DOI: 10.1101/gad.8.8.926. The 3'-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation.

The 3'-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation.

10.1101/gad.8.8.926

Crossref journal-article

Cold Spring Harbor Laboratory

Genes & Development (246)

Abstract

Early in the development of many animals, before transcription begins, any change in the pattern of protein synthesis is attributable to a change in the translational activity or stability of an mRNA in the egg. As a result, translational control is critical for a variety of developmental decisions, including axis formation in Drosophila and sex determination in Caenorhabditis elegans. Previous work demonstrated that increases in poly(A) length can activate translation, whereas removal of poly(A) can prevent it. In this report we focus on the control of c-mos and cyclin A1, B1, and B2 mRNAs during meiotic maturation and after fertilization of frog eggs. We show that addition and removal of poly(A) from these mRNAs is extensively regulated: The time at which each mRNA receives or loses poly(A), as well as the number of adenosines it gains or loses, differ substantially. Signals in the 3'-untranslated region (UTR) of each mRNA are sufficient to reconstitute both the temporal and quantitative control of poly(A) addition: Chimeric mRNAs in which a luciferase-coding region is joined to the 3' UTRs of cyclin A1, cyclin B1, or c-mos mRNA, receive poly(A) of the same length and at the same time as do the endogenous mRNAs. Moreover, each 3' UTR also regulates translation of the chimeric mRNAs, determining when and how much translation of the luciferase reporter is stimulated during maturation. The magnitude of stimulation in luciferase activity varies from 5- to 100-fold, depending on the 3' UTR. Translational stimulation by each 3' UTR requires poly(A) lengthening, as it is prevented by mutations that prevent that process. These results suggest that the 3' UTRs of cyclin and c-mos mRNAs control not only whether or not an mRNA is turned on during maturation, but when that activation occurs and to what extent. Translational control of c-mos mRNA, which may be achieved through regulation of poly(A) length, may be critical in the activation of maturation, and in the onset of cleavage divisions. Our findings, as well as those of others, suggest that even quite complex patterns of translational activation in the early embryo can be attained through the differential control of a common mechanism.

Bibliography

Sheets, M. D., Fox, C. A., Hunt, T., Vande Woude, G., & Wickens, M. (1994). The 3â-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes & Development, 8(8), 926â938.

Authors 5

M D Sheets (first)
C A Fox (additional)
T Hunt (additional)
G Vande Woude (additional)
M Wickens (additional)

References 44 Referenced 271

10.1038/349346a0
{'key': '2021111418142098000_8.8.926.2', 'first-page': '1697', 'article-title': 'Poly(A) shortening and degradation of the A + U-rich sequences of human c-myc mRNA in a cell free system.', 'volume': '8', 'year': '1988', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Poly(A) shortening and degradation of the A + U-rich sequences of human c-myc mRNA in a cell free system. (1988)
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Maniatis, T., E.F. Fritsch, and J. Sambrook. 1982. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
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{'key': '2021111418142098000_8.8.926.25', 'first-page': '3441', 'article-title': 'mRNA poly(A) tail, a 3â\x80² enhancer of translation.', 'volume': '10', 'year': '1990', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / mRNA poly(A) tail, a 3â² enhancer of translation. (1990)
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{'key': '2021111418142098000_8.8.926.29', 'first-page': '5634', 'article-title': 'Maturation-specific polyadenylation and translational control: Diversity of cytoplasmic polyadenylation elements, influence of poly(A) tail size, and formation of stable polyadenylation complexes.', 'volume': '10', 'year': '1990', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Maturation-specific polyadenylation and translational control: Diversity of cytoplasmic polyadenylation elements, influence of poly(A) tail size, and formation of stable polyadenylation complexes. (1990)
10.1016/0378-1119(88)90139-4
{'key': '2021111418142098000_8.8.926.31', 'first-page': '519', 'article-title': 'Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes.', 'volume': '338', 'year': '1988', 'journal-title': 'Nature'} / Nature / Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. (1988)
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{'key': '2021111418142098000_8.8.926.43', 'first-page': '399', 'article-title': 'Forward, backward, how much, when: Mechanisms of poly(A) addition and removal and their role in early development.', 'volume': '3', 'year': '1992', 'journal-title': 'Sem. Dev. Biol.'} / Sem. Dev. Biol. / Forward, backward, how much, when: Mechanisms of poly(A) addition and removal and their role in early development. (1992)
10.1126/science.6208611

Dates

Type	When
Created	18 years, 2 months ago (June 5, 2007, 5:15 p.m.)
Deposited	3 years, 9 months ago (Nov. 14, 2021, 9:19 p.m.)
Indexed	3 weeks, 5 days ago (Aug. 7, 2025, 4:56 a.m.)
Issued	31 years, 4 months ago (April 15, 1994)
Published	31 years, 4 months ago (April 15, 1994)
Published Online	31 years, 4 months ago (April 15, 1994)
Published Print	31 years, 4 months ago (April 15, 1994)

Funders 0

None

BibTeX

@article{Sheets_1994, title={The 3’-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation.}, volume={8}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.8.8.926}, DOI={10.1101/gad.8.8.926}, number={8}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Sheets, M D and Fox, C A and Hunt, T and Vande Woude, G and Wickens, M}, year={1994}, month=apr, pages={926–938} }

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