development in zebrafish

被引:38
作者
Ren, Fan [1 ]
Lin, Qiaohong [1 ]
Gong, Gaorui [1 ]
Du, Xian [2 ,3 ]
Dan, Hong [1 ]
Qin, Wenying [2 ,3 ]
Miao, Ran [1 ]
Xiong, Yang [1 ]
Xiao, Rui [2 ,3 ]
Li, Xiaohui [1 ]
Gui, Jian-Fang [1 ,4 ]
Mei, Jie [1 ]
机构
[1] Huazhong Agr Univ, Coll Fisheries, Wuhan 430070, Peoples R China
[2] Wuhan Univ, Zhongnan Hosp, Med Res Inst, Frontier Sci Ctr Immunol & Metab, Wuhan 430071, Peoples R China
[3] Wuhan Univ, Zhongnan Hosp, Dept Hematol, Wuhan 430071, Peoples R China
[4] Chinese Acad Sci, Univ Chinese Acad Sci, Inst Hydrobiol, State Key Lab Freshwater Ecol & Biotechnol, Wuhan 430072, Peoples R China
基金
国家重点研发计划;
关键词
TO-ZYGOTIC TRANSITION; FILAMENTOUS ACTIN; BUCKY BALL; MYOSIN-II; GENE; TRANSCRIPTOME; CLEARANCE; CYTOSKELETON; TRANSLATION; PACKAGE;
D O I
10.1038/s42003-020-0827-2
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Early embryogenesis relies on maternally inherited mRNAs. Although the mechanism of maternal mRNA degradation during maternal-to-zygotic transition (MZT) has been extensively studied in vertebrates, how the embryos maintain maternal mRNA stability remains unclear. Here, we identify Igf2bp3 as an important regulator of maternal mRNA stability in zebrafish. Depletion of maternal igf2bp3 destabilizes maternal mRNAs prior to MZT and leads to severe developmental defects, including abnormal cytoskeleton organization and cell division. However, the process of oogenesis and the expression levels of maternal mRNAs in unfertilized eggs are normal in maternal igf2bp3 mutants. Gene ontology analysis revealed that these functions are largely mediated by Igf2bp3-bound mRNAs. Indeed, Igf2bp3 depletion destabilizes while its overexpression enhances its targeting maternal mRNAs. Interestingly, igf2bp3 overexpression in wild-type embryos also causes a developmental delay. Altogether, these findings highlight an important function of Igf2bp3 in controlling early zebrafish embryogenesis by binding and regulating the stability of maternal mRNAs. In early embryogenesis, maternal mRNAs are degraded at the maternal-to-zygotic transition (MZT). Mei et al find that the stability of maternal mRNAs before MZT is maintained by the mRNA binding protein Igf2bp3, which is also required for normal zebrafish development.
引用
收藏
页数:10
相关论文
共 52 条
[1]   HNRNPA2B1 Is a Mediator of m6A-Dependent Nuclear RNA Processing Events [J].
Alarcon, Claudio R. ;
Goodarzi, Hani ;
Lee, Hyeseung ;
Liu, Xuhang ;
Tavazoie, Saeed ;
Tavazoie, Sohail F. .
CELL, 2015, 162 (06) :1299-1308
[2]   Ribosome Profiling Shows That miR-430 Reduces Translation Before Causing mRNA Decay in Zebrafish [J].
Bazzini, Ariel A. ;
Lee, Miler T. ;
Giraldez, Antonio J. .
SCIENCE, 2012, 336 (6078) :233-237
[3]  
Becker KA, 1999, J CELL SCI, V112, P97
[4]  
Becker KA, 1996, MOL REPROD DEV, V43, P536
[5]  
Bement WM, 2000, J EXP ZOOL, V286, P767, DOI 10.1002/(SICI)1097-010X(20000601)286:7<767::AID-JEZ11>3.0.CO
[6]  
2-L
[7]   CONTROLLING THE FALSE DISCOVERY RATE - A PRACTICAL AND POWERFUL APPROACH TO MULTIPLE TESTING [J].
BENJAMINI, Y ;
HOCHBERG, Y .
JOURNAL OF THE ROYAL STATISTICAL SOCIETY SERIES B-STATISTICAL METHODOLOGY, 1995, 57 (01) :289-300
[8]   The minimal cadherin-catenin complex binds to actin filaments under force [J].
Buckley, Craig D. ;
Tan, Jiongyi ;
Anderson, Karen L. ;
Hanein, Dorit ;
Volkmann, Niels ;
Weis, William I. ;
Nelson, W. James ;
Dunn, Alexander R. .
SCIENCE, 2014, 346 (6209) :600-+
[9]   Kinesin-1 interacts with Bucky ball to form germ cells and is required to pattern the zebrafish body axis [J].
Campbell, Philip D. ;
Heim, Amanda E. ;
Smith, Mordechai Z. ;
Marlow, Florence L. .
DEVELOPMENT, 2015, 142 (17) :2996-+
[10]   Terminal Uridylyltransferases Execute Programmed Clearance of Maternal Transcriptome in Vertebrate Embryos [J].
Chang, Hyeshik ;
Yeo, Jinah ;
Kim, Jeong-gyun ;
Kim, Hyunjoon ;
Lim, Jaechul ;
Lee, Mihye ;
Kim, Hyun Ho ;
Ohk, Jiyeon ;
Jeon, Hee-Yeon ;
Lee, Hyunsook ;
Jung, Hosung ;
Kim, Kyu-Won ;
Kim, V. Narry .
MOLECULAR CELL, 2018, 70 (01) :72-+