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
[21]   The RNA m6A Reader YTHDF2 Is Essential for the Post-transcriptional Regulation of the Maternal Transcriptome and Oocyte Competence [J].
Ivanova, Ivayla ;
Much, Christian ;
Di Giacomo, Monica ;
Azzi, Chiara ;
Morgan, Marcos ;
Moreira, Pedro N. ;
Monahan, Jack ;
Carrieri, Claudia ;
Enright, Anton J. ;
O'Carroll, Donal .
MOLECULAR CELL, 2017, 67 (06) :1059-+
[22]   STAGES OF EMBRYONIC-DEVELOPMENT OF THE ZEBRAFISH [J].
KIMMEL, CB ;
BALLARD, WW ;
KIMMEL, SR ;
ULLMANN, B ;
SCHILLING, TF .
DEVELOPMENTAL DYNAMICS, 1995, 203 (03) :253-310
[23]   Regulation and Function of Maternal Gene Products During the Maternal-to-Zygotic Transition in Drosophila [J].
Laver, John D. ;
Marsolais, Alexander J. ;
Smibert, Craig A. ;
Lipshitz, Howard D. .
MATERNAL-TO-ZYGOTIC TRANSITION, 2015, 113 :43-84
[24]   RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome [J].
Li, Bo ;
Dewey, Colin N. .
BMC BIOINFORMATICS, 2011, 12
[25]   featureCounts: an efficient general purpose program for assigning sequence reads to genomic features [J].
Liao, Yang ;
Smyth, Gordon K. ;
Shi, Wei .
BIOINFORMATICS, 2014, 30 (07) :923-930
[26]   N6-methyladenosine alters RNA structure to regulate binding of a low-complexity protein [J].
Liu, Nian ;
Zhou, Katherine I. ;
Parisien, Marc ;
Dai, Qing ;
Diatchenko, Luda ;
Pan, Tao .
NUCLEIC ACIDS RESEARCH, 2017, 45 (10) :6051-6063
[27]   Deadenylation of maternal mRNAs mediated by miR-427 in Xenopus laevis embryos [J].
Lund, Elsebet ;
Liu, Mingzhu ;
Hartley, Rebecca S. ;
Sheets, Michael D. ;
Dahlberg, James E. .
RNA, 2009, 15 (12) :2351-2363
[28]   Bucky ball functions in Balbiani body assembly and animal-vegetal polarity in the oocyte and follicle cell layer in zebrafish [J].
Marlow, Florence L. ;
Mullins, Mary C. .
DEVELOPMENTAL BIOLOGY, 2008, 321 (01) :40-50
[29]  
Martin M., 2011, EMBNET J, V17, P10, DOI [DOI 10.14806/EJ.17.1.200, 10.14806/ej.17.1.200]
[30]   Transcriptome analysis of zebrafish embryogenesis using microarrays [J].
Mathavan, S ;
Lee, SGP ;
Mak, A ;
Miller, LD ;
Murthy, KRK ;
Govindarajan, KR ;
Tong, Y ;
Wu, YL ;
Lam, SH ;
Yang, H ;
Ruan, YJ ;
Korzh, V ;
Gong, ZY ;
Liu, ET ;
Lufkin, T .
PLOS GENETICS, 2005, 1 (02) :260-276