Overexpression of poly(A) binding protein prevents maturation-specific deadenylation and translational inactivation in Xenopus oocytes

EMBO Journal

Volumn 15, Issue 4, 1996, Pages 900-909

  Wormington, Michael ^a   Searfoss, Anjanette M ^a   Hurney, Carol A ^b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Deadenylation; Maternal mRNA; Oocyte maturation; Poly(A) binding protein; Xenopus

Indexed keywords

MESSENGER RNA; NUCLEASE; POLYADENYLATED RNA; RNA BINDING PROTEIN;

ANIMAL CELL; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; FEMALE; NONHUMAN; OOCYTE MATURATION; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN SYNTHESIS; RNA TRANSLATION; TRANSLATION INITIATION; TRANSLATION REGULATION; XENOPUS;

EID: 0030041959     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00424.x     Document Type: Article

References (65)

1. Åström, J., Åström, A. and Virtanen, A. (1992) Properties of a HeLa cell 3′ exonuclease specific for degrading poly(A) tails of mammalian mRNA. J. Biol. Chem., 267, 18154-18159.
2. Ballantyne, S., Bilger, A., Åström, J., Virtanen, A. and Wickens, M. (1995) Poly(A) polymerases in the nucleus and cytoplasm of frog oocytes: Dynamic changes during oocyte maturation and early development. RNA, 1, 64-78.
3. Bass, B.L, Hurst, S.R. and Singer, J.D (1994) Binding properties of newly identified Xenopus proteins containing dsRNA-binding motifs. Curr. Biol., 4, 301-314.
4. Bernstein, P., Peltz, S.W. and Ross, J (1989) The poly(A)-binding protein complex is a major determinant of mRNA stability in vitro. Mol. Cell. Biol., 9, 659-670
5. Bilger, A, Fox, C.A., Wahle, E. and Wickens, M. (1994) Nuclear polyadenylation factors recognize cytoplasmic polyadenylation elements. Genes Dev., 8, 1106-1116.
6. Bouvet, P., Omilli, F., Arlot-Bonnemains, Y., Legagneux, V., Roghi, C., Bassez, T. and Osborne, H.B. (1994) The deadenylation conferred by the 3′ untranslated region of a developmentally controlled mRNA in Xenopus embryos is switched to polyadenylation by deletion of a short sequence element. Mol. Cell. Biol., 14, 1893-1900.
7. Campbell, L.H., Borg, K.T., Haines, J.K., Moon, R.T., Schoenberg, D.R and Arrigo, S.J. (1994) Human immunodeficiency virus type 1 Rev is required in vivo for binding of poly(A)-binding protein to Rev-dependent RNAs. J. Virol., 68, 5433-5438.
8. Caruccio, N. and Ross, J. (1994) Purification of a human polyribosome-associated 3′ to 5′ exoribonuclease. J. Biol. Chem., 269, 31814-31821.
9. Curtis, D., Lehmann, R. and Zamore, P.D. (1995) Translational regulation in development. Cell, 81, 171-178.
10. Davidson, E.H. (1986) Gene Activity in Early Development Academic Press, New York.
11. Decker, C.J. and Parker, R. (1993) A turnover pathway for both stable and unstable mRNAs in yeast: Evidence for a requirement for deadenylation. Genes Dev., 7, 1632-1643.
12. Duval, C, Bouvet, P., Omilli, F. Roghi, C., Dorel, C. LeGuellec, R., Paris, J. and Osborne, H.B. (1990) Stability of maternal mRNA in Xenopus embryos: Role of transcription and translation. Mol Cell. Biol., 10, 4123-4129.
13. Dworkin, M.B and Dworkin-Rastl, E. (1985) Changes in RNA titers and polyadenylation during oogenesis and oocyte maturation in Xenopus laevis. Dev. Biol., 2, 451-457.
14. Ford, P.J., and Southern, E.M. (1979) Different sequences for 5S RNA in kidney cells and ovaries of Xenopus laevis. Nature New Biol., 241, 7-12
15. Fox, C.A. and Wickens, M. (1990) Poly(A) removal during oocyte maturation: A default reaction selectively prevented by specific sequences in the 3′ UTR of certain maternal mRNAs. Genes Dev., 4, 2287-2298.
16. Fox, C.A., Sheets, M A. and Wickens, M.P. (1989) Poly(A) addition during maturation of frog oocytes Distinct nuclear and cytoplasmic activities and regulation by the sequence UUUUUAU. Genes Dev., 3, 2151-2162.
17. Fox, C.A., Sheets, M.A., Wahle, E. and Wickens, M. (1992) Polyadenylation of maternal mRNAs during oocyte maturation. Poly(A) addition in vitro requires a regulated RNA binding activity and a poly(A) polymerase. EMBO J., 11, 5021-5032.
18. Gallie, D.R. (1991) The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev., 5, 2108-2116.
19. Gebauer, F. and Richter, J.D. (1995) Cloning and characterization of a Xenopus poly(A) polymerase. Mol. Cell Biol., 15, 1422-1430.
20. Görlach, M., Burd, C.G. and Dreyfuss, G. (1994) The mRNA poly(A)-binding protein: Localization, abundance, and RNA-binding specificity. Exp. Cell Res., 211, 400-407.
21. Gurdon, J.B. (1976) Injected nuclei in frog oocytes: Fate, enlargement and chromatin dispersal. J. Embryol. Exp. Morphol., 36, 523-540.
22. Hake, L.E. and Richter, J.D. (1994) CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell, 79, 617-627
23. Huarte, J., Stutz, A , O'Connell, M.L., Gubler, P., Belin, D., Darrow, A.L., Strickland, S. and Vassalli, J.-D. (1992) Transient translational silencing by reversible mRNA deadenylation. Cell, 69, 1021-1030.
24. Hyman, L.E. and Wormington, W.M. (1988) Translational inactivation of ribosomal protein mRNAs during Xenopus oocyte maturation. Genes Dev., 2, 598-605.
25. Hyman, L.E., Colot, H V. and Rosbash, M. (1984) Accumulation and behavior of mRNA during oogenesis and early embryogenesis of Xenopus laevis. In Malicinski, G.M. and Klein, W.H. (eds), Molecular Aspects of Early Development. Plenum Press, New York, pp. 253-266.
26. Keiper, B.D. and Wormington, W.M. (1990) Nucleotide sequence and 40S subunit assembly of Xenopus laevis ribosomal protein S22. J. Biol. Chem., 265, 19397-19400.
27. Krieg, P.A. and Melton, D.A. (1984) Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res, 12, 7057-7070.
28. Lowell, J.E., Rudner, D.Z. and Sachs, A.B. (1992) 3′-UTR-dependent deadenylation by the yeast poly(A) nuclease. Genes Dev., 6, 2088-2099.
29. Marello, K., LaRovere, J. and Sommerville, J. (1992) Binding of Xenopus oocyte masking proteins to mRNA sequences. Nucleic Acids Res., 20, 5593-5600.
30. McGrew, L.L., Dworkin-Rastl, E., Dworkin, M.B. and Richter, J.D. (1989) Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. Genes Dev., 3, 803-815.
31. Millar, A.J., Short, S.R., Chua, N.H. and Kay, S.A. (1992) A novel circadian phenotype based on firefly luciferase expression in transgenic plants. Plant Cell, 4, 1075-1087.
32. Muhlrad, D., Decker, C.J and Parker, R. (1994) Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5′→3′ digestion of the transcript. Genes Dev., 8, 855-866.
33. Munroe, D. and Jacobson, A (1990) mRNA poly(A) tail: a 3′ enhancer of translational initiation. Mol. Cell. Biol., 10, 3441-3455.
34. Murray, M.T., Krohne, G. and Franke, W.W. (1991) Different forms of soluble cytoplasmic mRNA binding proteins and particles in Xenopus laevis oocytes and embryos. J. Cell Biol., 112, 1-11.
35. Nietfeld, W., Mentzel, H. and Pieler, T. (1990) The Xenopus laevis poly(A) binding protein is composed of multiple functionally independent RNA binding domains. EMBO J.. 9, 3699-3705.
36. Paris, J and Richter, J D. (1990) 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., 10, 5634-5645.
37. Paris, J., Swenson, K., Piwnica-Worms, H. and Richter, J.D. (1991) Maturation-specific polyadenylation: in vitro activation by p34cdc2 and phosphorylation of a 58-kD CPE-binding protein. Genes Dev., 5, 1697-1708.
38. Paynton, B.V. and Bachvarova, R. (1994) Polyadenylation and deadenylation of maternal mRNAs during oocyte growth and maturation in the mouse. Mol. Reprod. Dev., 37, 172-180.
39. Richter, J.D. and Smith, L.D. (1981) Differential capacity for translation and lack of competition between mRNAs that segregate to free and membrane-bound polysomes. Cell, 27, 183-191.
40. Sachs, A.B. (1993) Messenger RNA degradation in eukaryotes. Cell, 74, 413-421.
41. Sachs, A.B. and Davis, R.W. (1989) The poly(A) binding protein is required for poly(A) shortening and 60S ribosomal subunit-dependent translation initiation. Cell, 58, 857-867.
42. Sachs, A.B. and Deardorff, J A. (1992) Translation initiation requires the PAB-dependent poly(A) ribonuclease in yeast. Cell, 70, 961-973.
43. Sachs, A. and Wahle, E. (1993) Poly(A) tail metabolism and function in eucaryotes. J. Biol. Chem., 268, 22955-22958.
44. Sachs, A.B, Davis, R.W. and Kornberg, R.D. (1987) A single domain of yeast poly(A)-binding protein is necessary and sufficient for RNA binding and cell viability. Mol. Cell. Biol., 7, 3268-3276.
45. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Sheets, M.D., Fox, C.A., Hunt, T., Vande Woude, G. and Wickens, M. (1994) The 3′-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation Genes Dev., 8, 926-938.
47. Simon, R. and Richter, J.D. (1994) Further analysis of cytoplasmic polyadenylation in Xenopus embryos and identification of embryonic cytoplasmic polyadenylation element-binding proteins. Mol. Cell. Biol., 14, 7867-7875.
48. Simon, R., Tassan, J.-P. and Richter, J.D. (1992) Translational control by poly(A) elongation during Xenopus development: Differential repression and enhancement by a novel cytoplasmic polyadenylation element. Genes Dev., 6, 2580-2591.
49. Smith, R C. (1990) Synthesis of a 180 kDa protein is a molecular marker of Xenopus oocyte meiotic maturation. Cell Dig. Dev., 31, 97-104.
50. +-binding protein expressed in a baculovirus system. Biochem. J., 287, 761-766.
51. Standart, N (1992) Masking and unmasking of maternal mRNA. Semin. Dev. Biol, 3, 367-379.
52. Standart, N. (1993) The RNA-protein partners in mRNP. Mol. Biol. Reports, 18, 135-142.
53. Stebbins-Boaz, B. and Richter, J D. (1994) Multiple sequence elements and a maternal mRNA product control cdk2 RNA polyadenylation and translation during early Xenopus development. Mol. Cell. Biol., 14, 5870-5874.
54. Swanson, M.S. and Dreyfuss, G. (1988) Classification and purification of proteins of heterogeneous nuclear ribonucleoprotein particles by RNA-binding specificities. Mol. Cell. Biol., 8, 2237-2241.
55. Tafuri, S.R. and Wolffe, A.P (1993) Selective recruitment of marked maternal mRNA from messenger ribonucleoprotein particles containing FRGY2 (mRNP4). J. Biol. Chem., 268, 24255-24261
56. Varnum, S M. (1990) Deadenylation and translational inactivation of ribosomal protein mRNAs during Xenopus laevis oocyte maturation. Ph D. Thesis, Brandeis University, USA.
57. Varnum, S.M and Wormington, W.M (1990) Deadenylation of maternal mRNAs during Xenopus oocyte maturation does not require specific cis-sequences. A default mechanism for translational control. Genes Dev., 4, 2278-2286.
58. Varnum, S.M., Hurney, C.A and Wormington, W.M. (1992) Maturation-specific deadenylation in Xenopus oocytes requires nuclear and cytoplasmic factors. Dev. Biol., 153, 283-290.
59. Wahle, E. (1991) A novel poly(A)-binding protein acts as a specificity factor in the second phase of messenger RNA polyadenylation. Cell, 66, 759-768.
60. Wahle, E. and Keller, W. (1992) The biochemistry of 3′-end cleavage and polyadenylation of messenger RNA precursors. Annu Rev. Biochem., 61, 419-440.
61. Wickens, M. (1992) Forward, backward, how much when: Mechanisms of poly(A) addition and removal and their role in early development. Semin. Dev. Biol., 3, 399-412.
62. Wormington, M. (1991) Preparation of synthetic mRNAs and analyses of translational efficiency in microinjected Xenopus oocytes. Methods Cell Biol., 36, 163-179.
63. Wormington, M. (1993) Poly(A) and translation: development control. Curr. Opin. Cell Biol., 5, 950-954.
64. Wormington, W.M. (1989) Developmental expression and 5S rRNA-binding activity of Xenopus laevis ribosomal protein L5. Mol. Cell. Biol., 9, 5281-5288.
65. Zelus, B.D., Giebelhaus, D.H., Eib, D.W., Kenner, K.A. and Moon, R.T (1989) Expression of the poly(A)-binding protein during development of Xenopus laevis. Mol. Cell. Biol., 9, 2756-2760.