Spatial and temporal translational control of germ cell mRNAs mediated by the eIF4E isoform IFE-1

被引:11
|
作者
Friday, Andrew J. [1 ]
Henderson, Melissa A. [2 ]
Morrison, J. Kaitlin [1 ]
Hoffman, Jenna L. [1 ]
Keiper, Brett D. [1 ]
机构
[1] E Carolina Univ, Brody Sch Med, Dept Biochem & Mol Biol, Greenville, NC 27834 USA
[2] Lincoln Mem Univ, DeBusk Coll Osteopath Med, Dept Mol Sci, Harrogate, TN 37752 USA
基金
美国国家科学基金会;
关键词
mRNA translational control; Oogenesis; C; elegans; Translation state array analysis; TSAA; Protein synthesis; Meiotic maturation; INITIATION-FACTOR; 4E; OOCYTE MEIOTIC MATURATION; CAENORHABDITIS-ELEGANS; C-ELEGANS; DEVELOPMENT DECISION; GENE-EXPRESSION; STEM-CELLS; PROTEIN; REPRESSION; GRANULES;
D O I
10.1242/jcs.172684
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Regulated mRNA translation is vital for germ cells to produce new proteins in the spatial and temporal patterns that drive gamete development. Translational control involves the de-repression of stored mRNAs and their recruitment by eukaryotic initiation factors (eIFs) to ribosomes. C. elegans expresses five eIF4Es (IFE-1-IFE-5); several have been shown to selectively recruit unique pools of mRNA. Individual IFE knockouts yield unique phenotypes due to inefficient translation of certain mRNAs. Here, we identified mRNAs preferentially translated through the germline-specific eIF4E isoform IFE-1. Differential polysome microarray analysis identified 77 mRNAs recruited by IFE-1. Among the IFE-1-dependent mRNAs are several required for late germ cell differentiation and maturation. Polysome association of gld-1, vab-1, vpr-1, rab-7 and rnp-3 mRNAs relies on IFE-1. Live animal imaging showed IFE-1-dependent selectivity in spatial and temporal translation of germline mRNAs. Altered MAPK activation in oocytes suggests dual roles for IFE-1, both promoting and suppressing oocyte maturation at different stages. This single eIF4E isoform exerts positive, selective translational control during germ cell differentiation.
引用
收藏
页码:4487 / 4498
页数:12
相关论文
共 50 条
  • [21] PPM1G dephosphorylates eIF4E in control of mRNA translation and cell proliferation
    Wang, Peng
    Li, Zixian
    Kim, Sung-Hoon
    Xu, Haijin
    Huang, Hao
    Yang, Chutong
    Snape, Abby
    Choi, Jung-Hyun
    Bermudez, Sara
    Boivin, Marie-Noelle
    Ferry, Nicolas
    Karamchandani, Jason
    Nagar, Bhushan
    Sonenberg, Nahum
    LIFE SCIENCE ALLIANCE, 2024, 7 (10)
  • [22] Translational repression by human 4E-BP1 in yeast specifically requires human eIF4E as target
    Hughes, JMX
    Ptushkina, M
    Karim, MM
    Koloteva, N
    von der Haar, T
    McCarthy, JEG
    JOURNAL OF BIOLOGICAL CHEMISTRY, 1999, 274 (06) : 3261 - 3264
  • [23] 4E-BP1/eIF4E Cap Dependent Translational Signaling and Regulation in Lung Mesenchymal Cells
    Lama, V. N.
    Walker, N. M.
    AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE, 2018, 197
  • [24] Regulation of Germ Cell mRNPs by eIF4E:4EIP Complexes: Multiple Mechanisms, One Goal
    Huggins, Hayden P.
    Keiper, Brett D.
    FRONTIERS IN CELL AND DEVELOPMENTAL BIOLOGY, 2020, 8
  • [25] 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
  • [26] Phosphorylation of eIF4E promotes EMT and metastasis via translational control of SNAIL and MMP-3
    Robichaud, N.
    del Rincon, S. V.
    Huor, B.
    Alain, T.
    Petruccelli, L. A.
    Hearnden, J.
    Goncalves, C.
    Grotegut, S.
    Spruck, C. H.
    Furic, L.
    Larsson, O.
    Muller, W. J.
    Miller, W. H.
    Sonenberg, N.
    ONCOGENE, 2015, 34 (16) : 2032 - 2042
  • [27] Phosphorylation of eIF4E promotes EMT and metastasis via translational control of SNAIL and MMP-3
    N Robichaud
    S V del Rincon
    B Huor
    T Alain
    L A Petruccelli
    J Hearnden
    C Goncalves
    S Grotegut
    C H Spruck
    L Furic
    O Larsson
    W J Muller
    W H Miller
    N Sonenberg
    Oncogene, 2015, 34 : 2032 - 2042
  • [28] Murine Norovirus 1 (MNV1) Replication Induces Translational Control of the Host by Regulating eIF4E Activity during Infection
    Royall, Elizabeth
    Doyle, Nicole
    Abdul-Wahab, Azimah
    Emmott, Ed
    Morley, Simon J.
    Goodfellow, Ian
    Roberts, Lisa O.
    Locker, Nicolas
    JOURNAL OF BIOLOGICAL CHEMISTRY, 2015, 290 (08) : 4748 - 4758
  • [29] eIF4E promotes nuclear export of cyclin D1 mRNAs via an element in the 3′ UTR
    Culjkovic, B
    Topisirovic, I
    Skrabanek, L
    Ruiz-Gutierrez, M
    Borden, KLB
    JOURNAL OF CELL BIOLOGY, 2005, 169 (02): : 245 - 256
  • [30] The mRNA 5′ cap-binding protein eIF4E and control of cell growth
    Sonenberg, N
    Gingras, AC
    CURRENT OPINION IN CELL BIOLOGY, 1998, 10 (02) : 268 - 275