Interaction between Ski7p and Upf1p is required for nonsense-mediated 3′-to-5′ mRNA decay in yeast

EMBO Journal

Volumn 22, Issue 15, 2003, Pages 3951-3959

  Takahashi, Shinya ^a   Araki, Yasuhiro ^a   Sakuno, Takeshi ^a   Katada, Toshiaki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Exosome; Nonsense mediated decay; Ski complex; Ski7p; Upf proteins

Indexed keywords

FUNGAL RNA; MESSENGER RNA; PROTEIN; PROTEIN SKI7P; PROTEIN UPF1P; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; CYTOPLASM; GENE OVEREXPRESSION; GENE SEQUENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; RNA DEGRADATION; SIGNAL TRANSDUCTION; YEAST;

BASE SEQUENCE; CYTOPLASM; GTP-BINDING PROTEINS; HYDROLYSIS; MOLECULAR SEQUENCE DATA; OLIGODEOXYRIBONUCLEOTIDES; PLASMIDS; PRECIPITIN TESTS; PROTEIN BINDING; RNA HELICASES; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 0041524062     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg374     Document Type: Article

References (50)

1. Allmang, C., Petfalski, E., Podtelejnikov, A., Mann, M., Tollervey, D. and Mitchell, P. (1999) The yeast exosome and human PM-Scl are related complexes of 3′ → 5′ exonucleases. Genes Dev., 13, 2148-2158.
2. Araki, Y., Takahashi, S., Kobayashi, T., Kajiho, H., Hoshino, S. and Katada, T. (2001) Ski7p G protein interacts with the exosome and the Ski complex for 3′-to-5′ mRNA decay in yeast. EMBO J., 20, 4684-4693.
3. Atkin, A.L., Schenkman, L.R., Eastham, M., Dahlseid, J.N., Lelivelt, M.J. and Culbertson, M.R. (1997) Relationship between yeast polyribosomes and Upf proteins required for nonsense mRNA decay. J. Biol. Chem., 272, 22163-22172.
4. Beelman, C.A., Stevens, A., Caponigro, G., LaGrandeur, T.E., Hatfield, L., Fortner, D.M. and Parker, R. (1996) An essential component of the decapping enzyme required for normal rates of mRNA turnover. Nature, 382, 642-646.
5. Brown, J.T., Bai, X. and Johnson, A.W. (2000) The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo. RNA, 6, 449-457.
6. Caponigro, G. and Parker, R. (1996) Mechanisms and control of mRNA turnover in Saccharomyces cerevisiae. Microbiol. Rev., 60, 233-249.
7. Chen, C.Y. et al. (2001) AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell, 107, 451-464.
8. Cui, Y., Hagan, K.W., Zhang, S. and Peltz, S.W. (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.
9. Czaplinski, K., Weng, Y., Hagan, K.W. and Peltz, S.W. (1995) Purification and characterization of the Upf1 protein: a factor involved in translation and mRNA degradation. RNA, 1, 610-623.
10. Czaplinski, K., Ruiz-Echevarria, M.J., Paushkin, S.V., Han, X., Weng, Y., Perlick, H.A., Dietz, H.C., Ter-Avanesyan, M.D. and Peltz, S.W. (1998) The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev., 12, 1665-1677.
11. Czaplinski, K., Ruiz-Echevarria, M.J., Gonzalez, C.I. and Peltz, S.W. (1999) Should we kill the messenger? The role of the surveillance complex in translation termination and mRNA turnover. BioEssays, 21, 685-696.
12. Decker, C.J. and Parker, R. (1993) A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev., 7, 1632-1643.
13. Frischmeyer, P.A., van Hoof, A., O'Donnell, K., Guerrerio, A.L., Parker, R. and Dietz, H.C. (2002) An mRNA surveillance mechanism that eliminates transcripts lacking termination codons. Science, 295, 2258-2261.
14. Goldstein, A.L. and McCusker, J.H. (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast, 15, 1541-1553.
15. Gonzalez, C.I., Ruiz-Echevarria, M.J., Vasudevan, S., Henry, M.F. and Peltz, S.W. (2000) The yeast hnRNP-like protein Hrp1/Nab4 marks a transcript for nonsense-mediated mRNA decay. Mol. Cell, 5, 489-499.
16. He, F. and Jacobson, A. (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.
17. He, F., Brown, A.H. and Jacobson, A. (1997) Upf1p, Nmd2p, and Upf3p are interacting components of the yeast nonsense-mediated mRNA decay pathway. Mol. Cell. Biol., 17, 1580-1594.
18. Hilleren, P. and Parker, R. (1999) Mechanisms of mRNA surveillance in eukaryotes. Annu. Rev. Genet., 33, 229-260.
19. Hsu, C.L. and Stevens, A. (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.
20. Jacobs Anderson, A.R. and Parker, R. (1998) The 3′ to 5′ degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3′ to 5′ exonucleases of the exosome complex. EMBO J., 17, 1497-1506.
21. 1-to-S transition encodes a protein containing an A-kinase target site and GTPase domain. EMBO J., 7, 1175-1182.
22. Knop, M., Siegers, K., Pereira, G., Zachariae, W., Winsor, B., Nasmyth, K. and Schiebel, E. (1999) Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast, 15, 963-972.
23. Lee, B.S. and Culbertson, M.R. (1995) Identification of an additional gene required for eukaryotic nonsense mRNA turnover. Proc. Natl Acad. Sci. USA, 92, 10354-10358.
24. Leeds, P., Peltz, S.W., Jacobson, A. and Culbertson, M.R. (1991) The product of the yeast UPF1 gene is required for rapid turnover of mRNAs containing a premature translational termination codon. Genes Dev., 5, 2303-2314.
25. Lykke-Andersen, J., Shu, M.D. and Steitz, J.A. (2000) Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell, 103, 1121-1131.
26. Maderazo, A.B., He, F., Mangus, D.A. and Jacobson, A. (2000) Upf1p control of nonsense mRNA translation is regulated by Nmd2p and Upf3p. Mol. Cell. Biol., 20, 4591-4603.
27. Mendell, J.T., Medghalchi, S.M., Lake, R.G., Noensie, E.N. and Dietz, H.C. (2000) Novel Upf2p orthologues suggest a functional link between translation initiation and nonsense surveillance complexes. Mol. Cell. Biol., 20, 8944-8957.
28. Mitchell, P. and Tollervey, D. (2000) mRNA stability in eukaryotes. Curr. Opin. Genet. Dev., 10, 193-198.
29. Mitchell, P., Petfalski, E. and Tollervey, D. (1996) The 3′ end of yeast 5.8S rRNA is generated by an exonuclease processing mechanism. Genes Dev., 10, 502-513.
30. Mitchell, P., Petfalski, E., Shevchenko, A., Mann, M. and Tollervey, D. (1997) The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′ → 5′ exoribonucleases. Cell, 91, 457-466.
31. Muhlrad, D. and Parker, R. (1992) Mutations affecting stability and deadenylation of the yeast MFA2 transcript. Genes Dev., 6, 2100-2111.
32. Muhlrad, D. and Parker, R. (1994) Premature translational termination triggers mRNA decapping. Nature, 370, 578-581.
33. Muhlrad, D., Decker, C.J. and Parker, R. (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.
34. Muhlrad, D., Decker, C.J. and Parker, R. (1995) Turnover mechanisms of the stable yeast PGKI mRNA. Mol. Cell. Biol., 15, 2145-2156.
35. Mukherjee, D., Gao, M., O'Connor, J.P., Raijmakers, R., Pruijn, G., Lutz, C.S. and Wilusz, J. (2002) The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements. EMBO J., 21, 165-174.
36. Page, M.F., Carr, B., Anders, K.R., Grimson, A. and Anderson, P. (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.
37. Peltz, S.W., Brown, A.H. and Jacobson, A. (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.
38. Perlick, H.A., Medghalchi, S.M., Spencer, F.A., Kendzior, R.J., Jr and Dietz, H.C. (1996) Mammalian orthologues of a yeast regulator of nonsense transcript stability. Proe. Natl Acad. Sci. USA, 93, 10928-10932.
39. Pulak, R. and Anderson, P. (1993) mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Dev., 7, 1885-1897.
40. Ruiz-Echevarria, M.J. and Peltz, S.W. (2000) The RNA binding protein Pub1 modulates the stability of transcripts containing upstream open reading frames. Cell, 101, 741-751.
41. Serin, G., Gersappe, A., Black, J.D., Aronoff, R. and Maquat, L.E. (2001) Identification and characterization of human orthologues to Saccharomyces cerevisiae Upf2 protein and Upf3 protein (Caenorhabditis elegans SMG-4). Mol. Cell. Biol., 21, 209-223.
42. Shirley, R.L., Lelivelt, M.J., Schenkman, L.R., Dahlseid, J.N. and Culbertson, M.R. (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.
43. Tharun, S. and Parker, R. (1999) Analysis of mutations in the yeast mRNA decapping enzyme. Genetics, 151, 1273-1285.
44. van Hoof, A., Staples, R.R., Baker, R.E. and Parker, R. (2000) Function of the Ski4p (Cs14p) and Ski7p proteins in 3′-to-5′ degradation of mRNA. Mol. Cell. Biol., 20, 8230-8243.
45. van Hoof, A., Frischmeyer, P.A., Dietz, H.C. and Parker, R. (2002) Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science, 295, 2262-2264.
46. Wang, W., Czaplinski, K., Rao, Y. and Peltz, S.W. (2001) The role of Upf proteins in modulating the translation read-through of nonsense-containing transcripts. EMBO J., 20, 980-990.
47. Wang, Z. and Kiledjian, M. (2001) Functional link between the mammalian exosome and mRNA decapping. Cell, 107, 751-762.
48. Weng, Y., Czaplinski, K. and Peltz, S.W. (1996a) Genetic and biochemical characterization of mutations in the ATPase and helicase regions of the Upf1 protein. Mol. Cell. Biol., 16, 5477-5490.
49. Weng, Y., Czaplinski, K. and Peltz, S.W. (1996b) 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.
50. Zhang, S., Ruiz-Echevarria, M.J., Quan, Y. and Peltz, S.W. (1995) Identification and characterization of a sequence motif involved in nonsense-mediated mRNA decay. Mol. Cell. Biol., 15, 2231-2244.