Genome-Wide Analysis of mRNAs Regulated by the Nonsense-Mediated and 5′ to 3′ mRNA Decay Pathways in Yeast

Molecular Cell

Volumn 12, Issue 6, 2003, Pages 1439-1452

  He, Feng ^a   Li, Xiangrui ^a,b   Spatrick, Phyllis ^a   Casillo, Ryan ^a,c   Dong, Shuyun ^a   Jacobson, Allan ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b NANJING AGRICULTURAL UNIVERSITY   (China)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ACCURACY; ARTICLE; CONTROLLED STUDY; DNA MICROARRAY; GENE CLUSTER; GENE DELETION; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENOME ANALYSIS; NONHUMAN; RNA DEGRADATION; STRAIN DIFFERENCE; TRANSCRIPTION REGULATION; YEAST CELL;

EID: 0347416978     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(03)00446-5     Document Type: Article

References (48)

1. Beelman C.A., Parker R. Degradation of mRNA in eukaryotes. Cell. 81:1995;179-183.
2. Beelman C.A., Stevens A., Caponigro G., LaGrandeur T.E., Hatfield L., Fortner D.M., Parker R. An essential component of the decapping enzyme required for normal rates of mRNA turnover. Nature. 382:1996;642-646.
3. Cao D., Parker R. Computational modeling of eukaryotic mRNA turnover. RNA. 7:2001;1192-1212.
4. Cao D., Parker R. Computational modeling and experimental analysis of nonsense-mediated decay in yeast. Cell. 113:2003;533-545.
5. Dahlseid J.N., Lew-Smith J., Lelivelt M.J., Enomoto S., Ford A., Desruisseaux M., McClellan M., Lue N., Culbertson M.R., Berman J. mRNAs encoding telomerase components and regulators are controlled by UPF genes in Saccharomyces cerevisiae. Eukaryot. Cell. 2:2003;134-142.
6. Decker C.J., Parker R. A turnover pathway for both stable and unstable mRNAs in yeast. evidence for a requirement for deadenylation Genes Dev. 7:1993;1632-1643.
7. Dunckley T., Parker R. The DCP2 protein is required for mRNA decapping in Saccharomyces cerevisiae and contains a functional MutT motif. EMBO J. 18:1999;5411-5422.
8. Eisen M.B., Spellman P.T., Brown P.O., Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA. 95:1998;14863-14868.
9. Farabaugh P.J., Zhao H., Vimaladithan A. A novel programmed frameshift expresses the POL3 gene of retrotransposon Ty3 of yeast. frameshifting without tRNA slippage Cell. 74:1993;93-103.
10. Frischmeyer P.A., van Hoof A., O'Donnell K., Guerrerio A.L., Parker R., Dietz H.C. An mRNA surveillance mechanism that eliminates transcripts lacking termination codons. Science. 295:2002;2258-2261.
11. Gonzalez C.I., Bhattacharya A., Wang W., Peltz S.W. Nonsense-mediated mRNA decay in Saccharomyces cerevisiae. Gene. 274:2001;15-25.
12. Harrison P., Kumar A., Lan N., Echols N., Snyder M., Gerstein M. A small reservoir of disabled ORFs in the yeast genome and its implications for the dynamics of proteome evolution. J. Mol. Biol. 316:2002;409-419.
13. He F., Jacobson A. Identification of a novel component of the nonsense-mediated mRNA decay pathway by use of an interacting protein screen. Genes Dev. 9:1995;437-454.
14. He F., Jacobson A. Upf1p, Nmd2p, and Upf3p regulate the decapping and exonucleolytic degradation of both nonsense-containing mRNAs and wild-type mRNAs. Mol. Cell. Biol. 21:2001;1515-1530.
15. He F., Peltz S.W., Donahue J.L., Rosbash M., Jacobson A. Stabilization and ribosome association of unspliced pre-mRNAs in a yeast upf1- mutant. Proc. Natl. Acad. Sci. USA. 90:1993;7034-7038.
16. He F., Brown A.H., Jacobson A. Upf1p, Nmd2p, and Upf3p are interacting components of the yeast nonsense-mediated mRNA decay pathway. Mol. Cell. Biol. 17:1997;1580-1594.
17. Herrick, D. (1989). Structural determinants of mRNA turnover in yeast. PhD thesis, University of Massachusetts Medical School, Worcester, Massachusetts.
18. Hsu C.L., Stevens A. 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. 13:1993;4826-4835.
19. Jacobs Anderson J.S., Parker R. 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. 17:1998;1497-1506.
20. Jacobson A., Peltz S.W. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu. Rev. Biochem. 65:1996;693-739.
21. Jacobson A., Peltz S.W. Destabilization of nonsense-containing transcripts in Saccharomyces cerevisiae. Sonenberg N., Hershey J.W.B., Mathews M.B. Translational Control of Gene Expression. 2000;827-847 Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
22. Leeds P., Peltz S.W., Jacobson A., Culbertson M.R. The product of the yeast UPF1 gene is required for rapid turnover of mRNAs containing a premature translational termination codon. Genes Dev. 5:1991;2303-2314.
23. Lelivelt M.J., Culbertson M.R. Yeast Upf proteins required for RNA surveillance affect global expression of the yeast transcriptome. Mol. Cell. Biol. 19:1999;6710-6719.
24. Lew J.E., Enomoto S., Berman J. Telomere length regulation and telomeric chromatin require the nonsense-mediated mRNA decay pathway. Mol. Cell. Biol. 18:1998;6121-6130.
25. Losson R., Lacroute F. Interference of nonsense mutations with eukaryotic messenger RNA stability. Proc. Natl. Acad. Sci. USA. 76:1979;5134-5137.
26. Maderazo A.B., He F., Mangus D.A., Jacobson A. Upf1p control of nonsense mRNA translation is regulated by Nmd2p and Upf3p. Mol. Cell. Biol. 20:2000;4591-4603.
27. Maderazo A.B., Belk J.P., He F., Jacobson A. Nonsense-containing mRNAs that accumulate in the absence of a functional nonsense-mediated mRNA decay pathway are destabilized rapidly upon its restitution. Mol. Cell. Biol. 23:2003;842-851.
28. Mangus D., Evans M., Jacobson A. Poly(A)-binding proteins. multifunctional scaffolds for the post-transcriptional control of gene expression Genome Biol. 4:2003;223. 1-223.14.
29. Mendell J.T., Medghalchi S.M., Lake R.G., Noensie E.N., Dietz H.C. Novel Upf2p orthologues suggest a functional link between translation initiation and nonsense surveillance complexes. Mol. Cell. Biol. 20:2000;8944-8957.
30. Mitchell P., Tollervey D. An NMD pathway in yeast involving accelerated deadenylation and exosome-mediated 3′→5′ degradation. Mol. Cell. 11:2003;1405-1413.
31. Morris D.K., Lundblad V. Programmed translational frameshifting in a gene required for yeast telomere replication. Curr. Biol. 7:1997;969-976.
32. Muhlrad D., Parker R. Premature translational termination triggers mRNA decapping. Nature. 370:1994;578-581.
33. Muhlrad D., Parker R. Aberrant mRNAs with extended 3′ UTRs are substrates for rapid degradation by mRNA surveillance. RNA. 5:1999;1299-1307.
34. Muhlrad D., Decker C.J., Parker R. Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5′→3′ digestion of the transcript. Genes Dev. 8:1994;855-866.
35. Muhlrad D., Decker C.J., Parker R. Turnover mechanisms of the stable yeast PGK1 mRNA. Mol. Cell. Biol. 15:1995;2145-2156.
36. Oliveira C.C., McCarthy J.E. The relationship between eukaryotic translation and mRNA stability. A short upstream open reading frame strongly inhibits translational initiation and greatly accelerates mRNA degradation in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 270:1995;8936-8943.
37. Page M.F., Carr B., Anders K.R., Grimson A., Anderson P. SMG-2 is a phosphorylated protein required for mRNA surveillance in Caenorhabditis elegans and related to Upf1p of yeast. Mol. Cell. Biol. 19:1999;5943-5951.
38. Peltz S.W., Brown A.H., Jacobson A. mRNA destabilization triggered by premature translational termination depends on at least three cis-acting sequence elements and one trans-acting factor. Genes Dev. 7:1993;1737-1754. a.
39. Peltz S.W., Trotta C., He F., Brown A., Donahue J.L., Welch E., Jacobson A. Identification of the cis-acting sequences and trans-acting factors involved in nonsense-mediated mRNA decay. McCarthy J., Brown A., Sherman F. Protein Synthesis and Targeting in Yeast. M. Tuite. 1993;1-10 Springer-Verlag, Berlin. b Vol. H71
40. Pulak R., Anderson P. mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Dev. 7:1993;1885-1897.
41. Ruiz-Echevarria M.J., Peltz S.W. The RNA binding protein Pub1 modulates the stability of transcripts containing upstream open reading frames. Cell. 101:2000;741-751.
42. Serin G., Gersappe A., Black J.D., Aronoff R., Maquat L.E. Identification and characterization of human orthologues to Saccharomyces cerevisiae Upf2 protein and Upf3 protein (Caenorhabditis elegans SMG-4). Mol. Cell. Biol. 21:2001;209-223.
43. Tamayo P., Slonim D., Mesirov J., Zhu Q., Kitareewan S., Dmitrovsky E., Lander E.S., Golub T.R. Interpreting patterns of gene expression with self-organizing maps. methods and application to hematopoietic differentiation Proc. Natl. Acad. Sci. USA. 96:1999;2907-2912.
44. van Hoof A., Frischmeyer P.A., Dietz H.C., Parker R. Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science. 295:2002;2262-2264.
45. Vilela C., Linz B., Rodrigues-Pousada C., McCarthy J.E. The yeast transcription factor genes YAP1 and YAP2 are subject to differential control at the levels of both translation and mRNA stability. Nucleic Acids Res. 26:1998;1150-1159.
46. Wang Y., Liu C.L., Storey J.D., Tibshirani R.J., Herschlag D., Brown P.O. Precision and functional specificity in mRNA decay. Proc. Natl. Acad. Sci. USA. 99:2002;5860-5865.
47. Welch E.M., Jacobson A. An internal open reading frame triggers nonsense-mediated decay of the yeast SPT10 mRNA. EMBO J. 18:1999;6134-6145.
48. Wodicka L., Dong H., Mittmann M., Ho M.H., Lockhart D.J. Genome-wide expression monitoring in Saccharomyces cerevisiae. Nat. Biotechnol. 15:1997;1359-1367.