Abstract
Early development in Xenopus laevis is programmed in part by maternally inherited mRNAs that are synthesized and stored in the growing oocyte. During oocyte maturation, several of these messages are translationally activated by poly(A) elongation, which in turn is regulated by two cis elements in the 3' untranslated region, the hexanucleotide AAUAAA and a cytoplasmic polyadenylation element (CPE) consisting of UUUUUAU or similar sequence. In the early embryo, a different set of maternal mRNAs is translationally activated. We have shown previously that one of these, C12, requires a CPE consisting of at least 12 uridine residues, in addition to the hexanucleotide, for its cytoplasmic polyadenylation and subsequent translation (R. Simon, J.-P. Tassan, and J.D. Richter, Genes Dev. 6:2580-2591, 1992). To assess whether this embryonic CPE functions in other maternal mRNAs, we have chosen Cl1 RNA, which is known to be polyadenylated during early embryogenesis (J. Paris, B. Osborne, A. Couturier, R. LeGuellec, and M. Philippe, Gene 72:169-176, 1988). Wild-type as well as mutated versions of Cl1 RNA were injected into fertilized eggs and were analyzed for cytoplasmic polyadenylation at times up to the gastrula stage. This RNA also required a poly(U) CPE for cytoplasmic polyadenylation in embryos, but in this case the CPE consisted of 18 uridine residues. In addition, the timing and extent of cytoplasmic poly(A) elongation during early embryogenesis were dependent upon the distance between the CPE and the hexanucleotide. Further, as was the case with Cl2 RNA, Cl1 RNA contains a large masking element that prevents premature cytoplasmic polyadenylation during oocyte maturation. To examine the factors that may be involved in the cytoplasmic polyadenylation of both C12 and C11 RNAs, we performed UV cross-linking experiments in egg extracts. Two proteins with sizes of ~36 and ~45 kDa interacted specifically with the CPEs of both RNAs, although they bound preferentially to the C12 CPE. The role that these proteins might play in cytoplasmic polyadenylation is discussed.
MeSH Terms
Age Factors
Animals
Base Sequence
Cytoplasm/metabolism
Gene Expression Regulation, Developmental
Molecular Sequence Data
Oligodeoxyribonucleotides/chemistry
Oocytes/metabolism
Oogenesis
Poly A/metabolism
Protein Binding
RNA, Messenger/metabolism
RNA-Binding Proteins/metabolism
Regulatory Sequences, Nucleic Acid
Xenopus laevis/embryology
Chemicals
Oligodeoxyribonucleotides
RNA, Messenger
RNA-Binding Proteins
Poly A
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Simon R
Worcester Foundation for Experimental Biology, Shrewsbury, Massachusetts 01545.
Richter J D
References (35)
35 references, click to expand
-
Characterization of a second highly conserved B-type lamin present in cells previously thought to contain only a single B-type lamin.
Chromosoma. 1990 Oct;99(6):379-90
PMID: 2102682
-
Control of the sperm-oocyte switch in Caenorhabditis elegans hermaphrodites by the fem-3 3' untranslated region.
Nature. 1991 Jan 24;349(6307):346-8
PMID: 1702880
-
Maturation-specific polyadenylation: in vitro activation by p34cdc2 and phosphorylation of a 58-kD CPE-binding protein.
Genes Dev. 1991 Sep;5(9):1697-708
PMID: 1653174
-
Activin receptor mRNA is expressed early in Xenopus embryogenesis and the level of the expression affects the body axis formation.
Biochem Biophys Res Commun. 1991 Dec 16;181(2):684-90
PMID: 1661587
-
Identification and characterization of alternatively spliced fibronectin mRNAs expressed in early Xenopus embryos.
Dev Biol. 1992 Feb;149(2):357-69
PMID: 1730390
-
The origin of pattern and polarity in the Drosophila embryo.
Cell. 1992 Jan 24;68(2):201-19
PMID: 1733499
-
The Caenorhabditis elegans sex determining gene fem-3 is regulated post-transcriptionally.
EMBO J. 1992 Jun;11(6):2303-10
PMID: 1376249
-
Isolation of novel murine maternal mRNAs regulated by cytoplasmic polyadenylation.
Genes Dev. 1992 Jul;6(7):1202-12
PMID: 1628827
-
Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos.
Cell. 1992 Sep 4;70(5):829-40
PMID: 1339313
-
Embryonic expression and functional analysis of a Xenopus activin receptor.
Dev Dyn. 1992 May;194(1):1-11
PMID: 1384808
-
Localization of nanos RNA controls embryonic polarity.
Cell. 1992 Oct 16;71(2):301-13
PMID: 1423595
-
In Xenopus laevis, the product of a developmentally regulated mRNA is structurally and functionally homologous to a Saccharomyces cerevisiae protein involved in translation fidelity.
Mol Cell Biol. 1993 May;13(5):2815-21
PMID: 8474443
-
Translational regulation of tra-2 by its 3' untranslated region controls sexual identity in C. elegans.
Cell. 1993 Oct 22;75(2):329-39
PMID: 8402916
-
Translational control by poly(A) elongation during Xenopus development: differential repression and enhancement by a novel cytoplasmic polyadenylation element.
Genes Dev. 1992 Dec;6(12B):2580-91
PMID: 1285126
-
Poly(A) tail metabolism and function in eucaryotes.
J Biol Chem. 1993 Nov 5;268(31):22955-8
PMID: 8226806
-
Xwnt-11: a maternally expressed Xenopus wnt gene.
Development. 1993 Dec;119(4):1161-73
PMID: 8306880
-
Translational control of maternal glp-1 mRNA establishes an asymmetry in the C. elegans embryo.
Cell. 1994 Apr 22;77(2):183-94
PMID: 8168128
-
Translational regulation of nanos by RNA localization.
Nature. 1994 May 26;369(6478):315-8
PMID: 7514276
-
Multiple sequence elements and a maternal mRNA product control cdk2 RNA polyadenylation and translation during early Xenopus development.
Mol Cell Biol. 1994 Sep;14(9):5870-80
PMID: 8065320
-
The 3'-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation.
Genes Dev. 1994 Apr 15;8(8):926-38
PMID: 7926777
-
Temporal and spatial regulation of fibronectin in early Xenopus development.
Cell. 1984 Mar;36(3):729-40
PMID: 6697394
-
Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs.
Nucleic Acids Res. 1984 Sep 25;12(18):7057-70
PMID: 6207484
-
Changes in the polyadenylation of specific stable RNA during the early development of Xenopus laevis.
Gene. 1988 Dec 10;72(1-2):169-76
PMID: 2468559
-
Cyclin synthesis drives the early embryonic cell cycle.
Nature. 1989 May 25;339(6222):275-80
PMID: 2566917
-
Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element.
Genes Dev. 1989 Jun;3(6):803-15
PMID: 2568313
-
Poly(A) addition during maturation of frog oocytes: distinct nuclear and cytoplasmic activities and regulation by the sequence UUUUUAU.
Genes Dev. 1989 Dec;3(12B):2151-62
PMID: 2628165
-
Regulated polyadenylation controls mRNA translation during meiotic maturation of mouse oocytes.
Genes Dev. 1989 Dec;3(12B):2163-71
PMID: 2483395
-
The sequence of TGF-beta 2 from Xenopus laevis.
Nucleic Acids Res. 1990 Apr 25;18(8):2185
PMID: 2336403
-
Poly(A) metabolism and polysomal recruitment of maternal mRNAs during early Xenopus development.
Dev Biol. 1990 Jul;140(1):221-4
PMID: 2358121
-
Xotch, the Xenopus homolog of Drosophila notch.
Science. 1990 Sep 21;249(4975):1438-41
PMID: 2402639
-
Translational control by cytoplasmic polyadenylation during Xenopus oocyte maturation: characterization of cis and trans elements and regulation by cyclin/MPF.
EMBO J. 1990 Nov;9(11):3743-51
PMID: 2145153
-
Nuclear polyadenylation factors recognize cytoplasmic polyadenylation elements.
Genes Dev. 1994 May 1;8(9):1106-16
PMID: 7926790
-
Maturation-specific polyadenylation and translational control: diversity of cytoplasmic polyadenylation elements, influence of poly(A) tail size, and formation of stable polyadenylation complexes.
Mol Cell Biol. 1990 Nov;10(11):5634-45
PMID: 1700272
-
A nervous system-specific isotype of the beta subunit of Na+,K(+)-ATPase expressed during early development of Xenopus laevis.
Proc Natl Acad Sci U S A. 1990 Dec;87(23):9088-92
PMID: 2174552
-
Translational control during early development.
Bioessays. 1991 Apr;13(4):179-83
PMID: 1859396