Impact of nonsense-mediated mRNA decay on the global expression profile of budding yeast

PLoS Genetics

Volumn 2, Issue 11, 2006, Pages 1924-1943

  Guan, Qiaoning ^a   Zheng, Wei ^a   Tang, Shijie ^b   Liu, Xiaosong ^c   Zinkel, Robert A ^a   Tsui, Kam Wah ^b   Yandell, Brian S ^a,b   Culbertson, Michael R ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b University of Wisconsin Madison   (United States)

^c University of Wisconsin Madison   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RNA POLYMERASE II; THIOLUTIN; 2 PYRROLIDONE DERIVATIVE;

ARTICLE; BUDDING; CHROMOSOME; CONTROLLED STUDY; EUKARYOTE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HALF LIFE TIME; MUTANT; NONHUMAN; PROTEIN DEGRADATION; SACCHAROMYCES CEREVISIAE; TRANSLATION INITIATION; YEAST; BIOLOGICAL MODEL; CLASSIFICATION; COMPARATIVE STUDY; COMPUTER SIMULATION; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHODOLOGY; OPEN READING FRAME; PHYSIOLOGY; PROTEIN SYNTHESIS; REPRODUCIBILITY; RNA INTERFERENCE; RNA PROCESSING; RNA STABILITY; START CODON; THEORETICAL MODEL; TRANSGENIC ORGANISM;

EUKARYOTA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

CODON, INITIATOR; COMPUTER SIMULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; HALF-LIFE; MODELS, BIOLOGICAL; MODELS, THEORETICAL; OPEN READING FRAMES; ORGANISMS, GENETICALLY MODIFIED; PROTEIN BIOSYNTHESIS; PYRROLIDINONES; REPRODUCIBILITY OF RESULTS; RNA INTERFERENCE; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE;

EID: 33751375141     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.0020203     Document Type: Article

References (79)

1. Culbertson MR, Leeds P (2003) Looking at mRNA decay pathways through the window of molecular evolution. Curr Op Gen Dev 13: 207-214.
2. Lynch M, Richardson AO (2002) The evolution of spliceosomal introns. Curr Op Gen Dev 12: 701-710.
3. Culbertson M (1999) RNA surveillance: Unforeseen consequences for gene expression, inherited genetic disorders, and cancer. Trends Genet 15: 74-80.
4. He F, 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.
5. Lee BS, Culbertson MR (1995) Identification of an additional gene required for eukaryotic nonsense mRNA turnover. Proc Natl Acad Sci U S A 92: 10354-10358.
6. Leeds P, Peltz SW, Jacobson A, Culbertson MR (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.
7. Leeds P, Wood JM, Lee BS, Culbertson MR (1992) Gene products that promote mRNA turnover in Saccharomyces cerevisiae. Mol Cell Biol 12: 2165-2177.
8. Culbertson MR, Neeno-Eckwall E (2005) Transcript selection and the recruitment of mRNA decay factors for NMD in Saccharomyces cerevisiae. RNA 11: 1333-1339.
9. Czaplinski K, Ruiz-Echevarria MJ, Paushkin MJ, Han X, Weng Y, et al. (1998) The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev 12: 1665-1677.
10. He F, Jacobson A (2001) Upd1p, Nmd2p, and Upf3p regulate the decapping and exonucleolytic degradation of both nonsense-containing and wild-type mRNAs. Mol Cell Biol 21: 1515-1530.
11. Hsu CL, Stevens A (1993) Yeast cells lacking 5′ to >3′ exoribonuclease 1 contain mRNA species that are poly(A) deficient and partially lack the 5′ cap structure. Mol Cell Biol 13: 4826-4835.
12. Muhlrad D, Parker R (1994) Premature translational termination triggers mRNA decapping. Nature 370: 578-581.
13. He F, Li X, Spatrick P, Casillo R, Dong S, et al. (2003) Genome-wide analysis of mRNAs regulated by the nonsense-mediated and 5′ to 3′ mRNA decay pathways in yeast. Mol Cell 12: 1439-1452.
14. Lelivelt MJ, Culbertson MR (1999) Yeast Upf proteins required for RNA surveillance affect the global expression of the yeast transcriptome. Mol Cell Biol 19: 6710-6719.
15. Altimura N, Groudinsky O, Dujardin G, Slonimski PP (1992) NAM7 nuclear gene encodes a novel member of a family of helicases with a Zn-ligand motif and is involved in mitochondrial functions in Sacchromyces cerevisiae. J Mol Biol 224: 575-587.
16. Dahlseid JN, Lew-Smith J, Lelivelt MJ, Enomoto S, Ford A, et al. (2003) mRNAs encoding telomerase components and regulators are controlled by UPF genes in Saccharomyces cerevisiae. Eukaryotic Cell 2: 134-142.
17. Dahlseid JN, Puziss J, Shirley RL, Atkin AL, Hieter P, et al. (1998) Accumulation of mRNA coding for the Ctf13p kinetochore subunit of Saccharomyces cerevisiae depends on the same factors that promote rapid decay of nonsense mRNAs. Genetics 150: 1019-1035.
18. Lew JE, Enomoto S, Berman J (1998) Telomere length regulation and telomeric chromatin require the nonsense-mediated mRNA decay pathway. Mol Cell Biol 18: 6121-6130.
19. Gaba A, Jacobson A, Sachs MS (2005) Ribosome occupancy of the yeast CPA1 upstream open reading frame termination codon modulates nonsense-mediated mRNA decay. Mol Cell 20: 449-460.
20. Welch EM, Jacobson A (1999) An internal open reading frame triggers nonsense-mediated decay of yeast SPT10 mRNA. EMBO J 18: 6134-6145.
21. Kebaara B, Nazarenus T, Taylor R, Forch A, Atkin AL (2003) The Upf-dependent decay of wild-type PPR1 mRNA depends on its 5′ UTR and first 92 ORF nucleotides. Nucleic Acids Res 31: 3157-3165.
22. Ruiz-Echevarria MJ, Peltz SW (2000) The RNA binding protein Pub1 modulates the stability of transcripts containing upstream open reading frames. Cell 101: 741-751.
23. Taylor R, Kebaara BW, Nazarenus T, Jones A, Yamanaka R, et al. (2005) Gene set co-regulated by the Saccharomyces cerevisiae nonsense-mediated mRNA decay pathway. Eukaryotic Cell 4: 2066-2077.
24. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high-density oligonucleotide array probe level data. Biostat 4: 249-264.
25. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121.
26. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J Royal Stat Soc Series B Methodological 57: 289-300.
27. Grigull J, Mnaimneh S, Pootoolal J, Robinson MD, Hughes TR (2004) Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol Biol Cell 24: 5534-5547.
28. Mitchell P, Tollervey D (2003) An NMD pathway in yeast involving accelerated deadenylation and exosome-mediated 3′ to >5′ degradation. Mol Cell 11: 1405-1413.
29. Milligan L, Torchet C, Allmang C, Shipman T, Tollervey D (2005) A nuclear surveillance pathway for mRNAs with defective polyadenylation. Mol Cell Biol 25: 9996-10004.
30. Harrison P, Kumar A, Lan N, Echols N, Snyder M, et al. (2002) A small reservoir of disabled ORFs in the yeast genome and its implications for the dynamics of proteome evolution. J Mol Biol 316: 409-419.
31. Namy O, Duchateau-Nguyen G, Hatin I, Hermann-Le Denmat S, Termier M, et al. (2003) Identification of stop codon read-through genes in Saccharomyces cerevisiae. Nucleic Acids Res 31: 2289-2296.
32. Farabaugh PJ (1996) Programmed translational frameshifting. Microbiol Rev 60: 103-134.
33. Kim JM, Vanguri S, Boeke JD, Gabriel A, Voytas DF (1998) Transposable elements and genome organization: A comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res 8: 464-478.
34. Zhu J, Zhang MQ (1999) SCPD: A promoter database of the yeast Saccharomyces cerevisiae. Bioinformatics 15: 607-611.
35. Zhang Z, Dietrich FS (2005) Mapping of transcription start sites in Saccharomyces cerevisiae using 59 SAGE. Nucleic Acids Res 33: 2838-2851.
36. Cigan AM, Pabich AM, Donahue TF (1988) Mutational analysis of the HIS4 translational initiator region in Saccharomyces cerevisiae. Mol Cell Biol 8: 2964-2975.
37. Yun DF, Laz TM, Clements JM, Sherman F (1996) mRNA sequences influencing translation and the selection of AUG initiator codons in the yeast Saccharomyces cerevisiae. Mol Microbiol 19: 1225-1239.
38. Hamilton R, Watanabe CK, de Boer HA (1987) Compilation and comparison of the sequence context around the AUG start codons in Saccharomyces cerevisiae mRNAs. Nucleic Acids Res 15: 3581-3593.
39. Miyasaka H (1999) The positive relationship between codon usage bias and translation initiation AUG context in Saccharomyces cerevisiae. Yeast 15: 633-637.
40. Ford A, Guan Q, Neeno-Eckwall E, Culbertson MR (2006) Ebs1p: A global negative regulator of gene expression controlled by the Upf proteins in yeast. Eukaryotic Cell 5: 301-312.
41. Wang Y, Liu CL, Storey JD, Tibshirani RJ, Herschlag D, et al. (2002) Precision and functional specificity in mRNA decay. Proc Natl Acad Sci U S A 99: 5860-5865.
42. Morris DK, Lundblad V (1997) Programmed translational frameshifting in a gene required for yeast telomere replication. Curr Biol 7: 969-976.
43. Asakura T, Sasaki T, Nagano F, Satoh A, Obaishi H, et al. (1998) Isolation and characterization of a novel actin filament-binding protein from Saccharomyces cerevisiae. Oncogene 16: 121-130.
44. Hodgkin J, Papp A, Pulak R, Ambros V, Anderson P (1989) A new kind of informational suppression in the nematode Caenorhabditis elegans. Genetics 123: 301-313.
45. Bertuch AA, Lundblad V (2004) EXO1 contributes to telomere maintenance in both telomerase-proficient and telomerase-deficient Saccharomyces cerevisiae. Genetics 66: 1651-1659.
46. Bose ME, McConnell KH, Gardner-Aukema KA, Muller U, Weinreich M, et al. (2004) The origin recognition complex and Sir4 protein recruit Sir1p to yeast silent chromatin through independent interactions requiring a common Sir1p domain. Mol Cell Biol 24: 774-786.
47. Smith JS, Caputo E, Boeke JD (1999) A genetic screen for ribosomal DNA silencing defects identifies multiple DNA replication and chromatin-modulating factors. Mol Cell Biol 19: 3184-3197.
48. Coissac E, Maillier E, Robineau S, Netter P (1996) Sequence of a 39411 bp DNA fragment covering the left end of Chromosome VII of Saccharomyces cerevisiae. Yeast 12: 1555-1562.
49. Despons L, Wirth B, Louis VL, Souciet J (2006) An evolutionary scenario for one of the largest yeast gene families. Trends Genet 22: 10-15.
50. Abramova N, Sertil O, Mehta S, Lowry CV (2001) Reciprocal regulation of anaerobic and aerobic cell wall mannoprotein gene expression in Saccharomyces cerevisiae. J Bacteriol 183: 2881-2887.
51. Zakian V (1996) Structure, function, and replication of Saccharomyces cerevisiae telomeres. Ann Rev Genet 30: 141-172.
52. Delneri D, Gardner DCJ, Oliver SG (1999) Analysis of the seven-member AAD gene set demonstrates that genetic redundancy in yeast may be more apparent than real. Genetics 153: 1591-1600.
53. Dickinson JR, Salgado EJ, Hewlins MJE (2003) The catabolsim of amino acids to long chain and complex alcohols in Saccharomyces cerevisiae. J Biol Chem 278: 8028-8034.
54. Yamada M, Hayatsu N, Matsuura A, Ishikawa F (1998) Y9-Help1, a DNA helicase encoded by the yeast subtelomeric Y′ element, is induced in survivors defective for telomerase. J Biol Chem 273: 33360-33366.
55. Ketchum CJ, Schmidt WK, Rajendrakumar GV, Michaelis S, Maloney PC (2001) The yeast a-factor transporter Ste6p, a member of the ABC superfamily, couples ATP hydrolysis to pheromone export. J Biol Chem 276: 29007-29011.
56. Burkholder AC, Hartwell LH (1985) The yeast alpha-factor receptor: Structural properties deduced from the sequence of the STE2 gene. Nucleic Acids Res 13: 8463-8475.
57. Chen H, Fink GR (2006) Feedback control of morphogenesis in fungi by aromatic alcohols. Genes Dev 20: 1150-1161.
58. Verstrepen KJ, Jansen A, Lewitter F, Fink GR (2005) Intragenic tandem repeats generate functional variability. Nat Genet 37: 986-990.
59. Le Crom S, Devaux F, Marc P, Zhang X, Moye-Rowley WS, et al. (2002) New insights into the pleiotropic drug resistance network from genome-wide characterization of the YRR1 transcription factor regulation system. Mol Cell Biol 22: 2642-2649.
60. Mamnun YM, Pandjaitan R, Mahe Y, Delahodde A, Kuchler K (2002) The yeast zinc finger regulators Pdr1p and Pdr3p control pleiotropic drug resistance (PDR) as homo- and heterodimers in vivo. Mol Microbiol 46: 1429-1440.
61. Hikkel I, Lucau-Danila A, Delaveau T, Marc P, Devaux F (2003) A general strategy to uncover transcription factor properties identifies a new regulator of drug resistance in yeast. J Biol Chem 278: 11427-11432.
62. Hellauer K, Akache B, MacPherson S, Sirard E, Turcotte B (2002) Zinc cluster protein Rdr1p is a transcriptional repressor of the PDR5 gene encoding a multi-drug transporter. J Biol Chem 277: 17671-17676.
63. Lucau-Danila A, Delaveau T, Lelandais G, Devaux F, Jacq C (2003) Competitive promoter occupancy by two yeast paralogous transcription factors controlling the multi-drug resistance phenomenon. J Biol Chem 278: 52641-52650.
64. DeRisi J, Hazel B, Marc P, Balzi E, Brown P, et al. (2000) Genome microarray analysis of transcriptional activation in multi-drug resistance yeast mutants. FEBS Lett 470: 156-160.
65. Sarver A, DeRisi J (2005) Fzf1p regulates an inducible response to nitrosative stress in Saccharomyces cerevisiae. Mol Biol Cell 16: 4781-4791.
66. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, et al. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
67. Mendell JT, Dietz HC (2001) When the message goes awry: Disease-producing mutations that influence mRNA content and performance. Cell 107: 411-414.
68. Holstege FC, Jennings EG, Wyrick JJ, Lee TI, Hengartner CJ, et al. (1998) Dissecting the regulatory circuitry of a eukaryotic genome. Cell: 717-728.
69. Herrick D, Parker R, Jacobson A (1990) Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol Cell Biol 10: 2269-2284.
70. Parker R, Herrick D, Peltz SW, Jacobson A (1991) Measurement of mRNA decay rates in Saccharomyces cerevisiae. Methods Enzymol 194: 415-423.
71. Hansen LJ, Chalker DL, Sandmeyer SB (1988) Ty3, a yeast retrotransposon associated with tRNA genes, has homology to animal retroviruses. Mol Cell Biol 8: 5245-5256.
72. Shirley RL, Lelivelt MJ, Schenkman LR, Dahlseid JN, Culbertson MR (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.
73. Wach A, Brachat A, Alberti-Segui C, Rebischung C, Phillipsen P (1994) Heterologous HIS3 marker and GFP reporter modules for PCR-targeting in Saccharomyces cerevisiae. Yeast 13: 1065-1075.
74. Jacobson A, Favreau M (1983) Possible involvement of poly(A) in protein synthesis. Nucleic Acids Res 11: 6353-6368.
75. Carbone A, Zinovyev A, Kepes F (2003) Codon adaptation index as a measure of dominating codon bias. Bioinformatics 19: 2005-2015.
76. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: A sequence logo generator. Genome Res 14: 1188-1190.
77. Sharp PM, Li WH (1987) The codon adaptation index: A measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15: 1281-1295.
78. Amrani N, Ganesan R, Kervestin S, Mangus D, Ghosh S, et al. (2004) A faux 39-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature 432: 112-118.
79. Peltz SW, Brown AH, 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.