Advertisement

Translational Regulation of Masked Maternal mRNAs in Early Development

  • Nancy Standart
Part of the Endocrine Updates book series (ENDO, volume 16)

Abstract

Gene expression in early development, at a time when transcription is silent, is essentially regulated at the level of protein synthesis in a wide variety of organisms. Overall, there is modest activation of the translational machinery at the time when the oocytes or eggs resume meiosis. More importantly, in every case examined in detail, specific sub-sets of mRNA are recruited onto polysomes from a masked form associated with proteins (mRNP). In contrast to ‘house-keeping’ mRNAs such as actin, tubulin and ribosomal protein mRNAs, which are actively translated in immature oocytes, mRNAs encoding proteins required for entry and progression through the cell cycle (including cyclins, c-mos and ribonucleotide reductase) are translationally inert until oocytes are induced to undergo meiotic maturation or fertilization, when their products are required (1,2). The control of mRNAs encoding cell cycle regulatory proteins in early development has been extensively characterized in lower and higher eukaryotes in the last decade; this research has uncovered one of the best-understood mRNA-specific translational regulators, cytoplasmic polyadenylation element binding protein (CPEB), the major subject of this chapter.

Keywords

Xenopus Oocyte Oocyte Maturation Ribonucleotide Reductase Mouse Oocyte Translational Control 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Standart, N. (1992). Masking and unmasking of maternal mRNA. Semin. Dev. Biol. 3, 367–379.CrossRefGoogle Scholar
  2. 2.
    Wickens, M., Goodwin, E., Kimble, J., Strickland, S., and Hentze, M., Translational control of developmental decisions, in Translational control of gene expression, N. Sonenberg, J. Hershey, and M. Mathews, Editors. 2000, Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York. p. 295–370.Google Scholar
  3. 3.
    Goodwin, E.R. and Evans, T.C. (1997). Translational control of development in C. elegans. Seminars in Cell and Dev. Biol. 8, 551–559.Google Scholar
  4. 4.
    St Johnston, D. (1995). The intracellular localization of messenger RNAs. Cell. 81, 161–170.CrossRefGoogle Scholar
  5. 5.
    Rouault, T.A. and Harford, J.B., Translational control of ferritin synthesis., in Translatonal control of gene expression, N. Sonenberg, J. Hershey, and M. Mathews, Editors. 2000, Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York. p. 655–670.Google Scholar
  6. 6.
    Ostareck-Lederer, A., Ostareck, D.H., and Hentze, M.W. (1998). Cytoplasmic regulatory functions of the KH-domain proteins hnRNP K and E 1/E2. Trends Biochem. Sci. 23, 409–411.CrossRefGoogle Scholar
  7. 7.
    Meyuhas, O. and Hornstein, E., Translational control of TOP mRNAs., in Translational control of gene expression, N. Sonenberg, J. Hershey, and M. Mathews, Editors. 2000, Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York. p. 671–694.Google Scholar
  8. 8.
    Wu, L., Wells, D., Tay, J., Mendis, D., Abbott, M.-A., Barnitt, A., Quinlan, E., Heynen, A., Fallon, J.R., and Richter, J.D. (1998). CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of a-CaMKII mRNA at synapses. Neuron. 21, 1129–1139.PubMedCrossRefGoogle Scholar
  9. 9.
    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.PubMedCrossRefGoogle Scholar
  10. 10.
    Murray, M.T., Schiller, D.L., and Franke, W.W. (1992). Sequence analysis of cytoplasmic mRNA-binding proteins of Xenopus oocytes identifies a family of RNA-binding proteins. Proc. Natl. Acad. Sci. USA. 89, 11–15.PubMedCrossRefGoogle Scholar
  11. 11.
    Bouvet, P. and Wolffe, A.P. (1994). A role for transcription and FRGY2 in masking maternal mRNA within Xenopus oocytes. Cell. 77, 931–941.PubMedCrossRefGoogle Scholar
  12. 12.
    Braddock, M., Muckenthaler, M., White, M.R.H., Thorburn, A.M., Sommerville, J., Kingsman, A.J., and Kingsman, S.M. (1994). Intron-less RNA injected into the nucleus of Xenopus oocytes accesses a regulated translation control pathway. Nucl. Acids Res. 22, 5255–5264.PubMedCrossRefGoogle Scholar
  13. 13.
    Davydova, E.K., Evdokimova, V.M., Ovchinnikov, L.P., and Hershey, J.W. (1997). Overexpression in COS cells of p50, the major core protein associated with mRNA, results in translation inhibition. Nucl. Acids Res. 25, 2911–2916.PubMedCrossRefGoogle Scholar
  14. 14.
    Davies, H.G., Giorgini, F., Fajardo, M.A., and Braun, R.E. (2000). A sequence-specific RNA binding complex expressed in murine germ cells contains MSY2 and MSY4. Dev. Biol. 221, 87–100.PubMedCrossRefGoogle Scholar
  15. 15.
    Standart, N. and Jackson, R. (1994). Y the message is masked ? Curr. Biol. 4, 939–941.PubMedCrossRefGoogle Scholar
  16. 16.
    Matsumoto, K. and Wolfe, A.P. (1998). Gene regulation by Y-box proteins: coupling control of transcription and translation. Trends Cell Biol. 8, 318–323.PubMedCrossRefGoogle Scholar
  17. 17.
    Sommerville, J. and Ladomery, M. (1996). Masking of mRNA by Y-box proteins. FASEB J. 10, 435–43.PubMedGoogle Scholar
  18. 18.
    Standart, N., Dale, M., Stewart, E., and Hunt, T. (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.PubMedCrossRefGoogle Scholar
  19. 19.
    Walker, J., Dale, M., and Standart, N. (1996). Unmasking mRNA in clam oocytes: Role of phosphorylation of a 3’ UTR masking element-binding protein at fertilization. Dev. Biol. 173, 292–305.PubMedCrossRefGoogle Scholar
  20. 20.
    Katsu, Y., Minshall, N., Nagahama, Y., and Standart, N. (1999). Ca2+ is required for phosphorylation of clam p82/CPEB in vitro: Implications for dual and independent roles of MAP and cdc2 kinases. Dev. Biol. 209, 186–199.PubMedCrossRefGoogle Scholar
  21. 21.
    Richter, J.D., Influence of polyadenylation-induced translation on metazoan development and neuronal synaptic function., in Translational control of gene expression, N. Sonenberg, J. Hershey, and M. Mathews, Editors. 2000, Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York. p. 785–806.Google Scholar
  22. 22.
    Rosenthal, E.T., Tansey, T.R., and Ruderman, J.V. (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.PubMedCrossRefGoogle Scholar
  23. 23.
    Sheets, M., Fox, C., 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.PubMedCrossRefGoogle Scholar
  24. 24.
    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.PubMedCrossRefGoogle Scholar
  25. 25.
    Simon, R. and Richter, J. (1994). Further analysis of cytoplasmic polyadenylation in Xenopus embryos and identification of embryonic cytoplasmic polyadenylation element-binding proteins. Mol. Cell. Biol. 14, 7867–7875.PubMedGoogle Scholar
  26. 26.
    de Moor, C.H. and Richter, J., D. (1997). The mos pathway regulates cytoplasmic polyadenylation in Xenopus oocytes. Mol. Cell Biol. 17, 6419–6426.PubMedGoogle Scholar
  27. 27.
    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.PubMedCrossRefGoogle Scholar
  28. 28.
    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.PubMedCrossRefGoogle Scholar
  29. 29.
    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.PubMedCrossRefGoogle Scholar
  30. 30.
    Fox, C.A., Sheets, M.D., 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.PubMedCrossRefGoogle Scholar
  31. 31.
    Ballantyne, S., Daniel, J., D. L., and Wickens, M. (1997). A dependent pathway of cytoplasmic polyadenylation reactions linked to cell cycle control by c-mos and CDK1 activation. Mol. Biol. Cell. 8, 1633–1648.Google Scholar
  32. 32.
    de Moor, C. and Richter, J.D. (1999). Cytoplasmic polyadenylation elements mediate masking and unmasking of cyclin B1 mRNA. EMBO J. 18, 2294–2303.PubMedCrossRefGoogle Scholar
  33. 33.
    Barkoff, A.F., Dickson, K.S., Gray, N.K., and Wickens, M. (2000). Translational control of cyclin B1 mRNA during meiotic maturation: coordinated repression and cytoplasmic polyadenylation. Dev. Biol. 220, 97–109.PubMedCrossRefGoogle Scholar
  34. 34.
    Ralle, T., Gremmels, D., and Stick, R. (1999). Translational control of nuclear lamin B1 mRNA during oogenesis and early development of Xenopus. Mech. Dev. 84, 89–101.PubMedCrossRefGoogle Scholar
  35. 35.
    Charlesworth, A., Welk, J., and MacNicol, A.M. (2000). The temporal control of weel mRNA translation during Xenopus oocyte maturation is regulated by cytoplasmic polyadenylation elements within the 3’-untranslated region. Dev. Biol. 227, 706–719.PubMedCrossRefGoogle Scholar
  36. 36.
    Stutz, A., Conne, B., Huarte, J., Gubler, P., VSlkel, V., Flandin, P., and Vassalli, J.D. (1998). Masking, unmasking, and regulated polyadenylation cooperate in the translational control of a dormant mRNA in mouse oocytes. Genes Dev. 12, 2535–2548.PubMedCrossRefGoogle Scholar
  37. 37.
    Tay, J., Hodgman, R., and Richter, J. (2000). The control of cyclin B 1 mRNA translation during mouse oocyte maturation. Dev. Biol. 221, 1–9.PubMedCrossRefGoogle Scholar
  38. 38.
    Minshall, N., Walker, J., Dale, M., and Standart, N. (1999). Dual roles of p82, the clam CPEB homolog, in cytoplasmic polyadenylation and translational masking. RIVA. 5, 27–38.Google Scholar
  39. 39.
    Sallés, F.J., Lieberfarb, M.E., Wreden, C., Gergen, J.P., and Strickland, S. (1994). Coordinate initiation of Drosophila development by regulated polyadenylation of maternal messenger RNAs. Science. 266, 1996–1999.PubMedCrossRefGoogle Scholar
  40. 40.
    Sheets, M.D., Wu, M., and Wickens, M. (1995). Polyadenylation of c-mos mRNA as a control point in Xenopus meiotic maturation. Nature. 374, 511–516.PubMedCrossRefGoogle Scholar
  41. 41.
    Gebauer, F., Xu, W., Cooper, G., and Richter, J. (1994). Translational control by cytoplasmic polyadenylation of c-mos mRNA is necessary for oocyte maturation in the mouse. EMBO J. 13, 5712–5720.PubMedGoogle Scholar
  42. 42.
    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.PubMedCrossRefGoogle Scholar
  43. 43.
    Hake, L.E., Mendez, R., and Richter, J.D. (1998). Specificity of RNA binding by CPEB: Requirement for RNA recognition motifs and a novel zinc finger. Mol. Cell. Biol. 18, 685–693.PubMedGoogle Scholar
  44. 44.
    Stebbins-Boaz, B., Hake, L.E., and Richter, J.D. (1996). CPEB controls the cytoplasmic polyadenylation of cyclin, Cdk2 and c-mos mRNAs and is necessary for oocyte maturation in Xenopus. EMBO J. 15, 2582–2592.PubMedGoogle Scholar
  45. 45.
    Lantz, V., Chang, J., Horabin, J., Bopp, D., and Schedi, P. (1994). The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes Dev. 8, 598–613.PubMedCrossRefGoogle Scholar
  46. 46.
    Chang, J., Tan, L., and Schedl, P. (1999). The Drosophila CPEB homolog, orb, is required for oskar protein expression in oocytes. Dev. Biol. 215, 91–106.PubMedCrossRefGoogle Scholar
  47. 47.
    Walker, J., Minshall, C., Hake, L., Richter, J., and Standart, N. (1999). The clam 3’UTR masking element-binding protein p82 is a member of the CPEB family. RNA. 5, 14–26.PubMedCrossRefGoogle Scholar
  48. 48.
    Luitjens, C., Gallegos, M., Kraemer, B., Kimble, J., and Wickens, M. (2000). CPEB proteins control two key steps in spermatogenesis in C. elegans. Genes Dev. 14, 2596–2609.PubMedCrossRefGoogle Scholar
  49. 49.
    Gebauer, F. and Richter, J. (1996). Mouse cytoplasmic polyadenylylation element binding protein: An evolutionary conserved protein that interacts with the cytoplasmic polyadenylylation elements of c-mos mRNA. Proc. Natl. Acad. Sci. USA. 93, 14602–14607.PubMedCrossRefGoogle Scholar
  50. 50.
    Bally-Cuif, L., Schatz, W.J., and Ho, R.K. (1998). Characterization of the zebrafish Orb/CPEB-related RNA-binding protein and localization of maternal components in the zebrafish oocyte. Mech. Dev. 77, 31–47.PubMedCrossRefGoogle Scholar
  51. 50a.
    Welk, J.F., Charlesworth, A., Smith, G.D, and MacNichols, A.M. (2001). Identification and characterization of the gene encoding human cytoplasmic polyadenylation element binding protein. Gene 263: 113–120.PubMedCrossRefGoogle Scholar
  52. 51.
    Stutz, A., Huarte, J., Gubler, P., Conne, B., Belin, D., and Vassalli, J.-D. (1997). In vivo antisense oligodeoxynucleotide mapping reveals masked regulatory elements in an mRNA dormant in mouse oocytes. Mol. Cell. Biol. 17 1759–1767.PubMedCrossRefGoogle Scholar
  53. 52.
    Huarte, J., Stutz, A., O’Connell, M.L., Gubler, P., Belin, D., Darrow, A.L., Strickland, S., and Vassali, J.-D. (1992). Transient translational silencing by reversible mRNA deadenylation. Cell. 69, 1021–1030.PubMedCrossRefGoogle Scholar
  54. 53.
    Culp, P.A. and Musci, T.J. (1998). Translational activation and cytoplasmic polyadenylation of FGF receptor-1 are independently regulated during Xenopus oocyte maturation. Dev. Biol. 193, 63–76.PubMedCrossRefGoogle Scholar
  55. 54.
    Sachs, A., Physical and functional interactions between the mRNA cap structure and the poly(A) tail, in Translational control of gene expression, N. Sonenberg, J. Hershey, and M. Mathews, Editors. 2000, Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York.Google Scholar
  56. 55.
    Gillian-Daniel, D.L., Gray, N.K., Astrom, J., Barkoff, A., and Wickens, M. (1998). Modifications of the 5’ cap of mRNAs during Xenopus oocyte maturation: independence from changes in poly(A) length and impact on translation. Mol. Cell Biol. 18, 6152–6153.PubMedGoogle Scholar
  57. 56.
    Kuge, H. and Richter, J. (1995). Cytoplasmic 3’ poly(A) addition induces 5’ cap ribose methylation: implications for translational control of maternal mRNA. EMBO J. 14, 6301–6310.PubMedGoogle Scholar
  58. 57.
    Gray, N., Coller, J., Dickson, K., and Wickens, M. (2000). Multiple portions of poly(A)-binding protein stimulate translation in vivo. EMBO J. 19, 4723–4733.PubMedCrossRefGoogle Scholar
  59. 58.
    Wakiyama, M., Imataka, H., and Sonenberg, N. (2000). Interaction of eIF4G with poly(A)-binding protein stimulates translation and is critical for Xenopus oocyte maturation. Curr Biol. 10, 1147–1150.PubMedCrossRefGoogle Scholar
  60. 59.
    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.PubMedGoogle Scholar
  61. 60.
    Voeltz, G.K., Ongkasuwan, J., Standart, N., and Steitz, J.A. (2001). A novel embryonic poly(A) binding protein, ePAB, regulates mRNA deadenylation in Xenopus egg extracts. Genes and Dev. 15, 774–778.PubMedCrossRefGoogle Scholar
  62. 61.
    Wormington, M., Searfoss, A., and Hurney, C. (1996). Overexpression of poly(A) binding protein prevents maturation-specific deadenylation and translational inactivation in Xenopus oocytes. EMBO J. 15, 900–909.PubMedGoogle Scholar
  63. 62.
    Stebbins-Boaz, B., Cao, Q., de Moor, C.H., Mendez, R., and Richter, J.D. (1999). Maskin is a CPEB-associated factor that transiently interacts with eIF-4E. Mol. Cell. 4, 1017–1027.PubMedCrossRefGoogle Scholar
  64. 63.
    Groisman, I., Huang, Y.-S., Mendez, R., Cao, Q., Therkauf, W., and Richter, J. (2000). CPEB, maskin, and cyclin B1 mRNA at the mitotic apparatus: Implications for local translational control of cell division. Cell. 103, 435–447.PubMedCrossRefGoogle Scholar
  65. 64.
    Minshall, N., Thom, G., and Standart, N. Conserved role of a DEAD-box helicase in mRNA masking. Submitted to RNA, 2001.Google Scholar
  66. 65.
    Ladomery, M., Wade, E., and Sommerville, J. (1997). Xp54, the Xenopus homologue of human RNA helicase p54, is an integral component of stored mRNP particles in oocytes. Nucl. Acids Res. 25, 965–973.PubMedCrossRefGoogle Scholar
  67. 66.
    Jankowsky, E., Gross, C.H., Shuman, S., and Pyle, A.M. (2001). Active disruption of an RNA-protein interaction by a DExH/D RNA helicase. Science. 291, 121–125.PubMedCrossRefGoogle Scholar
  68. 67.
    Dickson, K.S., Bilger, A., Ballantyne, S., and Wickens, M.P. (1999). The cleavage and polyadenylation specificity factor in Xenopus laevis oocytes is a cytoplasmic factor involved in regulated polyadenylation. Mol. Cell. Biol. 19, 5707–5717.PubMedGoogle Scholar
  69. 68.
    Mendez, R., Murthy, K.G.K., Ryan, K., Manley, J.L., and Richter, J.D. (2000). Phosphorylation of CPEB by Eg2 mediates the recruitment of CPSF into an active cytoplasmic polyadenylation complex. Mol. Cell. 6, 1253–1259.PubMedCrossRefGoogle Scholar
  70. 69.
    Paris, J., Swenson, K., Piwnica-Worms, H., and Richter, J.D. (1991). Maturation-specific polyadenylation: in vitro activation by p34cdc2 and phosphorylation of a 58kD CPE-binding protein. Genes Dev. 5, 1697–1708.PubMedCrossRefGoogle Scholar
  71. 70.
    Rechsteiner, M. and Rogers, S. (1996). PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21, 267–271.Google Scholar
  72. 70a.
    Reverse, C.G., Ahearn, M.D., and Hake, L.E. (2001). CPEB degradation during Xenopus oocyte maturation rewuires a PEST domain and the 26S proteasome. Dev. Biol. 231: 447–458.CrossRefGoogle Scholar
  73. 71.
    Shibuya, E.K., Boulton, T.G., Cobb, M.H., and Ruderman, J.V. (1992). Activation of p42 MAP kinase and the release of oocytes from cell cycle arrest. 11, 3963–3975.Google Scholar
  74. 72.
    Andresson, T. and Ruderman, J.V. (1998). The kinase Eg2 is a component of the Xenopus oocyte progesterone-activated signaling pathway. EMBO J. 17, 5627–5637.PubMedCrossRefGoogle Scholar
  75. 73.
    Frank-Vaillant, M., Haccard, O., Thibier, C., Ozon, R., Arlot-Bonnemains, Y., Prigent, C., and Jessus, C. (2000). Progesterone regulates the accumulation and the activation of Eg2 kinase in Xenopus oocytes. J. Cell Sci. 113, 1127–1138.PubMedGoogle Scholar
  76. 74.
    Howard, E.L., Charlesworth, A., Welk, J., and MacNicol, A.M. (1999). The mitogenactivated protein kinase signaling pathway stimulates mos mRNA cytoplasmic polyadenylation during Xenopus oocyte maturation. Mol. Cell. Biol. 19, 1990–1999.PubMedGoogle Scholar
  77. 75.
    Mendez, R., Hake, L.E., Andresson, T., Littlepage, L.E., Ruderman, J.V., and Richter, J.D. (2000). Phosphorylation of CPE binding factor by Eg2 regulates translation of cmos mRNA. Nature. 404, 302–307.PubMedCrossRefGoogle Scholar
  78. 76.
    Verrotti, A., Thompson, S., Wreden, C., Strickland, S., and Wickens, M. (1996). Evolutionary conservation of sequence elements controlling cytoplasmic polyadenylation. Proc. Natl. Acad. Sci. USA. 93, 9027–9032.PubMedCrossRefGoogle Scholar
  79. 77.
    Gunkel, N., Yano, T., Markussen, F.-H., Olsen, L.C., and Ephrussi, A. (1998). Localization-dependent translation requires a functional interaction between the 5’ and 3’ ends of oskar mRNA. Genes. Dev. 12, 1652–1664.PubMedCrossRefGoogle Scholar
  80. 78.
    Gavis, E.R., Lunsford, L., Bergsten, S.E., and Lehmann, R. (1996). A conserved 90 nucleotide element mediates translational repression of nanos RNA. Development. 122, 2791–2800.PubMedGoogle Scholar
  81. 79.
    Kim-Ha, J., Kerr, K., and Macdonald, P. (1995). Translational regulation of oskar mRNA by Bruno, an ovarian RNA-binding protein, is essential. Cell. 81, 403–412.PubMedCrossRefGoogle Scholar
  82. 80.
    Webster, P.J., Liang, L., Berg, C.A., Lasko, P., and Macdonald, P.M. (1997). Translational repressor bruno plays multiple roles in development and is widely conserved. Genes Dev. 11, 2510–2521.PubMedCrossRefGoogle Scholar
  83. 81.
    Micklem, D.R., Adams, J., Grunert, S., and St. Johnston, D. (2000). Distinct roles of two conserved Staufen domains in oskar mRNA localization and translation. EMBO J. 19, 1366–1377.PubMedCrossRefGoogle Scholar
  84. 82.
    Smibert, C., Lie, Y., Shillinglaw, W., Henzel, W., and Macdonald, P. (1999). Smaug, a novel and conserved protein, contributes to repression of nanos mRNA translation in vitro. RNA. 5, 1535–1547.PubMedCrossRefGoogle Scholar
  85. 83.
    Dahanukar, A., Walker, J.A., and Wharton, R.P. (1999). Smaug, a novel RNA-binding protein that operates a translational switch in Drosophila. Mol. Cell. 4, 209–218.PubMedCrossRefGoogle Scholar
  86. 84.
    Crucs, S., Chatterjee, S., and Gavis, E. (2000). Overlapping but distinct RNA elements control repression and activation of nanos translation. Mol Cell. 5, 457–467.PubMedCrossRefGoogle Scholar
  87. 85.
    Markussen, F.-H., Michon, A.-M., Breitwieser, W., and Ephrussi, A. (1995). Translational control of oskar generates Short OSK, the isoform that induces pole plasm assembly. Development. 121, 3723–3732.PubMedGoogle Scholar
  88. 86.
    Carrera, P., Johnstone, O., Nakamura, A., Casanova, J., Jackie, H., and Lasko, P. (2000). VASA mediates translation through interaction with a Drosophila yIF2 homolog. Mol Cell. 5, 181–187.PubMedCrossRefGoogle Scholar
  89. 87.
    Thompson, S., Goodwin, E., and Wickens, M. (2000). Rapid deadenylation and poly(A)-dependent translational repression mediated by the Caenorhabditis elegans tra-2 3’ untranslated region in the Xenopus embryos. Mol. Cell. Biol. 20, 2129–2137.PubMedCrossRefGoogle Scholar
  90. 88.
    Niessing, D., Dostatni, N., Jackie, H., and Rivera-Pomar, R. (1999). Sequence interval within the PEST motif of bicoid is important for translational repression of caudal mRNA in the anterior region of the Drosophila embryo. EMBO J. 18, 1966–1973.PubMedCrossRefGoogle Scholar
  91. 89.
    Rivera-Pomar, R., Niessing, D., Schmidt-Ott, U., Gehring, W.J., and Jackie, H. (1996). RNA binding and translational suppression by bicoid. Nature. 379, 746–749.PubMedCrossRefGoogle Scholar
  92. 90.
    Wharton, R.P., J., S., Lee, T., Patterson, M., and Murata, Y. (1998). The pumilio RNA-binding domain is also a translational repressor. Mol. Cell. 1, 863–872.Google Scholar
  93. 91.
    Ostareck-Lederer, A., Ostareck, D.H., Standart, N., and Thiele, B.J. (1994). Translation of 15-lipoxygenase mRNA is controlled by a protein that binds to a repeated sequence in the 3’ untranslated region. EMBO J. 13, 1476–1481.PubMedGoogle Scholar
  94. 92.
    Ostareck, D.H., Ostareck-Lederer, A., Shatsky, I.N., and Hentze, M.W. (2001). Lipoxygenase mRNA silencing in erythroid differentiation: The 3’UTR regulatory complex controls 60S ribosomal subunit joining. Cell 104, 281–290PubMedCrossRefGoogle Scholar
  95. 93.
    Wilhelm, J., Vale, R., and Hegde, R. (2000). Coordinate control of translation and localization of Vgl mRNA in Xenopus oocytes. Proc Natl Acad Sci U S A. 97, 13132–13137.PubMedCrossRefGoogle Scholar
  96. 94.
    Zhang, B., Gallegos, M., Puoti, A., Durkin, E., Fields, S., Kimble, J., and Wickens, M.P. (1997). A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature. 390, 477–484.PubMedCrossRefGoogle Scholar
  97. 95.
    Kraemer, B., Crittenden, S., Gallegos, M., Moulder, G., Barstead, R., Kimble, J., and Wickens, M. (1999). NANOS-3 and FBF proteins physically interact to control the sperm-oocyte switch in Caenorhabditis elegans. Curr. Biol. 9, 1009–1018.PubMedCrossRefGoogle Scholar
  98. 96.
    Jin, S.W., Kimble, J., and Ellis, R.E. (2001). Regulation of cell fate in Caenorhabditis elegans by a novel cytoplasmic polyadenylation element binding protein. Dev. Biol. 229, 537–553.PubMedCrossRefGoogle Scholar
  99. 97.
    Zamore, P., Williamson, J., and Lehmann, R. (1997). The pumilio protein binds RNA through a conserved domain that defines a new class of RNA-binding proteins. RNA. 3, 1421–1433.PubMedGoogle Scholar
  100. 98.
    Sonoda, J. and Wharton, R.P. (1999). Recruitment of Nanos to hunchback mRNA by Pumilio. Genes Dev. 13, 2704–2712.PubMedCrossRefGoogle Scholar
  101. 99.
    Spirin, A.S., On ‘masked’ forms of messenger RNA in early embryogenesis and in other differentiating systems. Current Topics in Developmetal Biology, ed. A.A. Moscona and A. Monroy. Vol. I. 1966, New York: Academic Press. 1–38.Google Scholar
  102. 100.
    Nakahata, S., Katsu, Y., Mita, K., Inoue, K., Nagakama, Y., and Yamashita, Y. (2001). Biochemical identification of Xenopus pumilioasa sequence-specific cyclin B1 mRNA-binding protein that physically interacts with a Nanos homolog, Xcat-2, and a cytoplasmic polyadenylation element-binding protein. J. Biol. Chem. 276: 20945–20953.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Nancy Standart
    • 1
  1. 1.Department of BiochemistryUniversity of CambridgeCambridgeUK

Personalised recommendations