Translational control of maternal glp-1 mRNA by POS-1 and its interacting protein SPN-4 in Caenorhabditis elegans

Abstract

The translation of maternal glp-1 mRNAs is regulated temporally and spatially in C. elegans embryos. The 3′ UTR (untranslated region) of the maternal glp-1 mRNA is important for both kinds of regulation. The spatial control region is required to suppress translation in the posterior blastomeres. The temporal one is required to suppress translation in oocytes and one-cell stage embryos. We show that a CCCH zinc-finger protein, POS-1, represses glp-1 mRNA translation by binding to the spatial control region. We identified an RNP-type RNA-binding protein, SPN-4, as a POS-1-interacting protein. SPN-4 is presentdevelopmentally from the oocyte to the early embryo and its distribution overlaps with that of POS-1 in the cytoplasm and P granules of the posterior blastomeres. SPN-4 binds to a subregion of the temporal control region in the 3′ UTR and is required for the translation of glp-1 mRNA in the anterior blastomeres. We propose that the balance between POS-1 and SPN-4 controls the translation of maternal glp-1 mRNA.

An Integrative Approach to Gain Insights into the Cellular Function of Human Ataxin-2

“…17 Interestingly, another C. elegans A2BP1/FOX-1 homolog/paralog is SPN-4/GEI-20 (spindle-orientation defective protein 4/GEX-3 interacting protein 20). This protein plays diverse roles in the translational control of cell-fate specification and patterning the early C. elegans embryo, [65][66][67][68][69] which is consistent with the observed essential role of the C. elegans homolog of ATX2 in embryonic development. 21 Similar to the Lsm12 interacting yeast protein Puf3, whose close yeast homologs Puf1/2 possess one RRM domain, SPN-4 binds the 3 0 UTR of mRNA.…”

“…Therefore, SNP-4 may be part of large complexes and also interacts with several other RNA-binding proteins such as GEX-3, MEX-3, and POS-1 implicated in RNA binding, transcriptional and translational regulation of embryogenesis, tissue morphogenesis, and cell polarity and migration. 22,[65][66][67][68][69][70] Moreover, GEX-3 forms a complex with GEX-2 at cell boundaries in embryos, whose closely related human and fly proteins NAP1 (Nck-associated protein 1) and Kette interact with the Rho-GTPase Rac1 and are required for axonal development and appropriate actin organization like the ATX2 homolog of D. melanogaster. 23,70,71 Overall, a bulk of evidence exists that ATX2 homologs might be involved in RNA splicing, mRNA stabilization or degradation and other essential RNA-processing pathways.…”

Translational Control in the Caenorhabditis elegans Germ Line

“…In oocytes, where GLD-1 is absent, members of the PUF-family, PUF-5 and PUF-6/7, suppress ef fi cient GLP-1 protein synthesis (Lublin and Evans 2007 ) . During early stages of embryogenesis, glp-1 mRNA is subject to POS-1-mediated repression, a maternally provided zinc fi nger-containing protein (Ogura et al 2003 ) . This illustrates nicely that an mRNA can be repressed by different translational regulators at different points during germ cell development.…”

RNA target specificity of the embryonic cell fate determinant POS-1

“…POS-1 is a critical RNA-binding protein required for C. elegans early embryogenesis (Tabara et al 1999;Ogura et al 2003). POS-1 accumulates in the posterior of the fertilized zygote and is inherited asymmetrically at each division ( Fig.…”

“…Three genes have been identified whose expression is perturbed in pos-1 mutants: glp-1, apx-1 (Ogura et al 2003), and nos-2 (D' Agostino et al 2006). nos-2 encodes a protein similar to Drosophila Nanos that is required for germ cell development and migration during gastrulation (Subramaniam and Seydoux 1999).…”