Nonsense-Containing mRNAs That Accumulate in the Absence of a Functional Nonsense-Mediated mRNA Decay Pathway Are Destabilized Rapidly upon Its Restitution

REFERENCES

• Atkin, A., L. Schenkman, M. Eastham, J. Dahlseid, M. Lelivelt, and M. Culbertson. 1997. Relationship between yeast polyribosomes and Upf proteins required for nonsense mRNA decay. J. Biol. Chem. 272: 22163–22172.
   PubMedGoogle Scholar
• Atkin, A., N. Altamura, P. Leeds, and M. Culbertson. 1995. The majority of yeast UPF1 colocalizes with polyribosomes in the cytoplasm. Mol. Cell. Biol. 6: 611–625.
   Google Scholar
• Beelman, C., A. Stevens, G. Caponigro, T. LaGrandeur, L. Hatfield, and R. Parker. 1996. An essential component of the decapping enzyme required for normal rates of mRNA turnover. Nature 382: 642–646.
   PubMedGoogle Scholar
• Belk, J., F. He, and A. Jacobson. 1999. Overexpression of truncated Nmd3p inhibits protein synthesis in yeast. RNA 5: 1055–1070.
   PubMedGoogle Scholar
• Benard, L., K. Carroll, R. Valle, and R. Wickner. 1998. Ski6p is a homolog of RNA-processing enzymes that affects translation of non-poly(A) mRNAs and 60S ribosomal subunit biogenesis. Mol. Cell. Biol. 18: 2688–2696.
   PubMedGoogle Scholar
• Bonetti, B., L. Fu, J. Moon, and D. M. Bedwell. 1995. The efficiency of translation termination is determined by a synergistic interplay between upstream and downstream sequences in Saccharomyces cerevisiae. J. Mol. Biol. 251: 334–345.
   PubMed Web of Science ®Google Scholar
• Carter, M., S. Li, and M. Wilkinson. 1996. A splicing-dependent regulatory mechanism that detects translation signals. EMBO J. 15: 5965–5975.
   PubMedGoogle Scholar
• Cheng, J., M. Fogel-Petrovic, and L. Maquat. 1990. Translation to near the distal end of the penultimate exon is required for normal levels of spliced triosephosphate isomerase mRNA. Mol. Cell. Biol. 10: 5215–5225.
   PubMedGoogle Scholar
• Cheng, J., and L. 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.
   PubMedGoogle Scholar
• Chin, K., and A. M. Pyle. 1995. Branch-point attack in group II introns is a highly reversible transesterification, providing a potential proofreading mechanism for 5′-splice site selection. RNA 1: 391–406.
   PubMed Web of Science ®Google Scholar
• Christianson, T. W., R. S. Sikorski, M. Dante, J. H. Shero, and P. Hieter. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119–122.
   PubMed Web of Science ®Google Scholar
• Cui, Y., K. Hagan, S. Zhang, and S. Peltz. 1995. Identification and characterization of genes that are required for the accelerated degradation of mRNAs containing a premature translational termination codon. Genes Dev. 9: 423–436.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Czaplinski, K., M. Ruiz-Echevarria, C. Gonzalez, and S. Peltz. 1999. Should we kill the messenger? The role of the surveillance complex in translation termination and mRNA turnover. Bioessays 21: 685–696.
   PubMedGoogle Scholar
• Daar, I., and L. Maquat. 1988. Premature translation termination mediates triosephosphate isomerase mRNA degradation. Mol. Cell. Biol. 8: 802–813.
   PubMed Web of Science ®Google Scholar
• Feinberg, A., and B. Vogelstein. 1983. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132: 6–13.
   PubMed Web of Science ®Google Scholar
• Freist, W., H. Sternbach, and F. Cramer. 1996. Phenylalanyl-tRNA synthetase from yeast and its discrimination of 19 amino acids in aminoacylation of tRNA(Phe)-C-C-A and tRNA(Phe)-C-C-A(3′NH2). Eur. J. Biochem. 240: 526–531.
   PubMedGoogle Scholar
• Gonzalez, C., M. Ruiz-Echevarria, S. Vasudevan, M. Henry, and S. Peltz. 2000. The yeast hnRNP-like protein Hrp1/Nab4 marks a transcript for nonsense-mediated mRNA decay. Mol. Cell 3: 489–499.
   Google Scholar
• Gottesman, S., R. Wickner, and M. R. Maurizi. 1997. Protein quality control: triage by chaperones and proteases. Genes Dev. 11: 815–823.
   PubMedGoogle Scholar
• Gozalbo, D., and S. Hohmann. 1990. Nonsense suppressors partially revert the decrease of the mRNA level of a nonsense mutant allele in yeast. Curr. Genet. 17: 77–79.
   PubMedGoogle Scholar
• Hagan, K., M. Ruiz-Echevarria, Y. Quan, and S. Peltz. 1995. Characterization of cis-acting sequences and decay intermediates involved in nonsense-mediated mRNA turnover. Mol. Cell. Biol. 15: 809–823.
   PubMedGoogle Scholar
• Hargrove, J. L., and F. H. Schmidt. 1989. The role of mRNA and protein stability in gene expression. FASEB J. 3: 2360–2370.
   PubMed Web of Science ®Google Scholar
• Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• He, F., and A. Jacobson. 1995. Identification of a novel component of the nonsense-mediated mRNA decay pathway by use of an interacting protein screen. Genes Dev. 9: 437–454.
   PubMedGoogle Scholar
• He, F., S. Peltz, J. Donahue, M. Rosbash, and A. Jacobson. 1993. Stabilization and ribosome association of unspliced pre-mRNAs in a yeast upf1 − mutant. Proc. Natl. Acad. Sci. USA 90: 7034–7038.
   PubMed Web of Science ®Google Scholar
• He, F., A. Brown, and A. Jacobson. 1996. Interaction between Nmd2p and Upf1p is required for activity but not for dominant-negative inhibition of the nonsense-mediated mRNA decay pathway in yeast. RNA 2: 153–170.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Henry, M., C. Z. Borland, M. Bossie, and P. A. Silver. 1996. Potential RNA binding proteins in Saccharomyces cerevisiae identified as suppressors of temperature-sensitive mutations in NPL3. Genetics 142: 103–115.
   PubMed Web of Science ®Google Scholar
• Herrick, D., R. Parker, and A. Jacobson. 1990. Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol. Cell. Biol. 10: 2269–2284.
   PubMed Web of Science ®Google Scholar
• Hilleren, P., and R. Parker. 1999. Mechanisms of mRNA surveillance in eukaryotes. Annu. Rev. Genet. 33: 229–260.
   PubMedGoogle Scholar
• Holstege, F., E. Jennings, J. Wyrick, T. Lee, C. Hengartner, M. Green, T. Golub, E. Lander, and R. Young. 1998. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95: 717–728.
   PubMed Web of Science ®Google Scholar
• Hsu, C., and A. Stevens. 1993. Yeast cells lacking 5′→3′ exoribonuclease 1 contain mRNA species that are poly(A) deficient and partially lack the 5′ cap structure. Mol. Cell. Biol. 13: 4826–4835.
   PubMedGoogle Scholar
• Iborra, F. J., D. A. Jackson, and P. R. Cook. 2001. Coupled transcription and translation within nuclei of mammalian cells. Science 293: 1139–1142.
   PubMed Web of Science ®Google Scholar
• Ishigaki, Y., X. Li, G. Serin, and L. E. 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: 607–617.
   PubMed Web of Science ®Google Scholar
• Jacobson, A., and S. W. Peltz. 1996. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu. Rev. Biochem. 65: 693–739.
   PubMed Web of Science ®Google Scholar
• Jacobson, A., and S. W. Peltz. 2000. Destabilization of nonsense-containing transcripts in Saccharomyces cerevisiae, p. 827–847. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control, 2nd ed. Cold Spring Harbor Laboratory Press, N.Y.
   Google Scholar
• Jeon, C., and K. Agarwal. 1996. Fidelity of RNA polymerase II transcription controlled by elongation factor TFIIS. Proc. Natl. Acad. Sci. USA 93: 13677–13682.
   PubMed Web of Science ®Google Scholar
• Kessler, M. M., M. F. Henry, E. Shen, J. Zhao, S. Gross, and P. A. Silver. 1997. Hrp1p, a sequence-specific RNA-binding protein that shuttles between the nucleus and the cytoplasm, is required for mRNA 3′-end formation in yeast. Genes Dev. 11: 2545–2556.
   PubMedGoogle Scholar
• Kessler, O., and L. A. Chasin. 1996. Effects of nonsense mutations on nuclear and cytoplasmic adenine phosphoribosyltransferase RNA. Mol. Cell. Biol. 16: 4426–4435.
   PubMedGoogle Scholar
• Kim, V. N., N. Kataoka, and G. Dreyfuss. 2001. Role of the nonsense-mediated decay factor hUpf3 in the splicing-dependent exon-exon junction complex. Science 293: 1832–1836.
   PubMedGoogle Scholar
• Kugler, W., J. Enssle, M. W. Hentze, and A. E. Kulozik. 1995. Nuclear degradation of nonsense mutated beta-globin mRNA: a post-transcriptional mechanism to protect heterozygotes from severe clinical manifestations of beta-thalassemia? Nucleic Acids Res. 23: 413–418.
   PubMed Web of Science ®Google Scholar
• Laemmli, U. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685.
   PubMed Web of Science ®Google Scholar
• LaGrandeur, T., and R. Parker. 1998. Isolation and characterization of Dcp1p, the yeast mRNA decapping enzyme. EMBO J. 17: 1487–1496.
   PubMedGoogle Scholar
• Lee, B., and M. Culbertson. 1995. Identification of an additional gene required for eukaryotic nonsense mRNA turnover. Proc. Natl. Acad. Sci. USA 92: 10354–10358.
   PubMedGoogle Scholar
• Leeds, P., J. Wood, B. Lee, and M. Culbertson. 1992. Gene products that promote mRNA turnover in Saccharomyces cerevisiae. Mol. Cell. Biol. 12: 2165–2177.
   PubMed Web of Science ®Google Scholar
• Leeds, P., S. Peltz, A. Jacobson, and M. Culbertson. 1991. The product of the yeast UPF1 gene is required for rapid turnover of mRNAs containing a premature translational termination codon. Genes Dev. 5: 2203–2314.
   Google Scholar
• Le Hir, H., M. J. Moore, and L. E. Maquat. 2000. Pre-mRNA splicing alters mRNP composition: evidence for stable association of proteins at exon-exon junctions. Genes Dev. 14: 1098–1108.
   PubMedGoogle Scholar
• Le Hir, H., E. Izaurralde, L. E. Maquat, and M. J. Moore. 2000. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 19: 6860–6869.
   PubMed Web of Science ®Google Scholar
• Losson, R., and F. Lacroute. 1979. Interference of nonsense mutations with eukaryotic messenger RNA stability. Proc. Natl. Acad. Sci. USA 76: 5134–5137.
   PubMed Web of Science ®Google Scholar
• Lozano, F., B. Maertzdorf, R. Pannell, and C. Milstein. 1994. Low cytoplasmic mRNA levels of immunoglobulin kappa light chain genes containing nonsense codons correlate with inefficient splicing. EMBO J. 13: 4617–4622.
   PubMedGoogle Scholar
• Lykke-Andersen, J., M. D. Shu, and J. A. Steitz. 2001. Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1. Science 293: 1836–1839.
   PubMed Web of Science ®Google Scholar
• Maderazo, A., F. He, D. Mangus, and A. Jacobson. 2000. Upf1p control of nonsense mRNA translation is regulated by Nmd2p and Upf3p. Mol. Cell. Biol. 20: 4591–4603.
   PubMedGoogle Scholar
• Mangus, D., and A. Jacobson. 1999. Linking mRNA turnover and translation: assessing the polyribosomal association of mRNA decay factors and degradative intermediates. Methods 17: 28–37.
   PubMedGoogle Scholar
• Maquat, L., A. Kinniburgh, E. Rachmilewitz, and J. Ross. 1981. Unstable beta-globin mRNA in mRNA-deficient beta0 thalassemia. Cell 27: 543–553.
   PubMed Web of Science ®Google Scholar
• Maquat, L. 1995. When cells stop making sense: effects of nonsense codons on RNA metabolism in vertebrate cells. RNA 1: 453–465.
   PubMed Web of Science ®Google Scholar
• 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 translation, p. 849–868. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control, 2nd ed. Cold Spring Harbor Laboratory Press, N.Y.
   Google Scholar
• Minvielle-Sebastia, L., K. Beyer, A. M. Krecic, R. E. Hector, M. S. Swanson, and W. Keller. 1998. Control of cleavage site selection during mRNA 3′ end formation by a yeast hnRNP. EMBO J. 17: 7454–7468.
   PubMedGoogle Scholar
• Moriarty, P. M., C. C. Reddy, and L. E. Maquat. 1997. The presence of an intron within the rat gene for selenium-dependent glutathione peroxidase 1 is not required to protect nuclear RNA from UGA-mediated decay. RNA 3: 1369–1373.
   PubMedGoogle Scholar
• Moriarty, P. M., C. C. Reddy, and L. E. Maquat. 1998. Selenium deficiency reduces the abundance of mRNA for Se-dependent glutathione peroxidase 1 by a UGA-dependent mechanism likely to be nonsense codon-mediated decay of cytoplasmic mRNA. Mol. Cell. Biol. 18: 2932–2939.
   PubMed Web of Science ®Google Scholar
• Muhlrad, D., and R. Parker. 1994. Premature translation termination triggers mRNA decapping. Nature 370: 578–581.
   PubMed Web of Science ®Google Scholar
• Muhlrad, D., and R. Parker. 1999. Aberrant mRNAs with extended 3′ UTRs are substrates for rapid degradation by mRNA surveillance. RNA 5: 1299–1307.
   PubMed Web of Science ®Google Scholar
• Muhlrad, D., C. Decker, and R. Parker. 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.
   PubMed Web of Science ®Google Scholar
• Pederson, T. 2001. Is the nucleus in need of translation? Trends Cell Biol. 11: 395–397.
   PubMed Web of Science ®Google Scholar
• Peltz, S., C. Trotta, F. He, A. Brown, J. Donahue, E. Welch, and A. Jacobson. 1993. Identification of the cis-acting sequences and trans-acting factors involved in nonsense-mediated mRNA decay, p. 1–10. In A. Brown, M. Tuite, and J. McCarthy (ed.), Protein synthesis and targeting in yeast. Springer-Verlag, Berlin, German.
   Google Scholar
• Peltz, S., J. L. Donahue, and A. Jacobson. 1992. A mutation in the tRNA nucleotidyltransferase gene promotes stabilization of mRNAs in Saccharomyces cerevisiae. Mol. Cell. Biol. 12: 5778–5784.
   PubMedGoogle Scholar
• Peltz, S., A. Brown, and A. Jacobson. 1993. mRNA destabilization triggered by premature translational termination depends on at least three cis-acting sequence elements and one trans-acting factor. Genes Dev. 7: 1737–1754.
   PubMed Web of Science ®Google Scholar
• Pulak, R., and P. Anderson. 1993. mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Dev. 7: 1885–1897.
   PubMedGoogle Scholar
• Rajavel, K. S., and E. F. Neufeld. 2001. Nonsense-mediated decay of human HEXA mRNA. Mol. Cell. Biol. 21: 5512–5519.
   PubMedGoogle Scholar
• Rose, M., F. Winston, and P. Heiter. 1990. Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Ruiz-Echevarria, M. J., C. I. Gonzalez, and S. W. Peltz. 1998. Identifying the right stop: determining how the surveillance complex recognizes and degrades an aberrant mRNA. EMBO J. 17: 575–589.
   PubMedGoogle Scholar
• Sambrook, J., E. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Sanger, F., S. Nicklen, and A. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463–5467.
   PubMed Web of Science ®Google Scholar
• Shirley, R., M. Lelivelt, L. Schenkman, J. Dahlseid, and M. Culbertson. 1998. A factor required for nonsense-mediated mRNA decay in yeast is exported from the nucleus to the cytoplasm by a nuclear export signal sequence. J. Cell Sci. 111: 3129–3143.
   PubMedGoogle Scholar
• Sikorski, R., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19–27.
   PubMed Web of Science ®Google Scholar
• Soni, R., J. Carmichael, and J. Murray. 1993. Parameters affecting lithium acetate-mediated transformation of Saccharomyces cerevisiae and development of a rapid and simplified procedure. Curr. Genet. 24: 455–459.
   PubMedGoogle Scholar
• Stephenson, L., and L. Maquat. 1996. Cytoplasmic mRNA for human triosephosphate isomerase is immune to nonsense-mediated decay despite forming polysomes. Biochimie 78: 1043–1047.
   PubMedGoogle Scholar
• Stotz, A., and P. Linder. 1990. The ADE2 gene from Saccharomyces cerevisiae: sequence and new vectors. Gene 95: 91–98.
   PubMedGoogle Scholar
• Sun, X., P. M. Moriarty, and L. E. Maquat. 2000. Nonsense-mediated decay of glutathione peroxidase 1 mRNA in the cytoplasm depends on intron position. EMBO J. 19: 4734–4744.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Wang, Y., C. L. Liu, J. D. Storey, R. J. Tibshirani, D. Herschlag, and P. O. Brown. 2002. Precision and functional specificity in mRNA decay. Proc. Natl. Acad. Sci. USA 99: 5860–5865.
   PubMed Web of Science ®Google Scholar
• Welch, E., and A. Jacobson. 1999. An internal open reading frame triggers nonsense-mediated decay of the yeast SPT10 mRNA. EMBO J. 18: 6134–6145.
   PubMedGoogle Scholar
• Weng, Y., K. Czaplinski, and S. W. Peltz. 1996. Identification and characterization of mutations in the UPF1 gene that affect nonsense suppression and the formation of the Upf protein complex but not mRNA turnover. Mol. Cell. Biol. 16: 5491–5506.
   PubMed Web of Science ®Google Scholar
• Weng, Y., K. Czaplinski, and S. W. Peltz. 1996. Genetic and biochemical characterization of mutations in the ATPase and helicase regions of the Upf1 protein. Mol. Cell. Biol. 16: 5477–5590.
   PubMed Web of Science ®Google Scholar
• White, T., N. Arnheim, and H. Erlich. 1989. The polymerase chain reaction. Trends Genet. 5: 185–189.
   PubMed Web of Science ®Google Scholar
• Yarus, M. 1992. Proofreading, NTPases and translation: successful increase in specificity. Trends Biochem. Sci. 17: 171–174.
   PubMedGoogle Scholar
• Zecherle, G., S. Whelen, and B. Hall. 1996. Purines are required at the 5′ ends of newly initiated RNAs for optimal RNA polymerase III gene expression. Mol. Cell. Biol. 16: 5801–5810.
   PubMedGoogle Scholar
• Zhang, J., X. Sun, Y. Qian, J. P. LaDuca, and L. E. Maquat. 1998. At least one intron is required for the nonsense-mediated decay of triosephosphate isomerase mRNA: a possible link between nuclear splicing and cytoplasmic translation. Mol. Cell. Biol. 18: 5272–5283.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Zhang, S., M. J. Ruiz-Echevarria, Y. Quan, and S. W. Peltz. 1995. Identification and characterization of a sequence motif involved in nonsense-mediated mRNA decay. Mol. Cell. Biol. 15: 2231–2244.
   PubMedGoogle Scholar
• Zhang, S., E. Welch, K. Hogan, A. Brown, S. Peltz, and A. Jacobson. 1997. Polysome-associated mRNAs are substrates for the nonsense-mediated mRNA decay pathway in Saccharomyces cerevisiae. RNA 3: 234–244.
   PubMedGoogle Scholar
• Zieler, H. A., M. Walberg, and P. Berg. 1995. Suppression of mutations in two Saccharomyces cerevisiae genes by the adenovirus E1A protein. Mol. Cell. Biol. 15: 3227–3237.
   PubMed Web of Science ®Google Scholar