Analyses of zebrafish and Xenopusoocyte maturation reveal conserved and diverged features of translational regulation of maternal cyclin B1 mRNA
© Zhang and Sheets; licensee BioMed Central Ltd. 2009
Received: 19 June 2008
Accepted: 28 January 2009
Published: 28 January 2009
Vertebrate development relies on the regulated translation of stored maternal mRNAs, but how these regulatory mechanisms may have evolved to control translational efficiency of individual mRNAs is poorly understood. We compared the translational regulation and polyadenylation of the cyclin B1 mRNA during zebrafish and Xenopus oocyte maturation. Polyadenylation and translational activation of cyclin B1 mRNA is well characterized during Xenopus oocyte maturation. Specifically, Xenopus cyclin B1 mRNA is polyadenylated and translationally activated during oocyte maturation by proteins that recognize the conserved AAUAAA hexanucleotide and U-rich Cytoplasmic Polyadenylation Elements (CPEs) within cyclin B1 mRNA's 3'UnTranslated Region (3'UTR).
The zebrafish cyclin B1 mRNA was polyadenylated during zebrafish oocyte maturation. Furthermore, the zebrafish cyclin B1 mRNA's 3'UTR was sufficient to stimulate translation of a reporter mRNA during zebrafish oocyte maturation. This stimulation required both AAUAAA and U-rich CPE-like sequences. However, in contrast to AAUAAA, the positions and sequences of the functionally defined CPEs were poorly conserved between Xenopus and zebrafish cyclin B1 mRNA 3'UTRs. To determine whether these differences were relevant to translation efficiency, we analyzed the translational activity of reporter mRNAs containing either the zebrafish or Xenopus cyclin B1 mRNA 3'UTRs during both zebrafish and Xenopus oocyte maturation. The zebrafish cyclin B1 3'UTR was quantitatively less effective at stimulating polyadenylation and translation compared to the Xenopus cyclin B1 3'UTR during both zebrafish and Xenopus oocyte maturation.
Although the factors that regulate translation of maternal mRNAs are highly conserved, the target sequences and overall sequence architecture within the 3'UTR of the cyclin B1 mRNA have diverged to affect translational efficiency, perhaps to optimize levels of cyclin B1 protein required by these different species during their earliest embryonic cell divisions.
In metazoans, early embryonic development is governed entirely by post-transcriptional mechanisms [1, 2]. During this period of development translational mechanisms dictate when and how efficiently each maternal mRNA is translated into protein [3, 4]. Many insights into these mechanisms come from studies of oocytes and eggs from the frog Xenopus laevis. For example, mechanisms that control maternal mRNA translation during Xenopus oocyte maturation are well studied and involve the regulated addition of 3' poly (A) to stored mRNAs [5, 6]. It is unclear, however, how conserved these mechanisms are at the level of individual mRNAs. An understanding of such conservation should provide insights into how differences in target mRNA sequences could affect translational regulation during maternally controlled development.
The specificity of maturation-specific polyadenylation of maternal mRNAs during Xenopus oocyte maturation is controlled by sequences within the 3'UTRs of these mRNAs called cytoplasmic polyadenylation elements (CPEs). CPEs are binding sites for CPEB (CPE binding protein) [6–9]. In Xenopus oocytes CPEB binds other proteins, such as maskin that repress the translation of CPE-containing mRNAs . During oocyte maturation CPEB phosphorylation stimulates its association with proteins that promote mRNA polyadenylation and translation [10–12]. CPEB is highly conserved in vertebrates, suggesting that CPE-regulated polyadenylation and translational activation during development is a highly conserved mechanism. In addition, recent studies have reported that some Xenopus maternal mRNAs contain polyadenylation response elements (PRE) that direct CPEB independent polyadenylation [13, 14], but it is unclear whether PRE type polyadenylation occurs in organisms other than Xenopus . Therefore, aside from studies in Xenopus, the mechanisms that control mRNA polyadenylation and translation during development in other vertebrate organisms have not been explored.
In this report we examine translational regulation of the maternal cyclin B1 mRNA during zebrafish oocyte maturation. Zebrafish oocytes, eggs and embryos offer many advantages for studying the maternal stages of vertebrate development. For example, maternal genes that regulate development have been identified in genetic screens [16–18], and the proteins encoded by these genes have provided insights into early vertebrate embryogenesis [19–21]. However, the mechanisms that govern maternal gene expression in zebrafish oocytes, eggs and embryos have not been explored. We chose to focus on cyclin B1 mRNA because its regulated polyadenylation and translation have been studied extensively during Xenopus oocyte maturation, and CPE-regulated translation is best characterized during this process. Using microinjection of reporter mRNAs into both zebrafish and Xenopus oocytes, we found that although translational regulation of both species' cyclin B1 mRNA was qualitatively similar, it differed quantitatively in terms of efficiency of both polyadenylation and translation. These quantitative differences were likely due distinctions between the 3'UTRs of zebrafish and Xenopus cyclin B1 mRNAs. These findings suggest that CPE-sequences and/or other aspects of 3'UTR sequence architecture evolved between species to modulate translational efficiency of maternal mRNAs, even those mRNAs that encode highly conserved proteins.
Zebrafish cyclin B1 mRNA was polyadenylated during oocyte maturation and early embryogenesis
Polyadenylation of the zebrafish cyclin B1 mRNA depended upon U-rich 3'UTR sequences
To help define putative CPEs in the zebrafish cyclin B1 3'UTR, we compared the cyclin B1 mRNA 3'UTRs from zebrafish and Xenopus. Although cyclin B1 protein is highly conserved, the cyclin B1 mRNA's 3'UTRs exhibit very limited sequence identity (data not shown). Nevertheless, the zebrafish cyclin B1 3'UTR contains two sequences of four contiguous U nucleotides positioned immediately 3' to AAUAAA. These characteristics, U-rich sequences close to AAUAAA are hallmarks of CPEs found in the Xenopus cyclin B1 3'UTR (Fig. 2B). There is another U-rich sequence (UUUUAAU, position -66/-60), but since CPE function decreases significantly as the distance from the AAUAAA sequence increases  we focused on potential U-rich sequences closest to the hexanucleotide. To test whether the U-rich sequences in the zebrafish cyclin B1 3'UTR functioned as CPEs, two radiolabeled 3'UTR RNAs (referred to as WT and CPE-MUT) were generated. The WT RNA contained the wild type 3'UTR and the CPE-Mut RNA contained UU to CG substitutions within each of the two putative CPEs in the zebrafish cyclin B1 3'UTR (Fig. 2A). Both radiolabeled RNAs were injected into zebrafish oocytes and a fraction of injected oocytes were exposed to 7α, 20β-dihydroxyprogesterone to induce maturation, while the remaining fraction was left untreated. Oocyte maturation was monitored based on translucence, a defining characteristic of mature zebrafish oocytes (Fig. 2C). After maturation was complete, RNA was isolated from injected oocytes and analyzed by denaturing gel electrophoresis. A portion of the injected WT cyclin B1 3'UTR RNA increased in size during oocyte maturation (Fig. 2D, lanes 2 and 3) due to the addition of a poly (A) as treatment with oligo-dT/RNaseH converted the high molecular weight species to the size of the injected RNA (Fig. 2D, lane 4). In contrast, the CPE-MUT cyclin B1 3'UTR RNA was not polyadenylated during oocyte maturation (Fig. 2D, lane 5–7). These results suggested that the zebrafish cyclin B1 3'UTR contained U-rich CPEs required for polyadenylation during oocyte maturation.
The zebrafish cyclin B1 mRNA 3'UTR was sufficient to activate translation during oocyte maturation in a CPE- and AAUAAA-dependent manner
To test whether the same sequences required for zebrafish cyclin B1 mRNA polyadenylation (Fig. 2) were also required for translational activation, luciferase reporter mRNAs were generated that contained the zebrafish cyclin B1 3'UTRs in which the two CPE (luc-ZF-cyclin B1-CPE-Mut) or the AAUAAA (luc-ZF-cyclin B1-AAUAAA-Mut) sequences were mutated (Fig. 3A and see Fig. 2A for specific mutations). Translational activity of these mutant reporter mRNAs was compared to the wild type reporter in zebrafish oocyte microinjection experiments as described above. Mutation of either the CPE sequences (luc-ZF-cyclin B1-CPE-Mut) or the AAUAAA (luc-ZF-cyclin B1-AAUAAA-Mut) that abolished zebrafish cyclin B1 mRNA polyadenylation (Fig. 2) significantly reduced the ability of the zebrafish cyclin B1 mRNA's 3'UTR to stimulate translation of the luciferase reporter mRNA during oocyte maturation (Fig. 3B). RT-PCR analysis demonstrated that the injected wild type, CPE-mutant and AAUAAA mutant reporter mRNAs were equally stable in mature and non-mature oocytes (Fig. 3C). Therefore, the zebrafish cyclin B1 3'UTR can activate mRNA translation during oocyte maturation and this activation depends upon the same CPE and AAUAAA sequences required for maturation-specific polyadenylation.
To directly assess the role of the poly (A) tail on translation in zebrafish oocytes, translation of two additional luciferase reporter mRNAs was measured in zebrafish oocytes. These reporters were identical except for the presence of a fifty-nucleotide 3' poly (A) tail. (Fig. 3A) [24, 30]. Equal amounts of each mRNA were injected into separate groups of oocytes. The injected oocytes were cultured for six hours (these oocytes were not induced to mature) and then extracts prepared from these oocytes were assayed for luciferase activity. Translation of the reporter mRNA containing the poly (A) tail (LucA50) was significantly higher than that of the reporter mRNA lacking a poly (A) tail (Luc), indicating that presence of a poly (A) tail was sufficient to stimulate mRNA translation in zebrafish oocytes (Fig. 3D). Therefore, 3' poly (A) is sufficient to enhance translation in zebrafish oocytes.
The zebrafish cyclin B1 3'UTR was less efficiently polyadenylated and less effective at enhancing translation during either zebrafish or Xenopus oocytematuration
We also tested whether the two different cyclin B1 mRNA 3'UTRs provided different levels of translational activation to a luciferase reporter mRNA during either Xenopus or zebrafish oocyte maturation. The Xenopus cyclin B1 3'UTR enhanced translation of the luciferase reporter mRNA more effectively than the zebrafish cyclin B1 3'UTR regardless of which species' oocytes were used for the experiment (Figs. 4C and 4D, compare zebrafish WT and Xenopus WT in both C and D). During oocyte maturation in both species, translational stimulation was due to the same sequences within the 3'UTRs required for polyadenylation (Figs. 4C and 4D, compare AAUAAA-mut and CPE-mut to WT). With the CPE-mut reporter RNA a small amount of stimulation was still observed raising the possibility of other elements that make detectable, but minimal contributions to translation (Figs. 4C and 4D). Together these results indicate that differences in translational efficiency of cyclin B1 mRNA were due to sequence differences between the zebrafish and Xenopus cyclin B1 3'UTRs.
In this report, we examined the underlying mechanisms required for the translational activation of the zebrafish cyclin B1 mRNA during zebrafish oocyte maturation. As expected based on extensive studies in Xenopus, the zebrafish cyclin B1 was polyadenylated during maturation, coincident with its translational activation . In addition the 3'UTR of this mRNA was sufficient to activate translation of a luciferase reporter mRNA microinjected into zebrafish oocytes induced to mature in vitro. Both polyadenylation and translational activation of relevant zebrafish cyclin B1 mRNAs required AAUAAA and CPE-like sequences. These data together with the analysis of cyclin B1 in mouse  revealed that the fundamental mechanisms underlying translational activation of the cyclin B1 mRNA in vertebrate organisms are conserved. However, despite this conservation, we found that the efficiency by which the highly conserved cyclin B1 mRNA was polyadenylated and translated during Xenopus and zebrafish oocyte maturation differed substantially between these two species. These differences were likely not due to differences in the polyadenylation and translational machinery between these two species oocytes, but rather to differences in the 3'UTRs of their respective cyclin B1 mRNAs. Thus, variations in 3'UTR sequences and architecture may contribute to controlling different species' needs for translational efficiency of individual mRNAs while relying on the same highly conserved protein components.
CPE-recognition by CPEB and the zorba protein
The CPEB binds to CPE sequences in the 3'UTRs of Xenopus mRNAs to provide specificity for maturation-specific poly (A) addition for many maternal mRNAs . CPEB proteins bind CPEs via the RRM and zinc finger domains found at their C-termini [8, 32]. The zebrafish ortholog of CPEB is called zorba . The cyclin B1 3'UTRs from zebrafish and Xenopus activate mRNA translation during oocyte maturation in both their normal and heterologous contexts, suggesting that the Xenopus CPEB and zebrafish zorba proteins recognize the same RNA sequences to direct polyadenylation. The amino acid sequences of the Xenopus CPEB and zorba protein share 61% identity over the entire protein and 91% identity over the RRM and zinc finger domains . This high degree of conservation is entirely consistent with the functional comparison of the Xenopus and zebrafish cyclin B1 3'UTRs during both species' oocyte maturation processes reported here. The UUUUAAAG and UUUU sequences identified in the ZF cyclin B1 3' UTR suggest variant non-consensus CPEs, although we have not yet tested direct interaction with either CPEB or Zorba.
Structural and functional differences in the 3'UTRs of the cyclin B1 mRNAs
Our data strongly suggest that the fundamental mechanisms underlying translational activation of the cyclin B1 mRNA in vertebrate organisms are conserved. However, despite this conservation, we found that the efficiency by which the highly conserved cyclin B1 mRNA was polyadenylated and translated during Xenopus and zebrafish oocyte maturation differed substantially between these two species. These differences were not due to differences in the polyadenylation and translational machinery between these two species oocytes, but could be attributed to the distinct 3'UTR elements of the respective cyclin B1 mRNAs. Thus, variations in 3'UTR sequences and architecture may contribute to controlling different species' needs for translational efficiency of individual mRNAs while relying on the same highly conserved trans-acting machinery.
Zebrafish mRNA 3'UTRs were generated by RT-PCR using total RNA extracted from early stage zebrafish embryos. cDNAs were synthesized using reverse transcriptase with either oligo dT 15 primer or a gene-specific reverse primer. The subsequent PCRs were performed with Tth DNA Polymerase. The following PCR primers were used for different 3'UTRs: zebrafish cyclin B1 (Accession NM_131513) forward primer 5'-TTATGCTGAAGAGACTTAACGACTGTGTGC-3', reverse primer 5'-CATGGATCCAAAACTTTAAAAAGTTTATTTGAATTCAAATGTACAAACTTGC-3'; zebrafish bactin2 (Accession BC045879) forward primer 5'-CGGACTGTTACCACTTCACGCCG-3', reverse primer 5'TGGATCCAGGATGTCTTACATGTGCAC-3'. PCR products for these wt 3'UTRs were ligated into pSTBlue-1 vector. Zebrafish cyclin B1 AAUAAA mutant and CPE mutant 3'UTRs were generated by PCR mutagenesis. To generate luciferase reporter plasmids, the BamH1 fragments of these 3'UTRs-containing pSTBlue1 plasmids were cloned into BamHI/BglII sites of pT7Luc vector .
The Xenopus cyclinB1 CPE-mutant 3'UTR was derived by PCR mutagenesis. The PCR product was digested with BamHI, ligated into the BglII/BamHI sites of pT7Luc vector. To generate pSTBlue-Xen cyclinB1 3'UTR CPE mutant plasmid, the above PCR product was BamHI digested, blunted and ligated into pSTBlue-1 vector. pT7Luc/A50, pGEM3Z/Xen CyclinB1-WT 3'UTR and pT7Luc/Xen CyclinB1 WT 3'UTR plasmids are as described .
Luciferase Reporter mRNAs Synthesis
To prepare transcription templates for synthesizing luciferase reporter mRNAs, pT7Luc plasmids containing different 3'UTRs were linearized with BamHI, pT7Luc vector alone was linearized with BglII, pT7Luc/A50 was linearized with DraI. Linearized templates were transcribed in vitro using T7 RNA polymerase .
Cell extracts were prepared from 10–20 oocytes, eggs or embryos by homogenization in 1× cell culture lysis reagent (50 μl/frog oocyte, 20 μl/zebrafish oocyte) and centrifuged at 10000 g, 4°C for 10 min. The clear supernatant was analyzed in a luminometer following the addition of luciferase assay reagent.
Total RNA was extracted from luciferase reporter injected zebrafish oocytes as described previously for Xenopus oocytes . RNA integrity was checked by agarose gel electrophoresis and the concentration determined by UV spectrophotometer. Total RNA from 1 oocyte was used to synthesize cDNAs and perform subsequent PCRs. The following primers were used for luciferase gene: forward primer 5'- GCTGTTTTTACGATCCCTTCAGG -3', reverse primer 5'-CGGTC AACTATG AAGAAGTGTTCG- 3' (498 nt product).
Collection of Oocytes, Eggs and Embryos
Ovaries from anaesthetized female zebrafish were immersed in 60% L-15 medium (Gibco), and single fully grown oocytes isolated and cultured at 26°C. After 1 h of culture, damaged oocytes were discarded. Xenopus oocytes, eggs and embryos were collected as previously described .
Microinjection and Oocyte Maturation
Zebrafish oocytes were injected with luciferase reporter RNAs in a volume of 1 nL (0.017 fmol) per oocyte. After 1 h of culture, some injected oocytes were cultured in 60% L-15 medium with 10 μg/ml 17α, 20β-dihydroxy-4-pregnen-3-one (Sigma) at 26°C for 4–6 h. Oocytes that became translucent after this treatment were harvested as mature oocytes. Xenopus oocytes were injected with 10 nL (0.5 fmol) RNA per oocyte and incubated at room temperature for 1–2 hours. Some of the injected oocytes were matured into eggs by treatment with progesterone (10 μg/ml) overnight at 18°C and matured oocytes were collected for analysis.
RNaseH Treatment/RNA Blot Analysis
Total RNA was isolated from 10–20 zebrafish oocytes, matured oocytes or embryos using Trizol Reagent. Total RNA (10 ug combined with 1 mM EDTA in 20 μl volume) was heated at 100°C for one minute, chilled on ice and incubated for 10 min at room temperature with 1 μg of DNA oligonucleotide (5'-CCAGCTCATCTTCAGTGTAGCC-3') complimentary to positions -393 to -372 of the zebrafish cyclin B1 mRNA's 3'UTR (the poly (A) addition site is +1). To remove poly (A), 1 μg of oligo dT15 was added to each reaction. RNaseH treatments and product analysis using high resolution blot hybridization was performed as described . The blots were hybridized with a radiolabeled probe generated from the zebrafish cyclin B1 3'UTR.
Synthesis and Analysis of P32Labeled 3'UTRs
Plasmids pGEM3Z/Xenopus cyclinB1 WT 3'UTR, pSTBlue-1/Xenopus cyclinB1 3'UTR CPE mutant, pSTBlue-1/zebrafish cyclinB1 WT 3'UTR, pSTBlue-1/zebrafish cyclinB1 3'UTR CPE mutant were linearized by digestion with XbaI, SalI, SalI, SalI respectively. P32 labeled 3'UTRs were generated by in vitro transcription as previously described . The zf-WT and zf-CPE cyclin B1 3'UTR RNAs were 274 nucleotides in length. The Xen-WT and Xen-CPE cyclin B1 3'UTRs were 105 and 202 nucleotides in length respectively. The additional length of the Xen-CPE RNA is due to vector sequences. 20 nl of radiolabeled RNA was injected per Xenopus oocyte and 1 nl injected per zebrafish oocyte. RNAs from injected oocytes and mature oocytes were isolated and analyzed by 4% denaturing PAGE as previously described .
We thank Meg Miller, Ralph Dosch, Francisco Pelegri and his colleagues for assistance and advice on zebrafish. We thank Catherine Fox for her comments on the manuscript. This work was supported by grants from the NIH HD43996 and the James and Dorothy Shaw Fund of the Greater Milwaukee Foundation to M.D.S.
- Kuersten S, Goodwin EB: The power of the 3'UTR: translational control and development. Nat Rev Genet. 2003, 4: 626-637. 10.1038/nrg1125.View ArticlePubMedGoogle Scholar
- Vardy L, Orr-Weaver TL: Regulating translation of maternal messages: multiple repression mechanisms. Trends Cell Biol. 2007, 17: 547-554. 10.1016/j.tcb.2007.09.002.View ArticlePubMedGoogle Scholar
- Colegrove-Otero LJ, Minshall N, Standart N: RNA-binding proteins in early development. Critical Reviews in Biochemistry & Molecular Biology. 2005, 40: 21-73. 10.1080/10409230590918612.View ArticleGoogle Scholar
- Vasudevan S, Seli E, Steitz JA: Metazoan oocyte and early embryo development program: a progression through translation regulatory cascades. Genes Dev. 2006, 20: 138-146. 10.1101/gad.1398906.View ArticlePubMedGoogle Scholar
- de Moor CH, Meijer H, Lissenden S: Mechanisms of translational control by the 3'UTR in development and differentiation. Semin Cell Dev Biol. 2005, 16: 49-58. 10.1016/j.semcdb.2004.11.007.View ArticlePubMedGoogle Scholar
- Mendez R, Richter JD: Translational control by CPEB: A means to the end [Review]. Nature Reviews Molecular Cell Biology. 2001, 2: 521-529. 10.1038/35080081.View ArticlePubMedGoogle Scholar
- Fox CA, Sheets MD, Wickens MP: Poly(A) addition during maturation of frog oocytes: distinct nuclear and cytoplasmic activities and regulation by the sequence UUUUUAU. Genes & Development. 1989, 3: 2151-2162. 10.1101/gad.3.12b.2151.View ArticleGoogle Scholar
- Hake LE, Richter JD: CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell. 1994, 79: 617-627. 10.1016/0092-8674(94)90547-9.View ArticlePubMedGoogle Scholar
- McGrew LL, Dworkin-Rastl E, Dworkin MB, Richter JD: Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. Genes & Development. 1989, 3: 803-815. 10.1101/gad.3.6.803.View ArticleGoogle Scholar
- Stebbins-Boaz B, Cao Q, de Moor CH, Mendez R, Richter JD: Maskin is a CPEB-associated factor that transiently interacts with elF-4E [published erratum appears in Mol Cell 2000 Apr;5(4):following 766]. Molecular Cell. 1999, 4: 1017-1027. 10.1016/S1097-2765(00)80230-0.View ArticlePubMedGoogle Scholar
- Mendez R, Murthy KGK, Ryan K, Manley JL, Richter JD: Phosphorylation of CPEB by Eg2 mediates the recruitment of CPSF into an active cytoplasmic polyadenylation complex. Molecular Cell. 2000, 6: 1253-1259. 10.1016/S1097-2765(00)00121-0.View ArticlePubMedGoogle Scholar
- Barnard DC, Ryan K, Manley JL, Richter JD: Symplekin and xGLD-2 are required for CPEB-mediated cytoplasmic polyadenylation. Cell. 2004, 119: 641-651. 10.1016/j.cell.2004.10.029.View ArticlePubMedGoogle Scholar
- Charlesworth A, Ridge JA, King LA, MacNicol MC, MacNicol AM: A novel regulatory element determines the timing of Mos mRNA translation during Xenopus oocyte maturation. Embo J. 2002, 21: 2798-2806. 10.1093/emboj/21.11.2798.PubMed CentralView ArticlePubMedGoogle Scholar
- Charlesworth A, Cox LL, MacNicol AM: Cytoplasmic polyadenylation element (CPE)- and CPE-binding protein (CPEB)-independent mechanisms regulate early class maternal mRNA translational activation in Xenopus oocytes. J Biol Chem. 2004, 279: 17650-17659. 10.1074/jbc.M313837200.PubMed CentralView ArticlePubMedGoogle Scholar
- Prasad CK, Mahadevan M, MacNicol MC, MacNicol AM: Mos 3'UTR regulatory differences underlie species-specific temporal patterns of Mos mRNA cytoplasmic polyadenylation and translational recruitment during oocyte maturation. Mol Reprod Dev. 2008, 75: 1258-1268. 10.1002/mrd.20877.PubMed CentralView ArticlePubMedGoogle Scholar
- Dosch R, Wagner DS, Mintzer KA, Runke G, Wiemelt AP, Mullins MC: Maternal control of vertebrate development before the midblastula transition: mutants from the zebrafish I. Dev Cell. 2004, 6: 771-780. 10.1016/j.devcel.2004.05.002.View ArticlePubMedGoogle Scholar
- Tribulo C, Aybar MJ, Nguyen VH, Mullins MC, Mayor R: Regulation of Msx genes by a Bmp gradient is essential for neural crest specification. Development. 2003, 130: 6441-6452. 10.1242/dev.00878.View ArticlePubMedGoogle Scholar
- Pelegri F: Maternal factors in zebrafish development. Developmental Dynamics. 2003, 228: 535-554. 10.1002/dvdy.10390.View ArticlePubMedGoogle Scholar
- Connors SA, Tucker JA, Mullins MC: Temporal and spatial action of tolloid (mini fin) and chordin to pattern tail tissues. Dev Biol. 2006, 293: 191-202. 10.1016/j.ydbio.2006.01.029.View ArticlePubMedGoogle Scholar
- Lyman Gingerich J, Westfall TA, Slusarski DC, Pelegri F: hecate, a zebrafish maternal effect gene, affects dorsal organizer induction and intracellular calcium transient frequency. Dev Biol. 2005, 286: 427-439. 10.1016/j.ydbio.2005.07.031.View ArticlePubMedGoogle Scholar
- Yabe T, Ge X, Pelegri F: The zebrafish maternal-effect gene cellular atoll encodes the centriolar component sas-6 and defects in its paternal function promote whole genome duplication. Dev Biol. 2007, 312: 44-60. 10.1016/j.ydbio.2007.08.054.PubMed CentralView ArticlePubMedGoogle Scholar
- Kondo T, Yanagawa T, Yoshida N, Yamashita M: Introduction of cyclin B induces activation of the maturation-promoting factor and breakdown of germinal vesicle in growing zebrafish oocytes unresponsive to the maturation-inducing hormone. Dev Biol. 1997, 190: 142-152. 10.1006/dbio.1997.8673.View ArticlePubMedGoogle Scholar
- Kondo T, Kotani T, Yamashita M: Dispersion of cyclin B mRNA aggregation is coupled with translational activation of the mRNA during zebrafish oocyte maturation. Dev Biol. 2001, 229: 421-431. 10.1006/dbio.2000.9990.View ArticlePubMedGoogle Scholar
- Sheets MD, Fox CA, Hunt T, Woude Vande G, Wickens M: The 3'-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes & Development. 1994, 8: 926-938. 10.1101/gad.8.8.926.View ArticleGoogle Scholar
- Fox CA, Sheets MD, Wahle E, Wickens M: Polyadenylation of maternal mRNA during oocyte maturation: poly(A) addition in vitro requires a regulated RNA binding activity and a poly(A) polymerase. Embo J. 1992, 11: 5021-5032.PubMed CentralPubMedGoogle Scholar
- Pique M, Lopez JM, Foissac S, Guigo R, Mendez R: A combinatorial code for CPE-mediated translational control. Cell. 2008, 132: 434-448. 10.1016/j.cell.2007.12.038.View ArticlePubMedGoogle Scholar
- Colgan DF, Manley JL: Mechanism and regulation of mRNA polyadenylation. Genes Dev. 1997, 11: 2755-2766. 10.1101/gad.11.21.2755.View ArticlePubMedGoogle Scholar
- Danckwardt S, Hentze MW, Kulozik AE: 3' end mRNA processing: molecular mechanisms and implications for health and disease. Embo J. 2008, 27: 482-498. 10.1038/sj.emboj.7601932.PubMed CentralView ArticlePubMedGoogle Scholar
- Barkoff AF, Dickson KS, Gray NK, Wickens M: Translational control of cyclin B1 mRNA during meiotic maturation: coordinated repression and cytoplasmic polyadenylation. Developmental Biology. 2000, 220: 97-109. 10.1006/dbio.2000.9613.View ArticlePubMedGoogle Scholar
- Gallie DR: The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev. 1991, 5: 2108-2116. 10.1101/gad.5.11.2108.View ArticlePubMedGoogle Scholar
- Tay J, Hodgman R, Richter JD: The control of cyclin B1 mRNA translation during mouse oocyte maturation. Dev Biol. 2000, 221: 1-9. 10.1006/dbio.2000.9669.View ArticlePubMedGoogle Scholar
- Hake LE, Mendez R, Richter JD: Specificity of RNA binding by CPEB: requirement for RNA recognition motifs and a novel zinc finger. Mol Cell Biol. 1998, 18: 685-693.PubMed CentralView ArticlePubMedGoogle Scholar
- Bally-Cuif L, Schatz WJ, Ho RK: Characterization of the zebrafish Orb/CPEB-related RNA binding protein and localization of maternal components in the zebrafish oocyte. Mech Dev. 1998, 77: 31-47. 10.1016/S0925-4773(98)00109-9.View ArticlePubMedGoogle Scholar
- Nakahata S, Kotani T, Mita K, Kawasaki T, Katsu Y, Nagahama Y, Yamashita M: Involvement of Xenopus Pumilio in the translational regulation that is specific to cyclin B1 mRNA during oocyte maturation. Mech Dev. 2003, 120: 865-880. 10.1016/S0925-4773(03)00160-6.View ArticlePubMedGoogle Scholar
- Nakahata S, Katsu Y, Mita K, Inoue K, Nagahama Y, Yamashita M: Biochemical identification of Xenopus pumilio as a sequence-specific cyclin B1 mRNA-binding protein that physically interacts with a nanos homolog, Xcat-2, and a cytoplasmic polyadenylation element-binding protein. Journal of Biological Chemistry. 2001, 276: 20945-20953. 10.1074/jbc.M010528200.View ArticlePubMedGoogle Scholar
- Fritz BR, Sheets MD: Regulation of the mRNAs encoding proteins of the BMP signaling pathway during the maternal stages of Xenopus development. Developmental Biology. 2001, 236: 230-243. 10.1006/dbio.2001.0324.View ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.