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
  • [21] eIF4E orchestrates mRNA processing, RNA export and translation to modify specific protein production
    Mars, Jean-Clement
    Culjkovic-Kraljacic, Biljana
    Borden, Katherine L. B.
    NUCLEUS, 2024, 15 (01)
  • [22] eIF4E Phosphorylation Influences Bdnf mRNA Translation in Mouse Dorsal Root Ganglion Neurons
    Moy, Jamie K.
    Khoutorsky, Arkady
    Asiedu, Marina N.
    Dussor, Gregory
    Price, Theodore J.
    FRONTIERS IN CELLULAR NEUROSCIENCE, 2018, 12
  • [23] Phosphorylation of Arabidopsis eIF4E and eIFiso4E by SnRK1 inhibits translation
    Bruns, Aaron N.
    Li, Sizhun
    Mohannath, Gireesha
    Bisaro, David M.
    FEBS JOURNAL, 2019, 286 (19) : 3778 - 3796
  • [24] Crystal structure of the Trypanosoma cruzi EIF4E5 translation factor homologue in complex with mRNA cap-4
    Reolon, Lidia Watanabe
    Vichier-Guerre, Sophie
    de Matos, Bruno Moises
    Dugue, Laurence
    da Silva Assuncao, Tatiana Reichert
    Tonin Zanchin, Nilson Ivo
    Pochet, Sylvie
    Guimaraes, Beatriz Gomes
    NUCLEIC ACIDS RESEARCH, 2019, 47 (11) : 5973 - 5987
  • [25] Dynamic Interaction of Eukaryotic Initiation Factor 4G1 (eIF4G1) with eIF4E and eIF1 Underlies Scanning-Dependent and -Independent Translation
    Haimov, Ora
    Sehrawat, Urmila
    Tamarkin-Ben Harush, Ana
    Bahat, Anat
    Uzonyi, Anna
    Will, Alexander
    Hiraishi, Hiroyuki
    Asano, Katsura
    Dikstein, Rivka
    MOLECULAR AND CELLULAR BIOLOGY, 2018, 38 (18)
  • [26] eIF4E phosphorylation by MST1 reduces translation of a subset of mRNAs, but increases lncRNA translation
    Min, Kyung-Won
    Davila, Sylvia
    Zealy, Richard W.
    Lloyd, Lawson T.
    Lee, In Young
    Lee, Rumi
    Roh, Kyung Hye
    Jung, Ahjin
    Jemielity, Jacek
    Choi, Eui-Ju
    Chang, Jeong Ho
    Yoon, Je-Hyun
    BIOCHIMICA ET BIOPHYSICA ACTA-GENE REGULATORY MECHANISMS, 2017, 1860 (07): : 761 - 772
  • [27] Migration and epithelial-to-mesenchymal transition of lung cancer can be targeted via translation initiation factors eIF4E and eIF4GI
    Attar-Schneider, Oshrat
    Drucker, Liat
    Gottfried, Maya
    LABORATORY INVESTIGATION, 2016, 96 (09) : 1004 - 1015
  • [28] Poisson-Boltzmann model analysis of binding mRNA cap analogues to the translation initiation factor eIF4E
    Szklarczyk, Oliwia
    Zuberek, Joanna
    Antosiewicz, Jan M.
    BIOPHYSICAL CHEMISTRY, 2009, 140 (1-3) : 16 - 23
  • [29] Breast cancer cell mesenchymal transition and metastasis directed by DAP5/eIF3d-mediated selective mRNA translation
    Alard, Amandine
    Katsara, Olga
    Rios-Fuller, Tiffany
    de la Parra, Columba
    Ozerdem, Ugur
    Ernlund, Amanda
    Schneider, Robert J.
    CELL REPORTS, 2023, 42 (06):
  • [30] Transforming Growth Factor-β1 Induced Epithelial Mesenchymal Transition is blocked by a chemical antagonist of translation factor eIF4E
    Smith, K. A.
    Zhou, B.
    Avdulov, S.
    Benyumov, A.
    Peterson, M.
    Liu, Y.
    Okon, A.
    Hergert, P.
    Braziunas, J.
    Wagner, C. R.
    Borok, Z.
    Bitterman, P. B.
    SCIENTIFIC REPORTS, 2015, 5