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Gene Expression

Rapid Deadenylation Triggered by a Nonsense Codon Precedes Decay of the RNA Body in a Mammalian Cytoplasmic Nonsense-Mediated Decay Pathway

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Pages 4805-4813 | Received 13 Mar 2003, Accepted 22 Apr 2003, Published online: 27 Mar 2023

REFERENCES

  • Baserga, S. J., and E. J. Benz, Jr. 1992. Beta-globin nonsense mutation: deficient accumulation of mRNA occurs despite normal cytoplasmic stability. Proc. Natl. Acad. Sci. USA 89: 2935–2939.
  • Beelman, C. A., and R. Parker. 1995. Degradation of mRNA in eukaryotes. Cell 81: 179–183.
  • Bogdan, J. A., C. Adams-Burton, D. L. Pedicord, D. A. Sukovich, P. A. Benfield, M. H. Corjay, J. K. Stoltenborg, and I. B. Dicker. 1998. Human carbon catabolite repressor protein (CCR4)-associative factor 1: cloning, expression and characterization of its interaction with the B-cell translocation protein BTG1. Biochem. J. 336: 471–481.
  • Cao, D., and R. Parker. 2003. Computational modeling and experimental analysis of nonsense-mediated decay in yeast. Cell 113: 533–545.
  • Carter, M. S., S. Li, and M. F. Wilkinson. 1996. A splicing-dependent regulatory mechanism that detects translation signals. EMBO J. 15: 5965–5975.
  • Chen, C. Y., R. Gherzi, S. E. Ong, E. L. Chan, R. Raijmakers, G. J. Pruijn, G. Stoecklin, C. Moroni, M. Mann, and M. Karin. 2001. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107: 451–464.
  • Chen, C. Y., and A. B. Shyu. 1994. Selective degradation of early-response-gene mRNAs: functional analyses of sequence features of the AU-rich elements. Mol. Cell. Biol. 14: 8471–8482.
  • Chen, C. Y., N. Xu, and A. B. Shyu. 1995. mRNA decay mediated by two distinct AU-rich elements from c-fos and granulocyte-macrophage colony-stimulating factor transcripts: different deadenylation kinetics and uncoupling from translation. Mol. Cell. Biol. 15: 5777–5788.
  • Cheng, J., and L. E. Maquat. 1993. Nonsense codons can reduce the abundance of nuclear mRNA without affecting the abundance of pre-mRNA or the half-life of cytoplasmic mRNA. Mol. Cell. Biol. 13: 1892–1902.
  • Czaplinski, K., M. J. Ruiz-Echevarria, S. V. Paushkin, X. Han, Y. Weng, H. A. Perlick, H. C. Dietz, M. D. Ter-Avanesyan, and S. W. Peltz. 1998. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev. 12: 1665–1677.
  • Frischmeyer, P., and H. Dietz. 1999. Nonsense-mediated mRNA decay in health and disease. Hum. Mol. Genet. 8: 1893–1900.
  • Grosset, C., C.-Y. A. Chen, N. Xu, N. Sonenberg, H. Jacquemin-Sablon, and A.-B. Shyu. 2000. A mechanism for translationally coupled mRNA turnover: interaction between the poly(A) tail and a c-fos RNA coding determinant via a protein complex. Cell 103: 29–40.
  • He, F., A. Brown, and A. Jacobson. 1997. Upf1p, Nmd2p, and Upf3p are interacting components of the yeast nonsense-mediated mRNA decay pathway. Mol. Cell. Biol. 17: 1580–1594.
  • Hentze, M. W., and A. E. Kulozik. 1999. A perfect message: RNA surveillance and nonsense-mediated decay. Cell 96: 307–310.
  • Hilleren, P., and R. Parker. 1999. mRNA surveillance in eukaryotes: kinetic proofreading of proper translation termination as assessed by mRNP domain organization? RNA 5: 711–719.
  • Hoshino, S., M. Imai, T. Kobayashi, N. Uchida, and T. Katada. 1999. The eukaryotic polypeptide chain releasing factor (eRF3/GSPT) carrying the translation termination signal to the 3′-poly(A) tail of mRNA. Direct association of erf3/GSPT with polyadenylate-binding protein. J. Biol. Chem. 274: 16677–16680.
  • Humphries, R. K., T. J. Ley, N. P. Anagnou, A. W. Baur, and A. W. Nienhuis. 1984. Beta O-39 thalassemia gene: a premature termination codon causes beta-mRNA deficiency without affecting cytoplasmic beta-mRNA stability. Blood 64: 23–32.
  • Ishigaki, Y., X. Li, G. Serin, and L. Maquat. 2001. Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell 106: 606–617.
  • Ishikawa, K., T. Nagase, M. Suyama, N. Miyajima, A. Tanaka, H. Kotani, N. Nomura, and O. Ohara. 1998. Prediction of the coding sequences of unidentified human genes. X. The complete sequences of 100 new cDNA clones from brain which can code for large proteins in vitro. DNA Res. 5: 169–176.
  • Li, S., and M. F. Wilkinson. 1998. Nonsense surveillance in lymphocytes? Immunity 8: 135–141.
  • Lim, S., J. Mullins, C. Chen, K. Gross, and L. Maquat. 1989. Novel metabolism of several beta zero-thalassemic beta-globin mRNAs in the erythroid tissues of transgenic mice. EMBO J. 8: 2613–2619.
  • Lim, S., C. Sigmund, K. Gross, and L. Maquat. 1992. Nonsense codons in human beta-globin mRNA result in the production of mRNA degradation products. Mol. Cell. Biol. 12: 1149–1161.
  • Loflin, P. T., C.-Y. A. Chen, N. Xu, and A.-B. Shyu. 1999. Transcriptional pulsing approaches for analysis of mRNA turnover in mammalian cells. Methods 17: 11–20.
  • Lykke-Andersen, J., M. D. Shu, and J. A. Steitz. 2000. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell 103: 1121–1131.
  • Maquat, L. E. 2000. Nonsense-mediated RNA decay in mammalian cells: a splicing dependent means to down-regulate the levels of mRNAs that prematurely terminate transcription, p. 849–868. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control of gene expression, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
  • Mendell, J., and H. Dietz. 2001. When the message goes awry: disease-producing mutations that influence mRNA content and performance. Cell 107: 411–414.
  • Mitchell, P., and D. Tollervey. 2003. An NMD pathway in yeast involving accelerated deadenylation and exosome-mediated 3′ to 5′ degradation. Mol. Cell 11: 1405–1413.
  • Muhlrad, D., and R. Parker. 1994. Premature translational termination triggers mRNA decapping. Nature 370: 578–581.
  • Mukherjee, D., M. Gao, J. P. O'Connor, R. Raijmakers, G. Pruijn, C. S. Lutz, and J. Wilusz. 2002. The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements. EMBO J. 21: 165–174.
  • Nagase, T., K. Ishikawa, R. Kikuno, M. Hirosawa, N. Nomura, and O. Ohara. 1999. Prediction of the coding sequences of unidentified human genes. XV. The complete sequences of 100 new cDNA clones from brain which can code for large proteins in vitro. DNA Res. 6: 337–345.
  • Neu-Yilik, G., N. H. Gehring, R. Thermann, U. Frede, M. W. Hentze, and A. E. Kulozik. 2001. Splicing and 3′ end formation in the definition of nonsense-mediated decay-competent human β-globin mRNPs. EMBO J. 20: 532–540.
  • Page, M. F., B. Carr, K. R. Anders, A. Grimson, and P. Anderson. 1999. SMG-2 is a phosphorylated protein required for mRNA surveillance in Caenorhabditis elegans and related to Upf1p of yeast. Mol. Cell. Biol. 19: 5943–5951.
  • Peltz, S. W., F. He, E. Welch, and A. Jacobson. 1994. Nonsense-mediated mRNA decay in yeast. Prog. Nucleic Acid Res. Mol. Biol. 47: 271–298.
  • Peng, S.-P., C.-Y. Chen, N. Xu, and A.-B. Shyu. 1998. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17: 3461–3470.
  • Sachs, A. B. 1993. Messenger RNA degradation in eukaryotes. Cell 74: 413–421.
  • Shyu, A.-B., J. G. Belasco, and M. G. Greenberg. 1991. Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay. Genes Dev. 5: 221–232.
  • Shyu, A.-B., J. A. Garcia-Sanz, and E. Mullner. 1996. Analysis of mRNA decay in mammalian cells, p. 450–462. In I. Lefkovits (ed.), The immunology methods manual. Academic Press, London, United Kingdom.
  • Shyu, A.-B., M. E. Greenberg, and J. G. Belasco. 1989. The c-fos mRNA is targeted for rapid decay by two distinct mRNA degradation pathways. Genes Dev. 3: 60–72.
  • Sun, X., H. A. Perlick, H. C. Dietz, and L. E. Maquat. 1998. A mutated human homologue to yeast Upf1 protein has a dominant-negative effect on the decay of nonsense containing mRNAs in mammalian cells. Proc. Natl. Acad. Sci. USA 95: 10009–10014.
  • Svitkin, Y. V., H. Imataka, K. Khaleghpour, A. Kahvejian, H. D. Liebig, and N. Sonenberg. 2001. Poly(A)-binding protein interaction with elF4G stimulates picornavirus IRES-dependent translation. RNA 7: 1743–1752.
  • Takeshita, K., B. G. Forget, A. Scarpa, and E. J. Benz. 1984. Intranuclear defect in beta-globin mRNA accumulation due to a premature translation termination codon. Blood 64: 13–22.
  • Thermann, R., G. Neu-Yilik, A. Deters, U. Frede, K. Wehr, C. Hagemeier, M. W. Hentze, and A. E. Kulozik. 1998. Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J. 17: 3484–3494.
  • Uchida, N., S.-I. Hoshino, H. Imataka, N. Sonenberg, and T. Katada. 2002. A novel role of the mammalian GSPT/eRF3 associating with poly(A)-binding protein in Cap/Poly(A)-dependent translation. J. Biol. Chem. 277: 50286–50292.
  • Urlaub, G., P. J. Mitchell, C. J. Ciudad, and L. A. Chasin. 1989. Nonsense mutations in the dihydrofolate reductase gene affect RNA processing. Mol. Cell. Biol. 9: 2868–2880.
  • Wakiyama, M., H. Imataka, and N. Sonenberg. 2000. Interaction of eIF4G with poly(A)-binding protein stimulates translation and is critical for Xenopus oocyte maturation. Curr. Biol. 10: 1147–1150.
  • Wang, W., K. Czaplinski, Y. Rao, and S. W. Peltz. 2001. The role of Upf proteins in modulating the translation read-through of nonsense-containing transcripts. EMBO J. 20: 880–890.
  • Wang, Z., N. Day, P. Trifillis, and M. Kiledjian. 1999. An mRNA stability complex functions with poly(A)-binding protein to stabilize mRNA in vitro. Mol. Cell. Biol. 19: 4552–4560.
  • Wang, Z., and M. Kiledjian. 2001. Functional link between the mammalian exosome and mRNA decapping. Cell 107: 751–762.
  • Wells, S. E., P. E. Hillner, R. D. Vale, and A. B. Sachs. 1998. Circularization of mRNA by eukaryotic translation initiation factors. Mol. Cell 2: 135–140.
  • Wilkinson, M., and A. Shyu. 2002. RNA surveillance by nuclear scanning? Nat. Cell Biol. 4: E144–E147.
  • Wilusz, C. W., M. Wormington, and S. W. Peltz. 2001. The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell Biol. 2: 237–246.
  • Xu, N., P. Loflin, C.-Y. A. Chen, and A.-B. Shyu. 1998. A broader role for AU-rich element-mediated mRNA turnover revealed by a new transcriptional pulse strategy. Nucleic Acids Res. 26: 558–565.
  • Zhang, J., X. Sun, Y. Qian, and L. E. Maquat. 1998. Intron function in the nonsense-mediated decay of beta-globin mRNA: indications that pre-mRNA splicing in the nucleus can influence mRNA translation in the cytoplasm. RNA 4: 801–815.

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