p70^S6K Controls Selective mRNA Translation during Oocyte Maturation and Early Embryogenesis in Xenopus laevis

REFERENCES

• Abraham, R. T., and J. Wiederrecht 1996. Immunopharmacology of rapamycin. Annu. Rev. Immunol. 14:483–510.
   PubMed Web of Science ®Google Scholar
• Alessi, D. R., M. T. Kozlowski, Q. P. Weng, N. Morrice, and J. Avruch 1998. 3-Phosphoinositide-dependent protein kinase 1 (PDK1) phosphorylates and activates the p70 S6 kinase in vivo and in vitro. Curr. Biol. 8:69–81.
   PubMed Web of Science ®Google Scholar
• Amaldi, F., I. Bozzoni, E. Beccari, and J. Pierandrei-Amaldi 1989. Expression of ribosomal protein genes and regulation of ribosome biosynthesis in Xenopus development. Trends Biochem. Sci. 14:175–178.
   PubMedGoogle Scholar
• Amaldi, F., O. Camacho-Vanegas, B. Cardinall, F. Cecconi, C. Crosio, F. Loreni, P. Mariottini, L. Pellizzoni, and J. Pierandrei-Amaldi 1995. Structure and expression of ribosomal protein genes in Xenopus laevis. Biochem. Cell Biol. 73:969–977.
   PubMedGoogle Scholar
• Amaldi, F., and J. Pierandrei-Amaldi 1997. TOP genes: a translationally controlled class of genes including those coding for ribosomal proteins. Prog. Mol. Subcell. Biol. 18:1–17.
   PubMedGoogle Scholar
• Amaldi, F., and J. Pierandrei-Amaldi 1990. Translational regulation of the expression of ribosomal protein genes in Xenopus laevis. Enzyme 44:93–105.
   PubMedGoogle Scholar
• Bandi, H. R., S. Ferrari, J. Krieg, H. E. Meyer, and J. Thomas 1993. Identification of 40 S ribosomal protein S6 phosphorylation sites in Swiss mouse 3T3 fibroblasts stimulated with serum. J. Biol. Chem. 268:4530–4533.
   PubMedGoogle Scholar
• Baum, E. Z., and J. Wormington 1985. Coordinate expression of ribosomal protein genes during Xenopus development. Dev. Biol. 111:488–498.
   PubMedGoogle Scholar
• Beretta, L., Y. V. Svitkin, and J. Sonenberg 1996. Rapamycin stimulates viral protein synthesis and augments the shutoff of host protein synthesis upon picornavirus infection. J. Virol. 70:8993–8996.
   PubMedGoogle Scholar
• Burnett, P. E., R. K. Barrow, N. A. Cohen, S. H. Snyder, and J. Sabatini 1998. RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc. Natl. Acad. Sci. USA 95:1432–1437.
   PubMed Web of Science ®Google Scholar
• Cardinali, B., N. Campioni, and J. Pierandrei-Amaldi 1987. Ribosomal protein, histone and calmodulin mRNAs are differently regulated at the translational level during oogenesis of Xenopus laevis. Exp. Cell Res. 169:432–441.
   PubMedGoogle Scholar
• Cardinali, B., M. Di Cristina, and J. Pierandrei-Amaldi 1993. Interaction of proteins with the mRNA for ribosomal protein L1 in Xenopus: structural characterization of in vivo complexes and identification of proteins that bind in vitro to its 5′UTR. Nucleic Acids Res. 21:2301–2308.
   PubMedGoogle Scholar
• Chen, M., and J. Cooper 1997. The beta subunit of CKII negatively regulates Xenopus oocyte maturation. Proc. Natl. Acad. Sci. USA 94:9136–9140.
   PubMedGoogle Scholar
• Chen, M., D. Li, E. G. Krebs, and J. Cooper 1997. The casein kinase II beta subunit binds to Mos and inhibits Mos activity. Mol. Cell. Biol. 17:1904–1912.
   PubMedGoogle Scholar
• Conus, N. M., B. A. Hemmings, and J. Pearson 1998. Differential regulation by calcium reveals distinct signaling requirements for the activation of Akt and p70S6k. J. Biol. Chem. 273:4776–4782.
   PubMedGoogle Scholar
• Dixon, L. K., and J. Ford 1982. Regulation of protein synthesis and accumulation during oogenesis in Xenopus laevis. Dev. Biol. 93:478–497.
   PubMed Web of Science ®Google Scholar
• Dumont, F. J., and J. Su 1996. Mechanism of action of the immunosuppressant rapamycin. Life Sci. 58:373–395.
   PubMed Web of Science ®Google Scholar
• Duncan, R., and J. McConkey 1982. Preferential utilization of phosphorylated 40-S ribosomal subunits during initiation complex formation. Eur. J. Biochem. 123:535–538.
   PubMedGoogle Scholar
• Duval, C., P. Bouvet, F. Omilli, C. Roghi, C. Dorel, R. LeGuellec, J. Paris, and J. Osborne 1990. Stability of maternal mRNA in Xenopus embryos: role of transcription and translation. Mol. Cell. Biol. 10:4123–4129.
   PubMedGoogle Scholar
• Erikson, E., and J. Maller 1989. In vivo phosphorylation and activation of ribosomal protein S6 kinases during Xenopus oocyte maturation. J. Biol. Chem. 264:13711–13717.
   PubMedGoogle Scholar
• Erikson, E., and J. Maller 1985. A protein kinase from Xenopus eggs specific for ribosomal protein S6. Proc. Natl. Acad. Sci. USA 82:742–746.
   PubMed Web of Science ®Google Scholar
• Erikson, E., and J. Maller 1986. Purification and characterization of a protein kinase from Xenopus eggs highly specific for ribosomal protein S6. J. Biol. Chem. 261:350–355.
   PubMedGoogle Scholar
• Erikson, E., J. L. Maller, and J. Erikson 1991. Xenopus ribosomal protein S6 kinase II. Methods Enzymol. 200:252–268.
   PubMedGoogle Scholar
• Gao, C., R. B. Arlinghaus, and J. Singh 1996. Further characterization of the c-mos transcript and its cell cycle specific expression in NIH3T3 cells. Oncogene 12:1571–1576.
   PubMedGoogle Scholar
• Gebauer, F., and J. Richter 1997. Synthesis and function of Mos: the control switch of vertebrate oocyte meiosis. Bioessays 19:23–28.
   PubMed Web of Science ®Google Scholar
• Graves, L. M., Y. Q. He, J. Lambert, D. Hunter, X. N. Li, and J. Earp 1997. An intracellular calcium signal activates P70 but not P90 ribosomal S6 kinase in liver epithelial cells. J. Biol. Chem. 272:1920–1928.
   PubMedGoogle Scholar
• Hartley, R. S., R. E. Rempel, and J. Maller 1996. In vivo regulation of the early embryonic cell cycle in Xenopus. Dev. Biol. 173:408–419.
   PubMedGoogle Scholar
• Hyman, L. E., and J. Wormington 1988. Translational inactivation of ribosomal protein mRNAs during Xenopus oocyte maturation. Genes Dev. 2:598–605.
   PubMed Web of Science ®Google Scholar
• Jefferies, H. B., S. Fumagalli, P. B. Dennis, C. Reinhard, R. B. Pearson, and J. Thomas 1997. Rapamycin suppresses 5′TOP mRNA translation through inhibition of p70s6k. EMBO J. 16:3693–3704.
   PubMed Web of Science ®Google Scholar
• Jefferies, H. B., C. Reinhard, S. C. Kozma, and J. Thomas 1994. Rapamycin selectively represses translation of the “polypyrimidine tract” mRNA family. Proc. Natl. Acad. Sci. USA 91:4441–4445.
   PubMed Web of Science ®Google Scholar
• Jefferies, H. B., and J. Thomas 1994. Elongation factor-1 alpha mRNA is selectively translated following mitogenic stimulation. J. Biol. Chem. 269:4367–4372.
   PubMedGoogle Scholar
• Jeffries, H. B. J., G. Thomas 1996. Ribosomal protein S6 phosphorylation and signal transduction, p. 389–409. In J. W. B. Hershey, M. B. Mathews, N. Sonenberg (ed.), Translational control Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Kawasome, H., P. Papst, S. Webb, G. M. Keller, G. L. Johnson, E. W. Gelfand, and J. Terada 1998. Targeted disruption of p70(s6k) defines its role in protein synthesis and rapamycin sensitivity. Proc. Natl. Acad. Sci. USA 95:5033–5038.
   PubMed Web of Science ®Google Scholar
• Kozak, M. 1986. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44:283–292.
   PubMed Web of Science ®Google Scholar
• Kuge, H., and J. Richter 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
• Lane, H. A., A. Fernandez, N. J. Lamb, and J. Thomas 1993. p70s6k function is essential for G1 progression. Nature 363:170–172.
   PubMed Web of Science ®Google Scholar
• Lane, H. A., S. J. Morley, M. Doree, S. C. Kozma, and J. Thomas 1992. Identification and early activation of a Xenopus laevis p70s6k following progesterone-induced meiotic maturation. EMBO J. 11:1743–1749.
   PubMedGoogle Scholar
• Laskey, R. A., A. D. Mills, J. B. Gurdon, and J. Partington 1977. Protein synthesis in oocytes of Xenopus laevis is not regulated by the supply of messenger RNA. Cell 11:345–351.
   PubMed Web of Science ®Google Scholar
• Lawrence, J. C. Jr., and J. Abraham 1997. PHAS/4E-BPs as regulators of mRNA translation and cell proliferation. Trends Biochem. Sci. 22:345–349.
   PubMedGoogle Scholar
• Loreni, F., and J. Amaldi 1997. Translational control of terminal oligopyrimidine mRNAs requires a specific regulator. FEBS Lett. 416:239–242.
   PubMedGoogle Scholar
• Maller, J. L. 1998. Recurring themes in oocyte maturation. Biol. Cell 90:453–460.
   PubMedGoogle Scholar
• Meyuhas, O., D. Avni, S. Shama 1996. Translational control of ribosomal protein mRNAs in eukaryotes, p. 363–388. In J. W. B. Hershey, M. B. Mathews, N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Moser, B. A., P. B. Dennis, N. Pullen, R. B. Pearson, N. A. Williamson, R. E. Wettenhall, S. C. Kozma, and J. Thomas 1997. Dual requirement for a newly identified phosphorylation site in p70S6K. Mol. Cell Biol. 17:5648–5655.
   PubMedGoogle Scholar
• Nakanishi, T., K. Kohno, M. Ishiura, H. Ohashi, and J. Uchida 1988. Complete nucleotide sequence and characterization of the 5′ flanking region of mammalian elongation factor 2 gene. J. Biol. Chem. 263:6384–6391.
   PubMed Web of Science ®Google Scholar
• Nielsen, P. J., G. Thomas, and J. Maller 1982. Increased phosphorylation of ribosomal protein S6 during meiotic maturation of Xenopus oocytes. Proc. Natl. Acad. Sci. USA 79:2937–2941.
   PubMedGoogle Scholar
• Nieuwkoop, P. D., J. Faber 1967. Normal table of Xenopus laevis (Daudin). North-Holland Publishing Co, Amsterdam, The Netherlands.
   Google Scholar
• Novak-Hofer, I., and J. Thomas 1984. An activated S6 kinase in extracts from serum- and epidermal growth factor-stimulated Swiss 3T3 cells. J. Biol. Chem. 259:5995–6000.
   PubMedGoogle Scholar
• Olivier, A. R., L. M. Ballou, and J. Thomas 1988. Differential regulation of S6 phosphorylation by insulin and epidermal growth factor in Swiss mouse 3T3 cells: insulin activation of type 1 phosphatase. Proc. Natl. Acad. Sci. USA 85:4720–4724.
   PubMed Web of Science ®Google Scholar
• Pearson, R. B., P. B. Dennis, J. W. Han, N. A. Williamson, S. C. Kozma, R. E. Wettenhall, and J. Thomas 1995. The principal target of rapamycin-induced p70s6k inactivation is a novel phosphorylation site within a conserved hydrophobic domain. EMBO J. 14:5279–5287.
   PubMedGoogle Scholar
• Pierandrei-Amaldi, P., N. Campioni, E. Beccari, I. Bozzoni, and J. Amaldi 1982. Expression of ribosomal-protein genes in Xenopus laevis development. Cell 30:163–171.
   PubMed Web of Science ®Google Scholar
• Pullen, N., P. B. Dennis, M. Andjelkovic, A. Dufner, S. C. Kozma, B. A. Hemmings, and J. Thomas 1998. Phosphorylation and activation of p70s6k by PDK1. Science 279:707–710.
   PubMed Web of Science ®Google Scholar
• Rebagliati, M. R., D. L. Weeks, R. P. Harvey, and J. Melton 1985. Identification and cloning of localized maternal RNAs from Xenopus eggs. Cell 42:769–777.
   PubMedGoogle Scholar
• Reinhard, C., G. Thomas, and J. Kozma 1992. A single gene encodes two isoforms of the p70 S6 kinase: activation upon mitogenic stimulation. Proc. Natl. Acad. Sci. USA 89:4052–4056.
   PubMedGoogle Scholar
• Richter, J. D., W. J. Wasserman, and J. Smith 1982. The mechanism for increased protein synthesis during Xenopus oocyte maturation. Dev. Biol. 89:159–167.
   PubMed Web of Science ®Google Scholar
• Roy, L. M., O. Haccard, T. Izumi, B. G. Lattes, A. L. Lewellyn, and J. Maller 1996. Mos proto-oncogene function during oocyte maturation in Xenopus. Oncogene 12:2203–2211.
   PubMed Web of Science ®Google Scholar
• Rupp, R. A., L. Snider, and J. Weintraub 1994. Xenopus embryos regulate the nuclear localization of XMyoD. Genes Dev. 8:1311–1323.
   PubMed Web of Science ®Google Scholar
• Sagata, N. 1997. What does Mos do in oocytes and somatic cells? Bioessays 19:13–21.
   PubMedGoogle Scholar
• Sagata, N., I. Daar, M. Oskarsson, S. D. Showalter, and J. Vande Woude 1989. The product of the mos proto-oncogene as a candidate “initiator” for oocyte maturation. Science 245:643–646.
   PubMed Web of Science ®Google Scholar
• Sagata, N., M. Oskarsson, T. Copeland, J. Brumbaugh, and J. Vande Woude 1988. Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. Nature 335:519–525.
   PubMed Web of Science ®Google Scholar
• Shima, H., M. Pende, Y. Chen, S. Fumagalli, G. Thomas, and J. Kozma 1998. Disruption of the p70s6k/p85s6k gene reveals a small mouse phenotype and a new functional S6 kinase. EMBO J. 17:6649–6659.
   PubMed Web of Science ®Google Scholar
• Stewart, M. J., and J. Thomas 1994. Mitogenesis and protein synthesis: a role for ribosomal protein S6 phosphorylation? Bioessays 16:809–815.
   PubMedGoogle Scholar
• Terada, N., H. R. Patel, K. Takase, K. Kohno, A. C. Nairn, and J. Gelfand 1994. Rapamycin selectively inhibits translation of mRNAs encoding elongation factors and ribosomal proteins. Proc. Natl. Acad. Sci. USA 91:11477–11481.
   PubMedGoogle Scholar
• Thomas, G., and J. Hall 1997. TOR signalling and control of cell growth. Curr. Opin. Cell Biol. 9:782–787.
   PubMed Web of Science ®Google Scholar
• Thomas, G., J. Martin-Perez, M. Siegmann, and J. Otto 1982. The effect of serum, EGF, PGF2 alpha and insulin on S6 phosphorylation and the initiation of protein and DNA synthesis. Cell 30:235–242.
   PubMed Web of Science ®Google Scholar
• Turner, D. L., and J. Weintraub 1994. Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev. 8:1434–1447.
   PubMed Web of Science ®Google Scholar
• Wettenhall, R. E., E. Erikson, and J. Maller 1992. Ordered multisite phosphorylation of Xenopus ribosomal protein S6 by S6 kinase II. J. Biol. Chem. 267:9021–9027.
   PubMedGoogle Scholar
• Woodland, H. R. 1974. Changes in the polysome content of developing Xenopus laevis embryos. Dev. Biol. 40:90–101.
   PubMed Web of Science ®Google Scholar
• Yew, N., M. L. Mellini, and J. Vande Woude 1992. Meiotic initiation by the mos protein in Xenopus. Nature 355:649–652.
   PubMed Web of Science ®Google Scholar