DAZL and CPEB1 regulate mRNA translation synergistically during oocyte maturation

• Published in: Journal of cell science Vol. 129; no. 6; pp. 1271 - 1282
• Main Authors: Sousa Martins, Joao P, Liu, Xueqing, Oke, Ashwini, Arora, Ripla, Franciosi, Federica, Viville, Stephan, Laird, Diana J, Fung, Jennifer C, Conti, Marco
• Format: Journal Article
• Language: English
• Published: England The Company of Biologists Ltd 15.03.2016
• Subjects: Animals; Female; Gene Expression Regulation, Developmental; Life Sciences; Male; Meiosis; Mice, Inbred C57BL; mRNA Cleavage and Polyadenylation Factors - genetics; mRNA Cleavage and Polyadenylation Factors - metabolism; Oocytes - cytology; Oocytes - metabolism; Oogenesis; Protein Biosynthesis; Reproductive Biology; RNA, Messenger - genetics; RNA, Messenger - metabolism; RNA-Binding Proteins - genetics; RNA-Binding Proteins - metabolism; Tools and Techniques; Transcription Factors - genetics; Transcription Factors - metabolism; DAZL; CPEB; RBPs; Translation control; Oocyte maturation
• ISSN: 0021-9533; 1477-9137; 1477-9137
• DOI: 10.1242/jcs.179218

Meiotic progression requires exquisitely coordinated translation of maternal messenger (m)RNA that has accumulated during oocyte growth. A major regulator of this program is the cytoplasmic polyadenylation element binding protein 1 (CPEB1). However, the temporal pattern of translation at different meiotic stages indicates the function of additional RNA binding proteins (RBPs). Here, we report that deleted in azoospermia-like (DAZL) cooperates with CPEB1 to regulate maternal mRNA translation. Using a strategy that monitors ribosome loading onto endogenous mRNAs and a prototypic translation target, we show that ribosome loading is induced in a DAZL- and CPEB1-dependent manner, as the oocyte reenters meiosis. Depletion of the two RBPs from oocytes and mutagenesis of the 3' untranslated regions (UTRs) demonstrate that both RBPs interact with the Tex19.1 3' UTR and cooperate in translation activation of this mRNA. We observed a synergism between DAZL and cytoplasmic polyadenylation elements (CPEs) in the translation pattern of maternal mRNAs when using a genome-wide analysis. Mechanistically, the number of DAZL proteins loaded onto the mRNA and the characteristics of the CPE might define the degree of cooperation between the two RBPs in activating translation and meiotic progression.