Caspase Cleavage of Initiation Factor 4E-Binding Protein 1 Yields a Dominant Inhibitor of Cap-Dependent Translation and Reveals a Novel Regulatory Motif

REFERENCES

• Beretta, L., A.-C. Gingras, Y. V. Svitkin, M. N. Hall, and N. Sonenberg. 1996. Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent translation. EMBO J. 15: 658–664.
   PubMed Web of Science ®Google Scholar
• Brunn, G. J., C. C. Hudson, A. Sekulic, J. M. Williams, H. Hosoi, P. J. Houghton, J. C. Lawrence, and R. T. Abraham. 1997. Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 277: 99–101.
   PubMed Web of Science ®Google Scholar
• Burnett, P. E., R. K. Barrow, N. A. Cohen, S. H. Snyder, and D. M. 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
• Bushell, M., L. McKendrick, R. U. Jaenicke, M. J. Clemens, and S. J. Morley. 1999. Caspase-3 is necessary and sufficient for cleavage of protein synthesis eukaryotic initiation factor 4G during apoptosis. FEBS Lett. 451: 332–336.
   PubMedGoogle Scholar
• Bushell, M., D. Poncet, W. E. Marissen, H. Flotow, R. E. Lloyd, M. J. Clemens, and S. J. Morley. 2000. Cleavage of polypeptide chain initiation factor eIF4GI during apoptosis in lymphoma cells: characterisation of an internal fragment by caspase-3-mediated cleavage. Cell Death Differ. 7: 628–636.
   PubMedGoogle Scholar
• Bushell, M., W. Wood, M. J. Clemens, and S. J. Morley. 2000. Changes in integrity and association of eukaryotic protein synthesis initiation factors during apoptosis. Eur. J. Biochem. 267: 1083–1091.
   PubMedGoogle Scholar
• Clemens, M. J., M. Bushell, I. W. Jeffrey, V. M. Pain, and S. J. Morley. 2000. Translation initiation factor modifications and the regulation of protein synthesis in apoptotic cells. Cell Death Differ. 7: 603–615.
   PubMed Web of Science ®Google Scholar
• Clemens, M. J., M. Bushell, and S. J. Morley. 1998. Degradation of eukaryotic polypeptide chain initiation factor (eIF) 4G in response to induction of apoptosis in human lymphoma cell lines. Oncogene 17: 2921–2931.
   PubMedGoogle Scholar
• Coldwell, M. J., S. A. Mitchell, M. Stoneley, M. MacFarlane, and A. E. Willis. 2000. Initiation of APAF-1 translation by internal ribosome entry. Oncogene 19: 899–905.
   PubMed Web of Science ®Google Scholar
• Gingras, A.-C., S. P. Gygi, B. Raught, R. D. Polakiewicz, R. T. Abraham, M. F. Hoekstra, R. Aebersold, and N. Sonenberg. 1999. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev. 13: 1422–1437.
   PubMed Web of Science ®Google Scholar
• Gingras, A.-C., B. Raught, and N. Sonenberg. 1999. eIF4 translation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68: 913–963.
   PubMed Web of Science ®Google Scholar
• Gout, I., T. Minami, K. Hara, Y. Tsujishita, V. Filonenko, M. D. Waterfield, and K. Yonezawa. 1998. Molecular cloning and characterization of a novel p70 S6 kinase, p70 S6 kinase β containing a proline-rich region. J. Biol. Chem. 273: 30061–30064.
   PubMedGoogle Scholar
• Haghighat, A., S. Mader, A. Pause, and N. Sonenberg. 1995. Repression of cap-dependent translation by 4E-binding protein 1: competition with p220 for binding to eukaryotic initiation factor-4E. EMBO J. 14: 5701–5709.
   PubMed Web of Science ®Google Scholar
• Hall-Jackson, C. A., D. A. Cross, N. Morrice, and C. Smythe. 1999. ATR is a caffeine-sensitive, DNA-activated protein kinase with a substrate specificity distinct from DNA-PK. Oncogene 18: 6707–6713.
   PubMed Web of Science ®Google Scholar
• Henis-Korenblit, S., N. Levy-Strumpf, D. Goldstaub, and A. Kimchi. 2000. A novel form of DAP5 protein accumulates in apoptotic cells as a result of caspase cleavage and internal ribosome entry site-mediated translation. Mol. Cell. Biol. 20: 496–506.
   PubMedGoogle Scholar
• Hibi, M., A. Lin, T. Smeal, A. Minden, and M. Karin. 1993. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev. 7: 2135–2148.
   PubMed Web of Science ®Google Scholar
• Holcik, M., C. Lefebvre, C. Yeh, T. Chow, and R. G. Korneluk. 1999. A new internal-ribosome-entry-site motif potentiates XIAP-mediated cytoprotection. Nat. Cell Biol. 1: 190–192.
   PubMed Web of Science ®Google Scholar
• Holcik, M., N. Sonenberg, and R. G. Korneluk. 2000. Internal ribosome initiation of translation and the control of cell death. Trends Genet. 16: 469–473.
   PubMedGoogle Scholar
• Huang, T. S., M. L. Kuo, J. Y. Shew, Y. W. Chou, and W. K. Yang. 1996. Distinct p53-mediated G1/S checkpoint responses in two NIH3T3 subclone cells following treatment with DNA-damaging agents. Oncogene 13: 625–632.
   PubMedGoogle Scholar
• Karim, M. M., J. M. X. Hughes, J. Warricker, G. C. Scheper, C. G. Proud, and J. E. G. McCarthy. 2001. A quantitative molecular model for modulation of mammalian translation by the eIF4E-binding protein 1. J. Biol. Chem. 276: 20750–20757.
   Google Scholar
• Lawrence, J. C., and R. T. Abraham. 1997. PHAS/4E-BPs as regulators of mRNA translation and cell proliferation. Trends Biochem. Sci. 22: 345–349.
   PubMedGoogle Scholar
• Lin, T. A., and J. C. Lawrence. 1996. Control of the translational regulators PHAS-I and PHAS-II by insulin and cAMP in 3T3-L1 adipocytes. J. Biol. Chem. 271: 30199–30204.
   PubMedGoogle Scholar
• Mader, S., H. Lee, A. Pause, and N. Sonenberg. 1995. The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4γ and the translational repressors 4E-binding proteins. Mol. Cell. Biol. 15: 4990–4997.
   PubMed Web of Science ®Google Scholar
• Marissen, W. E., A. Gradi, N. Sonenberg, and R. E. Lloyd. 2000. Cleavage of eukaryotic initiation factor 4GII correlates with translation inhibition during apoptosis. Cell Death Differ. 7: 1234–1243.
   PubMedGoogle Scholar
• Marissen, W. E., Y. Guo, A. A. M. Thomas, R. L. Matts, and R. E. Lloyd. 2000. Identification of caspase 3-mediated cleavage and functional alteration of eukaryotic initiation factor 2α in apoptosis. J. Biol. Chem. 275: 9314–9323.
   PubMed Web of Science ®Google Scholar
• Marissen, W. E., and R. E. Lloyd. 1998. Eukaryotic translation initiation factor 4G is targeted for proteolytic cleavage by caspase-3 during inhibition of translation in apoptotic cells. Mol. Cell. Biol. 18: 7565–7574.
   PubMedGoogle Scholar
• Mathews, M. B., N. Sonenberg, and J. W. B. Hershey. 1997. Origins and targets of translational control, p. 1–30. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Morley, S. J., L. McKendrick, and M. Bushell. 1998. Cleavage of translation initiation factor 4G (eIF4G) during antiFas IgM-induced apoptosis does not require signalling through the p38 mitogen-activated protein (MAP) kinase. FEBS Lett. 438: 41–48.
   PubMed Web of Science ®Google Scholar
• Mothe-Satney, I., G. J. Brunn, L. P. McMahon, C. T. Capaldo, R. T. Abraham, and J. C. Lawrence. 2000. Mammalian target of rapamycin-dependent phosphorylation of PHAS-1 in four (S/T)P sites detected by phospho-specific antibodies. J. Biol. Chem. 275: 33836–33843.
   PubMedGoogle Scholar
• Mothe-Satney, I., D. Yang, P. Fadden, T. A. J. Haystead, and J. C. Lawrence. 2000. Multiple mechanisms control phosphorylation of PHAS-I in five (S/T)P sites that govern translational repression. Mol. Cell. Biol. 20: 3558–3567.
   PubMedGoogle Scholar
• Proud, C. G. 1992. Protein phosphorylation in translational control. Curr. Top. Cell Regul. 32: 243–369.
   PubMedGoogle Scholar
• Raught, B., A.-C. Gingras, and N. Sonenberg. 2000. Regulation of ribosome recruitment in eukaryotes, p. 245–293. In N. Sonenberg, J. W. B., Hershey,, and M. B. Mathews (ed.), Translational control of gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Redpath, N. T., N. T. Price, and C. G. Proud. 1996. Cloning and expression of cDNA encoding protein synthesis elongation factor-2 kinase. J. Biol. Chem. 271: 17547–17554.
   PubMedGoogle Scholar
• Rhoads, R. E. 1999. Signal transduction pathways that regulate eukaryotic protein synthesis. J. Biol. Chem. 274: 30337–30340.
   PubMed Web of Science ®Google Scholar
• Scheper, G. C., N. A. Morrice, and C. G. Proud. 2001. The MAP kinase signal-integrating kinase Mnk2 is an eIF4E kinase with high basal activity in mammalian cells. Mol. Cell. Biol. 21: 743–754.
   PubMed Web of Science ®Google Scholar
• Shima, H., M. Pende, Y. Chen, S. Fumagalli, G. Thomas, and S. C. 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
• Stoneley, M., S. A. Chappell, C. L. Jopling, M. Dickens, M. MacFarlane, and A. E. Willis. 2000. c-Myc protein synthesis is initiated from the internal ribosome entry segment during apoptosis. Mol. Cell. Biol. 20: 1162–1169.
   PubMed Web of Science ®Google Scholar
• Tee, A. R., and C. G. Proud. 2000. DNA damage causes inactivation of translational regulators linked to mTOR signalling. Oncogene 19: 3021–3031.
   PubMed Web of Science ®Google Scholar
• Tee, A. R., and C. G. Proud. 2001. Staurosporine inhibits phosphorylation of translational regulators linked to mTOR. Cell Death Differ. 8: 841–849.
   PubMedGoogle Scholar
• Yang, D., G. J. Brunn, and J. C. Lawrence. 1999. Mutational analysis of sites in the translational regulator, PHAS-I, that are selectively phosphorylated by mTOR. FEBS Lett. 453: 387–390.
   PubMedGoogle Scholar