In vivo antisense oligodeoxynucleotide mapping reveals masked regulatory elements in an mRNA dormant in mouse oocytes

Molecular and Cellular Biology

Volumn 17, Issue 4, 1997, Pages 1759-1767

  Stutz, André ^a,b   Huarte, Joachim ^a   Gubler, Pascale ^a   Conne, Béatrice ^a   Belin, Dominique ^a   Vassalli, Jean Dominique ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b CMU   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; MESSENGER RNA; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL CELL; ARTICLE; CELL GROWTH; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; MEIOSIS; MOUSE; NONHUMAN; OOCYTE MATURATION; POLYADENYLATION; PRIORITY JOURNAL; RNA TRANSLATION; TRANSLATION REGULATION;

ANIMALIA;

EID: 0030939071     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.4.1759     Document Type: Article

References (58)

1. Ahringer, J., and J. Kimble. 1991. Control of the sperm-oocyte switch in Caenorhabditis elegans hermaphrodites by the fem-3 3′ untranslated region. Nature 349:346-348.
2. Bachvarova, R., E. M. Cohen, V. De Leon, K. Tokunaga, S. Sakiyama, and B. V. Paynton. 1989. Amounts and modulation of actin mRNAs in mouse oocytes and embryos. Development 106:561-565.
3. Bachvarova, R. F. 1992. A maternal tail of poly(A): the long and the short of it. Cell 69:895-897.
4. Belin, D. 1996. The RNase protection assay. Methods Mol. Biol. 58:131-136.
5. Belin, D. 1994. The use of riboprobes for the analysis of gene expression. Methods Mol. Biol. 31:257-272.
6. Biggers, J. D., W. J. Whitten, and D. G. Whittingham. 1971. The culture of mouse embryos in vitro, p. 86-116. In G. C. Daniel (ed.), Methods in mammalian embryology. Academic Press, New York, N.Y.
7. Bilger, A., C. A. Fox, E. Wahle, and M. Wickens. 1994. Nuclear polyadenylation factors recognize cytoplasmic polyadenylation elements. Genes Dev. 8:1106-1116.
8. Bouvet, P., K. Matsumoto, and A. P. Wolffe. 1995. Sequence-specific RNA recognition by the Xenopus Y-box proteins. An essential role for the cold shock domain. J. Biol. Chem. 270:28297-28303.
9. Bouvet, P., and A. P. Wolffe. 1994. A role for transcription and FRGY2 in masking maternal mRNA within Xenopus oocytes. Cell 77:931-941.
10. Curtis, D., R. Lehmann, and P. D. Zamore. 1995. Translational regulation in development. Cell 81:171-178.
11. Davidson, E. H. 1986. Gene activity in early development, 3rd ed. Academic Press, New York, N.Y.
12. Gebauer, F., W. Xu, G. M. Cooper, and J. D. Richter. 1994. Translational control by cytoplasmic polyadenylation of c-mos mRNA is necessary for oocyte maturation in the mouse. EMBO J. 13:5712.
13. Goodwin, E. B., P. G. Okkema, T. C. Evans, and J. Kimble. 1993. Translational regulation of tra-2 by its 3′ untranslated region controls sexual identity in C. elegans. Cell 75:329-339.
14. Gray, N. K., and M. W. Hentze. 1994. Regulation of protein synthesis by mRNA structure. Mol. Biol. Rep. 19:195-200.
15. Hershey, J. W. B., M. B. Mathews, and N. Sonenberg. 1996. Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
16. Huarte, J., D. Belin, A. Vassalli, S. Strickland, and J.-D. Vassalli. 1987. Meiotic maturation of mouse oocytes triggers the translation and polyadenylation of dormant tissue-type plasminogen activator mRNA. Genes Dev. 1:1201-1211.
17. Huarte, J., D. Belin, and J.-D. Vassalli. 1985. Plasminogen activator in mouse and rat oocytes: induction during meiotic maturation. Cell 43:551-558.
18. Huarte, J., A. Stutz, M. L. O'Connell, P. Gubler, D. Belin, A. L. Darrow, S. Strickland, and J.-D. Vassalli. 1992. Transient translational silencing by reversible mRNA deadenylation. Cell 69:1021-1030.
19. Kelso Winemiller, L. C., and M. M. Winkler. 1991. 'Unmasking' of stored maternal mRNAs and the activation of protein synthesis at fertilization in sea urchins. Development 111:623-633.
20. Matsumoto, K., F. Meric, and A. P. Wolffe. 1996. Translational repression dependent on the interaction of the Xenopus Y-box protein FRGY2 with mRNA. J. Biol. Chem. 271:22706-22712.
21. Melton, D. A. 1985. Injected anti-sense RNAs specifically block messenger RNA translation in vivo. Proc. Natl. Acad. Sci. USA 82:144-148.
22. Morgan, R., M. Edge, and A. Colman. 1993. A more efficient and specific strategy in the ablation of mRNA in Xenopus laevis using mixtures of antisense oligos. Nucleic Acids Res. 21:4615-4620.
23. O'Keefe, S. J., A. A. Kiessling, and G. M. Cooper. 1991. The c-mos gene product is required for cyclin B accumulation during meiosis of mouse eggs. Proc. Natl. Acad. Sci. USA 88:7869-7872.
24. Paleos, G. A., and R. D. Powers. 1981. The effect of calcium on the first meiotic division of the mammalian oocyte. J. Exp. Zool. 217:409-416.
25. Paynton, B. V., and R. Bachvarova. 1994. Polyadenylation and deadenylation of maternal mRNAs during oocyte growth and maturation in the mouse. Mol. Reprod. Dev. 37:172-180.
26. Richter, J. D. 1995. Dynamics of poly(A) addition and removal during development, p. 481-503. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
27. Rickles, R. J., A. L. Darrow, and S. Strickland. 1988. Molecular cloning of complementary DNA to mouse tissue plasminogen activator mRNA and its expression during F9 teratocarcinoma cell differentiation. J. Biol. Chem. 263:1563-1569.
28. Rosenthal, E. T., M. Bahr, and F. H. Wilt. 1993. Regulation of maternal messenger RNA translation during oogenesis and embryogenesis in Urechis caupo. Dev. Biol. 155:297-306.
29. Rosenthal, E. T., and J. V. Ruderman. 1987. Widespread changes in the translation and adenylation of maternal messenger RNAs following fertilization of Spisula oocytes. Dev. Biol. 121:237-246.
30. Rosenthal, E. T., T. R. Tansey, and J. V. Ruderman. 1983. Sequence-specific adenylations and deadenylations accompany changes in the translation of maternal messenger RNA after fertilization of Spisula oocytes. J. Mol. Biol. 166:309-327.
31. Rosenthal, E. T., and F. H. Wilt. 1986. Patterns of maternal messenger RNA accumulation and adenylation during oogenesis in Urechis caupo. Dev. Biol. 117:55-63.
32. Rouault, T. A., R. D. Klausner, and J. B. Harford. 1995. Translational control of ferritin, p. 335-362. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
33. Sallés, F. J., A. L. Darrow, M. L. O'Connell, and S. Strickland. 1992. Isolation of novel murine maternal mRNAs regulated by cytoplasmic polyadenylation. Genes Dev. 6:1202-1212.
34. Sallés, F. J., W. G. Richards, J. Huarte, J.-D. Vassalli, and S. Strickland. 1993. Microinjecting antisense sequences into oocytes. Methods Enzymol. 225:351-361.
35. Sallés, F. J., and S. Strickland. 1995. Rapid and sensitive analysis of mRNA polyadenylation states by PCR. PCR Methods Appl. 4:317-321.
36. Sawadogo, M., and M. W. Van Dyke. 1991. A rapid method for the purification of deprotected oligodeoxynucleotides. Nucleic Acids Res. 19:674.
37. Sheets, M. D., M. Wu, and M. Wickens. 1995. Polyadenylation of c-mos mRNA as a control point in Xenopus meiotic maturation. Nature 374:511-516.
38. Spirin, A. S. 1995. Masked and translatable messenger ribonucleoproteins in higher eukaryotes, p. 319-334. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
39. Spirin, A. S. 1966. On "masked" forms of messenger RNA in early embryogenesis and in other differentiating systems. Curr. Top. Dev. Biol. 1:1-38.
40. Spirin, A. S. 1994. Storage of messenger RNA in eukaryotes: envelopment with protein, translational barrier at 5′ side, or conformational masking by 3′ side. Mol. Reprod. Dev. 38:107-117.
41. Standart, N. 1992. Masking and unmasking of maternal mRNA. Semin. Dev. Biol. 3:367-379.
42. Standart, N., and M. Dale. 1993. Regulated polyadenylation of clam maternal mRNAs in vitro. Dev. Genet. 14:492-499.
43. Standart, N., M. Dale, E. Stewart, and T. Hunt. 1990. Maternal mRNA from clam oocytes can be specifically unmasked in vitro by antisense RNA complementary to the 3′-untranslated region. Genes Dev. 4:2157-2168.
44. Standart, N., and T. Hunt. 1990. Control of translation of masked mRNAs in clam oocytes. Enzyme 44:106-119.
45. Standart, N., and R. Jackson. 1994. Translational regulation. Y the message is masked? Curr. Biol. 4:939-941.
46. Stebbins Boaz, B., and J. D. Richter. 1994. Multiple sequence elements and a maternal mRNA product control cdk2 RNA polyadenylation and translation during early Xenopus development. Mol. Cell. Biol. 14:5870-5880.
47. Stebbins-Boaz, B., L. E. Hake, and J. D. Richter. 1996. CPEB controls the cytoplasmic polyadenylation of cyclin, Cdk2 and c-mos mRNAs and is necessary for oocytes maturation in Xenopus. EMBO J. 15:2582-2592.
48. Strickland, S., J. Huarte, D. Belin, A. Vassalli, R. J. Rickles, and J.-D. Vassalli. 1988. Antisense RNA directed against the 3′ noncoding region prevents dormant mRNA activation in mouse oocytes. Science 241:680-684.
49. Tafuri, S. R., and A. P. Wolffe. 1993. Selective recruitment of masked maternal mRNA from messenger ribonucleoprotein particles containing FRGY2 (mRNP4). J. Biol. Chem. 268:24255-24261.
50. Tong, Z. B., L. M. Nelson, and J. Dean. 1995. Inhibition of zona pellucida gene expression by antisense oligonucleotides injected into mouse oocytes. J. Biol. Chem. 270:849-853.
51. Vassalli, J. D., and A. Stutz. 1995. Translational control. Awakening dormant mRNAs. Curr. Biol. 5:476-479.
52. Vassalli, J.-D., J. Huarte, D. Belin, P. Gubler, A. Vassalli, M. L. O'Connell, L. A. Parton, R. J. Rickles, and S. Strickland. 1989. Regulated polyadenylation controls mRNA translation during meiotic maturation of mouse oocytes. Genes Dev. 3:2163-2171.
53. Walker, J., M. Dale, and N. Standart. 1996. Unmasking mRNA in clam oocytes: role of phosphorylation of a 3′ UTR masking element-binding protein at fertilization. Dev. Biol. 173:292-305.
54. Wickens, M., J. Kimble, and S. Strickland. 1995. Translational control of developmental decisions, p. 411-450. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
55. Wolffe, A. P. 1994. Structural and functional properties of evolutionarily ancient Y-box family of nucleic acid binding proteins. J. Biol. Chem. 271: 22706-22712.
56. Woolf, T. M., C. G. Jennings, M. Rebagliati, and D. A. Melton. 1990. The stability, toxicity and effectiveness of unmodified and phosphorothioate antisense oligodeoxynucleotides in Xenopus oocytes and embryos. Nucleic Acids Res. 18:1763-1769.
57. Woolf, T. M., D. A. Melton, and C. G. Jennings. 1992. Specificity of antisense oligonucleotides in vivo. Proc. Natl. Acad. Sci. USA 89:7305-7309.
58. Wormington, M. 1994. Unmasking the role of the 3′ UTR in the cytoplasmic polyadenylation and translational regulation of maternal mRNAs. Bioessays 16:533-535.