Selective Translation of Maternal mRNA by eIF4E1B Controls Oocyte to Embryo Transition

被引:11
|
作者
Guo, Jing [1 ]
Zhao, Hailian [2 ,3 ]
Zhang, Jue [1 ]
Lv, Xiangjiang [4 ]
Zhang, Shen [1 ]
Su, Ruibao [2 ,3 ]
Zheng, Wei [1 ]
Dai, Jing [1 ,4 ]
Meng, Fei [1 ]
Gong, Fei [1 ,4 ]
Lu, Guangxiu [1 ,4 ]
Xue, Yuanchao [2 ,3 ]
Lin, Ge [1 ,4 ]
机构
[1] Reprod & Genet Hosp CIT Xiangya, Clin Res Ctr Reprod & Genet Hunan Prov, Changsha 410078, Peoples R China
[2] Chinese Acad Sci, Inst Biophys, Key Lab RNA Biol, Beijing 100101, Peoples R China
[3] Univ Chinese Acad Sci, Beijing 100049, Peoples R China
[4] Cent South Univ, Lab Reprod & Stem Cell Engn, NHC Key Lab Human Stem Cell & Reprod Engn, Changsha 410078, Peoples R China
基金
中国国家自然科学基金;
关键词
infertility; oocyte to embryo transition; RNA-binding protein; translation; GENOME-WIDE ANALYSIS; MAMMALIAN OOCYTE; FAMILY-MEMBERS; PROTEIN; REVEALS; MATURATION; DAZL; TRANSCRIPTOME; INFERTILITY; ACTIVATION;
D O I
10.1002/advs.202205500
中图分类号
O6 [化学];
学科分类号
0703 ;
摘要
Maternal messenger ribonucleic acids (mRNAs) are driven by a highly orchestrated scheme of recruitment to polysomes and translational activation. However, selecting and regulating individual mRNAs for the translation from a competitive pool of mRNAs are little-known processes. This research shows that the maternal eukaryotic translation initiation factor 4e1b (Eif4e1b) expresses during the oocyte-to-embryo transition (OET), and maternal deletion of Eif4e1b leads to multiple defects concerning oogenesis and embryonic developmental competence during OET. The linear amplification of complementary deoxyribonucleic acid (cDNA) ends, and sequencing (LACE-seq) is used to identify the distinct subset of mRNA and its CG-rich binding sites within the 5 ' untranslated region (UTR) targeted by eIF4E1B. The proteomics analyses indicate that eIF4E1B-specific bound genes show stronger downregulation at the protein level, which further verify a group of proteins that plays a crucial role in oocyte maturation and embryonic developmental competence is insufficiently synthesized in Eif4e1b-cKO oocytes during OET. Moreover, the biochemical results in vitro are combined to further confirm the maternal-specific translation activation model assembled by eIF4E1B and 3 ' UTR-associated mRNA binding proteins. The findings demonstrate the indispensability of eIF4E1B for selective translation activation in mammalian oocytes and provide a potential network regulated by eIF4E1B in OET.
引用
收藏
页数:17
相关论文
共 50 条
  • [31] Zap1-dependent transcription from an alternative upstream promoter controls translation of RTC4 mRNA in zinc-deficient Saccharomyces cerevisiae
    Taggart, Janet
    MacDiarmid, Colin W.
    Haws, Spencer
    Eide, David J.
    MOLECULAR MICROBIOLOGY, 2017, 106 (05) : 678 - 689
  • [32] A noncanonical function of EIF4E limits ALDH1B1 activity and increases susceptibility to ferroptosis
    Chen, Xin
    Huang, Jun
    Yu, Chunhua
    Liu, Jiao
    Gao, Wanli
    Li, Jingbo
    Song, Xinxin
    Zhou, Zhuan
    Li, Changfeng
    Xie, Yangchun
    Kroemer, Guido
    Liu, Jinbao
    Tang, Daolin
    Kang, Rui
    NATURE COMMUNICATIONS, 2022, 13 (01)
  • [33] Influenza virus polymerase confers independence of the cellular cap-binding factor eIF4E for viral mRNA translation
    Yangueez, Emilio
    Rodriguez, Paloma
    Goodfellow, Ian
    Nieto, Amelia
    VIROLOGY, 2012, 422 (02) : 297 - 307
  • [34] Regulation of the mammalian maternal-to-embryonic transition by eukaryotic translation initiation factor 4E
    Li, Yan
    Tang, Jianan
    Ji, Xu
    Hua, Min-Min
    Liu, Miao
    Chang, Lu
    Gu, Yihua
    Shi, Changgen
    Ni, Wuhua
    Liu, Jing
    Shi, Hui-juan
    Huang, Xuefeng
    O'Neill, Christopher
    Jin, Xingliang
    DEVELOPMENT, 2021, 148 (12):
  • [35] Structure of the eukaryotic translation initiation factor eIF4E in complex with 4EGI-1 reveals an allosteric mechanism for dissociating eIF4G
    Papadopoulos, Evangelos
    Jenni, Simon
    Kabha, Eihab
    Takrouri, Khuloud J.
    Yi, Tingfang
    Salvi, Nicola
    Luna, Rafael E.
    Gavathiotis, Evripidis
    Mahalingam, Poornachandran
    Arthanari, Haribabu
    Rodriguez-Mias, Ricard
    Yefidoff-Freedman, Revital
    Aktas, Bertal H.
    Chorev, Michael
    Halperin, Jose A.
    Wagner, Gerhard
    PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2014, 111 (31) : E3187 - E3195
  • [36] Structural Insights into the Allosteric Effects of 4EBP1 on the Eukaryotic Translation Initiation Factor eIF4E
    Siddiqui, Nadeem
    Tempel, Wolfram
    Nedyalkova, Lucy
    Volpon, Laurent
    Wernimont, Amy K.
    Osborne, Michael J.
    Park, Hee-Won
    Borden, Katherine L. B.
    JOURNAL OF MOLECULAR BIOLOGY, 2012, 415 (05) : 781 - 792
  • [37] Sensitivity of Global Translation to mTOR Inhibition in REN Cells Depends on the Equilibrium between eIF4E and 4E-BP1
    Grosso, Stefano
    Pesce, Elisa
    Brina, Daniela
    Beugnet, Anne
    Loreni, Fabrizio
    Biffo, Stefano
    PLOS ONE, 2011, 6 (12):
  • [38] Cap-dependent translation initiation factor, eIF4E, is the target for Ouabain-mediated inhibition of HIF-1α
    Cao, Ji
    He, Lingjuan
    Lin, Guanyu
    Hu, Chunqi
    Dong, Rong
    Zhang, Jun
    Zhu, Hong
    Hu, Yongzhou
    Wagner, Carston R.
    He, Qiaojun
    Yang, Bo
    BIOCHEMICAL PHARMACOLOGY, 2014, 89 (01) : 20 - 30
  • [39] Phosphorylation of eIF4E by Mnk-1 enhances HSV-1 translation and replication in quiescent cells
    Walsh, D
    Mohr, I
    GENES & DEVELOPMENT, 2004, 18 (06) : 660 - 672
  • [40] Biophysical studies of eIF4E cap-binding protein:: Recognition of mRNA 5′ cap structure and synthetic fragments of eIF4G and 4E-BP1 proteins
    Niedzwiecka, A
    Marcotrigiano, J
    Stepinski, J
    Jankowska-Anyszka, M
    Wyslouch-Cieszynska, A
    Dadlez, M
    Gingras, AC
    Mak, P
    Darzynkiewicz, E
    Sonenberg, N
    Burley, SK
    Stolarski, R
    JOURNAL OF MOLECULAR BIOLOGY, 2002, 319 (03) : 615 - 635