Abstract
Cytoplasmic polyadenylation of specific mRNAs commonly is correlated with their translational activation during development. Here, we focus on links between cytoplasmic polyadenylation, translational activation and the control of meiotic maturation in Xenopus oocytes. We manipulate endogenous c-mos mRNA, which encodes a protein kinase that regulates meiotic maturation. We determined that translational activation of endogenous c-mos mRNA requires a long poly(A) tail per se, rather than the process of polyadenylation. For this, we injected 'prosthetic' poly(A)_synthetic poly(A) tails designed to attach by base pairing to endogenous c-mos mRNA that has had its own polyadenylation signals removed. This prosthetic poly(A) tail activates c-mos translation and restores meiotic maturation in response to progesterone. Thus the role of polyadenylation in activating c-mos mRNA differs from its role in activating certain other mRNAs, for which the act of polyadenylation is required. In the absence of progesterone, prosthetic poly(A) does not stimulate c-mos expression, implying that progesterone acts at additional steps to elevate c-Mos protein. By using a general inhibitor of polyadenylation together with prosthetic poly(A), we demonstrate that these additional steps include polyadenylation of at least one other mRNA, in addition to that of c-mos mRNA. These other mRNAs, encoding regulators of meiotic maturation, act upstream of c-Mos in the meiotic maturation pathway.
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- Ballantyne S., Bilger A., Astrom J., Virtanen A., Wickens M. Poly (A) polymerases in the nucleus and cytoplasm of frog oocytes: dynamic changes during oocyte maturation and early development. RNA. 1995 Mar;1(1):64–78. [PMC free article] [PubMed] [Google Scholar]
- Ballantyne S., Daniel D. L., Jr, Wickens M. A dependent pathway of cytoplasmic polyadenylation reactions linked to cell cycle control by c-mos and CDK1 activation. Mol Biol Cell. 1997 Aug;8(8):1633–1648. doi: 10.1091/mbc.8.8.1633. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bouvet P., Wolffe A. P. A role for transcription and FRGY2 in masking maternal mRNA within Xenopus oocytes. Cell. 1994 Jun 17;77(6):931–941. doi: 10.1016/0092-8674(94)90141-4. [DOI] [PubMed] [Google Scholar]
- Braddock M., Muckenthaler M., White M. R., Thorburn A. M., Sommerville J., Kingsman A. J., Kingsman S. M. Intron-less RNA injected into the nucleus of Xenopus oocytes accesses a regulated translation control pathway. Nucleic Acids Res. 1994 Dec 11;22(24):5255–5264. doi: 10.1093/nar/22.24.5255. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Colledge W. H., Carlton M. B., Udy G. B., Evans M. J. Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature. 1994 Jul 7;370(6484):65–68. doi: 10.1038/370065a0. [DOI] [PubMed] [Google Scholar]
- Curtis D., Lehmann R., Zamore P. D. Translational regulation in development. Cell. 1995 Apr 21;81(2):171–178. doi: 10.1016/0092-8674(95)90325-9. [DOI] [PubMed] [Google Scholar]
- Darnell J. E., Philipson L., Wall R., Adesnik M. Polyadenylic acid sequences: role in conversion of nuclear RNA into messenger RNA. Science. 1971 Oct 29;174(4008):507–510. doi: 10.1126/science.174.4008.507. [DOI] [PubMed] [Google Scholar]
- Fox C. A., Sheets M. D., Wickens M. P. 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):2151–2162. doi: 10.1101/gad.3.12b.2151. [DOI] [PubMed] [Google Scholar]
- Fox C. A., Wickens M. Poly(A) removal during oocyte maturation: a default reaction selectively prevented by specific sequences in the 3' UTR of certain maternal mRNAs. Genes Dev. 1990 Dec;4(12B):2287–2298. doi: 10.1101/gad.4.12b.2287. [DOI] [PubMed] [Google Scholar]
- Galili G., Kawata E. E., Smith L. D., Larkins B. A. Role of the 3'-poly(A) sequence in translational regulation of mRNAs in Xenopus laevis oocytes. J Biol Chem. 1988 Apr 25;263(12):5764–5770. [PubMed] [Google Scholar]
- Gebauer F., Xu W., Cooper G. M., Richter J. D. Translational control by cytoplasmic polyadenylation of c-mos mRNA is necessary for oocyte maturation in the mouse. EMBO J. 1994 Dec 1;13(23):5712–5720. doi: 10.1002/j.1460-2075.1994.tb06909.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gotoh Y., Masuyama N., Dell K., Shirakabe K., Nishida E. Initiation of Xenopus oocyte maturation by activation of the mitogen-activated protein kinase cascade. J Biol Chem. 1995 Oct 27;270(43):25898–25904. doi: 10.1074/jbc.270.43.25898. [DOI] [PubMed] [Google Scholar]
- Hashimoto N., Watanabe N., Furuta Y., Tamemoto H., Sagata N., Yokoyama M., Okazaki K., Nagayoshi M., Takeda N., Ikawa Y. Parthenogenetic activation of oocytes in c-mos-deficient mice. Nature. 1994 Jul 7;370(6484):68–71. doi: 10.1038/370068a0. [DOI] [PubMed] [Google Scholar]
- Kuge H., Inoue A. Maturation of Xenopus laevis oocyte by progesterone requires poly(A) tail elongation of mRNA. Exp Cell Res. 1992 Sep;202(1):52–58. doi: 10.1016/0014-4827(92)90403-u. [DOI] [PubMed] [Google Scholar]
- Kuge H., Richter J. D. Cytoplasmic 3' poly(A) addition induces 5' cap ribose methylation: implications for translational control of maternal mRNA. EMBO J. 1995 Dec 15;14(24):6301–6310. doi: 10.1002/j.1460-2075.1995.tb00320.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lieberfarb M. E., Chu T., Wreden C., Theurkauf W., Gergen J. P., Strickland S. Mutations that perturb poly(A)-dependent maternal mRNA activation block the initiation of development. Development. 1996 Feb;122(2):579–588. doi: 10.1242/dev.122.2.579. [DOI] [PubMed] [Google Scholar]
- Maale G., Stein G., Mans R. Effects of cordycepin and cordycepintriphosphate on polyadenylic and ribonucleic acid-synthesising enzymes from eukaryotes. Nature. 1975 May 1;255(5503):80–82. doi: 10.1038/255080a0. [DOI] [PubMed] [Google Scholar]
- McGrew L. L., Dworkin-Rastl E., Dworkin M. B., Richter J. D. 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):803–815. doi: 10.1101/gad.3.6.803. [DOI] [PubMed] [Google Scholar]
- Meric F., Matsumoto K., Wolffe A. P. Regulated unmasking of in vivo synthesized maternal mRNA at oocyte maturation. A role for the chaperone nucleoplasmin. J Biol Chem. 1997 May 9;272(19):12840–12846. doi: 10.1074/jbc.272.19.12840. [DOI] [PubMed] [Google Scholar]
- Moore C. L., Skolnik-David H., Sharp P. A. Analysis of RNA cleavage at the adenovirus-2 L3 polyadenylation site. EMBO J. 1986 Aug;5(8):1929–1938. doi: 10.1002/j.1460-2075.1986.tb04446.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nebreda A. R., Gannon J. V., Hunt T. Newly synthesized protein(s) must associate with p34cdc2 to activate MAP kinase and MPF during progesterone-induced maturation of Xenopus oocytes. EMBO J. 1995 Nov 15;14(22):5597–5607. doi: 10.1002/j.1460-2075.1995.tb00247.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nishizawa M., Okazaki K., Furuno N., Watanabe N., Sagata N. The 'second-codon rule' and autophosphorylation govern the stability and activity of Mos during the meiotic cell cycle in Xenopus oocytes. EMBO J. 1992 Jul;11(7):2433–2446. doi: 10.1002/j.1460-2075.1992.tb05308.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Paris J., Richter J. D. 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):5634–5645. doi: 10.1128/mcb.10.11.5634. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sachs A. B., Kornberg R. D. Purification and characterization of polyadenylate-binding protein. Methods Enzymol. 1990;181:332–352. doi: 10.1016/0076-6879(90)81134-g. [DOI] [PubMed] [Google Scholar]
- Sagata N., Daar I., Oskarsson M., Showalter S. D., Vande Woude G. F. The product of the mos proto-oncogene as a candidate "initiator" for oocyte maturation. Science. 1989 Aug 11;245(4918):643–646. doi: 10.1126/science.2474853. [DOI] [PubMed] [Google Scholar]
- Sagata N., Oskarsson M., Copeland T., Brumbaugh J., Vande Woude G. F. Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. Nature. 1988 Oct 6;335(6190):519–525. doi: 10.1038/335519a0. [DOI] [PubMed] [Google Scholar]
- Sagata N. What does Mos do in oocytes and somatic cells? Bioessays. 1997 Jan;19(1):13–21. doi: 10.1002/bies.950190105. [DOI] [PubMed] [Google Scholar]
- Sallés F. J., Lieberfarb M. E., Wreden C., Gergen J. P., Strickland S. Coordinate initiation of Drosophila development by regulated polyadenylation of maternal messenger RNAs. Science. 1994 Dec 23;266(5193):1996–1999. doi: 10.1126/science.7801127. [DOI] [PubMed] [Google Scholar]
- Sheets M. D., Fox C. A., Hunt T., Vande Woude G., Wickens M. The 3'-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes Dev. 1994 Apr 15;8(8):926–938. doi: 10.1101/gad.8.8.926. [DOI] [PubMed] [Google Scholar]
- Sheets M. D., Stephenson P., Wickens M. P. Products of in vitro cleavage and polyadenylation of simian virus 40 late pre-mRNAs. Mol Cell Biol. 1987 Apr;7(4):1518–1529. doi: 10.1128/mcb.7.4.1518. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sheets M. D., Wu M., Wickens M. Polyadenylation of c-mos mRNA as a control point in Xenopus meiotic maturation. Nature. 1995 Apr 6;374(6522):511–516. doi: 10.1038/374511a0. [DOI] [PubMed] [Google Scholar]
- Simon R., Tassan J. P., Richter J. D. 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):2580–2591. doi: 10.1101/gad.6.12b.2580. [DOI] [PubMed] [Google Scholar]
- Sippel A. E. Purification and characterization of adenosine triphosphate: ribonucleic acid adenyltransferase from Escherichia coli. Eur J Biochem. 1973 Aug 1;37(1):31–40. doi: 10.1111/j.1432-1033.1973.tb02953.x. [DOI] [PubMed] [Google Scholar]
- Varnum S. M., Wormington W. M. Deadenylation of maternal mRNAs during Xenopus oocyte maturation does not require specific cis-sequences: a default mechanism for translational control. Genes Dev. 1990 Dec;4(12B):2278–2286. doi: 10.1101/gad.4.12b.2278. [DOI] [PubMed] [Google Scholar]
- Vassalli J. D., Huarte J., Belin D., Gubler P., Vassalli A., O'Connell M. L., Parton L. A., Rickles R. J., Strickland S. Regulated polyadenylation controls mRNA translation during meiotic maturation of mouse oocytes. Genes Dev. 1989 Dec;3(12B):2163–2171. doi: 10.1101/gad.3.12b.2163. [DOI] [PubMed] [Google Scholar]
- Verrotti A. C., Thompson S. R., Wreden C., Strickland S., Wickens M. Evolutionary conservation of sequence elements controlling cytoplasmic polyadenylylation. Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9027–9032. doi: 10.1073/pnas.93.17.9027. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wickens M., Anderson P., Jackson R. J. Life and death in the cytoplasm: messages from the 3' end. Curr Opin Genet Dev. 1997 Apr;7(2):220–232. doi: 10.1016/s0959-437x(97)80132-3. [DOI] [PubMed] [Google Scholar]
- Wreden C., Verrotti A. C., Schisa J. A., Lieberfarb M. E., Strickland S. Nanos and pumilio establish embryonic polarity in Drosophila by promoting posterior deadenylation of hunchback mRNA. Development. 1997 Aug;124(15):3015–3023. doi: 10.1242/dev.124.15.3015. [DOI] [PubMed] [Google Scholar]
- Yew N., Mellini M. L., Vande Woude G. F. Meiotic initiation by the mos protein in Xenopus. Nature. 1992 Feb 13;355(6361):649–652. doi: 10.1038/355649a0. [DOI] [PubMed] [Google Scholar]