Translational inactivation of ribosomal protein mRNAs during Xenopus oocyte maturation.

Abstract

Ribosomal protein synthesis ceases upon maturation of Xenopus oocytes. We find that this cessation results from the dissociation of ribosomal protein mRNAs from polysomes and is accompanied by the deadenylation of these transcripts. A synthetic mRNA encoding ribosomal protein LI, microinjected into stage VI oocytes, is deadenylated and released from polysomes upon maturation. Our results indicate that sequences located within 387 bp of the 3' terminus of LI mRNA direct both the deadenylation and polysomal release of this ribosomal protein mRNA. The proper translational regulation of an exogenous ribosomal protein mRNA in microinjected oocytes provides a basis for determining the sequence specificity for the differential utilization of maternal mRNAs during oocyte maturation. The synthesis of ribosomal proteins during Xenopus oo genesis contributes to the production of a maternal ribosome pool that is sufficient to support protein synthesis throughout embryogenesis. This elevated accumulation of ribosomal proteins is due largely to the preferential translation of ribosomal protein mRNAs (rp-mRNAs) in vitellogenic stage III oocytes w^hen ribosomal proteins comprise -20% of total protein synthesis (Dixon and Ford 1982;Baum and Wormington 1985; CardinaH et al. 1987). In contrast, synthesis of the majority of ribosomal proteins during embryogenesis is not observed until de velopment of the tail-bud embryo. Previous studies by Pierandrei-Amaldi and colleagues (1982) and Baum and Wormington (1985) have shoMrn that tv^o principal factors contribute to the absence of ribosomal protein synthesis in early embryonic development. First, ma ternal rp-mRNAs are degraded following fertilization. Second, although zygotic rp-mRNAs begin to accumu late during early gastrulation, these transcripts are ex cluded from polysomes until the tail-bud stage. Thus, the onset of ribosomal protein synthesis in both oo genesis and embryogenesis is regulated by selective rpmRNA utilization.We are interested in determining the mechanisms that direct the transition from active ribosomal protein syn thesis during oogenesis to the translational inactivity and instability of these maternal mRNAs follov^ing fer tilization. The process of oocyte maturation comprises several events likely to participate in the cessation of ribosomal subunit assembly. The induction of matura tion initiates a series of physiological changes, including the resumption of meiosis, breakdown of the nuclear en velope, chromosome condensation, and repression of transcription by all three classes of nuclear RNA poly merase (reviewed in Mailer 1985). The absence of both rp-mRNA and rRNA transcription and precursor rRNA processing (Busby and Reeder 1982), in particular, pre cludes the assembly of ribosomal subunits in mature oo cytes.In this paper we have examined the regulation of ribo somal protein synthesis during oocyte maturation. Our results indicate that the majority of ribosomal proteins are not synthesized in mature oocytes, despite a twofold increase in overall prote...

Cytoplasmic Polyadenylation Element (CPE)- and CPE-binding Protein (CPEB)-independent Mechanisms Regulate Early Class Maternal mRNA Translational Activation in Xenopus Oocytes

“…7B). The ␤-globin 3Ј-UTR is not subject to regulated cytoplasmic polyadenylation during oocyte maturation (9,30,41). When the histone-like B4 and D7 PREs were inserted into the ␤-globin 3Ј-UTR, they directed cytoplasmic polyadenylation in response to progesterone (Fig.…”

Translational control by poly(A) elongation during Xenopus development: differential repression and enhancement by a novel cytoplasmic polyadenylation element.

“…Although it is likely that no single mechanism dictates the timing of polysomal assembly of maternal mRNA during development, growing evidence suggests that at least during oocyte maturation, specific translation is con- trolled by poly(A) elongation and deadenylation. This was suggested initially by studies with marine invertebrates (Rosenthal et al 1983) and subsequently demonstrated in mouse (Vassalli et al 1989) and Xenopus (Hyman and Wormington 1988;McGrew et al 1989;Paris and Richter 1990}. In general, several mRNAs that are translationally dormant in fully grown oocytes contain short poly(A) tails that are elongated in the cytoplasm during maturation.…”

Proteomic approach to understanding the maternal effect in the flesh fly, Sarcophaga bullata (Diptera: Sarcophagidae)

“…In addition, a ribosomal protein is known to be required for oogenesis in Drosophila melanogaster (Qian et al, 1988). Translational inactivation of ribosomal protein mRNAs during oogenesis is reported in vertebrates (Hyman & Wormington, 1988).Thus, the decrease in the abundance of ribosomal protein LP1 in the ovaries of short-day females may also suggest that suppression of this protein might be related to oogenesis in flesh flies.…”