Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors

Molecular and Cellular Biology

Volumn 24, Issue 12, 2004, Pages 5534-5547

  Grigull, Jörg ^a   Mnaimneh, Sanie ^a   Pootoolal, Jeffrey ^a   Robinson, Mark D ^a   Hughes, Timothy R ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

1,10 PHENANTHROLINE; CHEMOKINE RECEPTOR CCR4; MESSENGER RNA; POLYADENYLIC ACID BINDING PROTEIN; PROTEIN INHIBITOR; PROTEIN PUB1P; PROTEIN PUF4P; RIBOSOME RNA; RNA BINDING PROTEIN; THIOLUTIN; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; BIOGENESIS; DNA MICROARRAY; GENE; GENE DELETION; GENETIC CODE; GENOME ANALYSIS; HEAT SHOCK; HEAT STRESS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; RIBOSOME; RNA STABILITY; RNA SYNTHESIS; RNA TRANSCRIPTION; RPB1 1 GENE; STRESS;

GENE EXPRESSION PROFILING; GENOME, FUNGAL; HEAT-SHOCK RESPONSE; MUTATION; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENANTHROLINES; PYRROLIDINONES; RIBONUCLEASES; RIBOSOMES; RNA POLYMERASE II; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TEMPERATURE; TRANSCRIPTION, GENETIC; URACIL;

EID: 2942561052     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.12.5534-5547.2004     Document Type: Article

References (62)

1. Adams, C. C., and D. S. Gross. 1991. The yeast heat shock response is induced by conversion of cells to spheroplasts and by potent transcriptional inhibitors. J. Bacteriol. 173:7429-7435.
2. Allison, L. A., J. K. Wong, V. D. Fitzpatrick, M. Moyle, and C. J. Ingles. 1988. The C-terminal domain of the largest subunit of RNA polymerase II of Saccharomyces cerevisiae, Drosophila melanogaster, and mammals: a conserved structure with an essential function. Mol. Cell. Biol. 8:321-329.
3. Anderson, J. S. J., and R. Parker. 2000. Computational identification of cis-acting elements affecting post-transcriptional control of gene expression in Saccharomyces cerevisiae. Nucleic Acids Res. 28:1604-1617.
4. Ashburner, M., C. A. Ball, J. A. Blake, D. Botstein, H. Butler, et al. 2000. Gene ontology: tool for the unification of biology. Nat. Genet. 25:25-29.
5. Baggs, J. E., and C. B. Green. 2003. Nocturnin, a deadenylase in Xenopus laevis retina: a mechanism for posttranscriptional control of circadian-related mRNA. Curr. Biol. 13:189-198.
6. Bateman, A. 2002. The SGS3 protein involved in PTGS finds a family. BMC Bioinformatics 3:21.
7. Belasco, J. G., and G. Brawerman (ed.). 1993. Control of messenger RNA stability. Academic Press, San Diego, Calif.
8. Bernstein, J. A., A. B. Khodursky, P. H. Lin, S. Lin-Chao, and S. N. Cohen. 2001. Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays. Proc. Natl. Acad. Sci. USA 99:9697-9702.
9. Blaxall, B. C., A. Pende, S. C. Wu, and J. D. Port. 2002. Correlation between intrinsic mRNA stability and the affinity of AUF1 (hnRNP D) and HuR for A+U-rich mRNAs. Mol. Cell. Biochem. 232:1-11.
10. Cao, D., and R. Parker. 2001. Computational modeling of eukaryotic mRNA turnover. RNA 7:1192-1212.
11. Causton, H. C., B. Ren, S. S. Koh, P. T. Harbison, E. Kanin, E. G. Jennings, T. I. Lee, H. L. True, E. S. Lander, and R. A. Young. 2001. Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell 12:323-337.
12. Chen, C. Y., and A. B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20:465-470.
13. Chen, C. Y., R. Gherzi, S. E. Ong, E. L. Chan, R. Rajmakers, G. J. Prujin, 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.
14. Exinger, F., and F. Lacroute. 1992. 6-Azauracil inhibition of GTP biosynthesis in Saccharomyces cerevisiae. Curr. Genet. 22:9-11.
15. Gasch, A. P., P. T. Spellman, C. M. Kao, O. Carmel-Harel, M. B. Eisen, G. Storz, D. Botstein, and P. O. Brown. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11:4241-4257.
16. Giaever, G., A. M. Chu, L. Ni, C. Connelly, L. Riles, et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387-391.
17. Gibbons, J. D., and S. Chakraborti. 1992. Nonparametric statistical inference, 3rd ed. Marcel Dekker Inc., New York, N.Y.
18. Gutierrez, R. A., R. M. Ewing, J. M. Cherry, and P. J. Green. 2002. Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: rapid decay is associated with a group of touch- and specific clock-controlled genes. Proc. Natl. Acad. Sci. USA 99:11513-11518.
19. Hegde, P., R. Qi, K. Abernathy, C. Gay, S. Dharap, et al. 2000. A concise guide to cDNA microarray analysis. BioTechniques 29:548-556.
20. 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.
21. Herruer, M. H., W. H. Mager, H. A. Raue, P. Vreken, E. Wilms, and R. J. Planta. 1988. Mild temperature shock affects transcription of yeast ribosomal protein genes as well as the stability of their mRNAs. Nucleic Acids Res. 16:7917-7929.
22. Hsu, C. L., 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.
23. Hu, Y. J. 2002. Prediction of structural motifs in a family of coregulated RNA sequences. Nucleic Acids Res. 30:3886-3893.
24. Hughes, T. R., M. J. Marton, A. R. Jones, C. J. Roberts, R. Stoughton, C. D. Armour, H. A. Bennett, E. Coffey, H. Dai, Y. D. He, M. J. Kidd, A. M. King, M. R. Meyer, D. Slade, P. Y. Lum, S. B. Stepaniants, D. D. Shoemaker, D. Gachotte, K. Chakraburtty, J. Simon, M. Bard, and S. H. Friend. 2000. Functional discovery via a compendium of expression profiles. Cell 102:109-126.
25. Issel-Tarver, L., K. R. Christie, K. Dolinski, R. Andrada, R. Balakrishnan, C. A. Ball, G. Binkley, S. Dong, S. S. Dwight, D. G. Fisk, M. Harris, M. Schroeder, A. Sethuraman, K. Tse, S. Weng, D. Botstein, and J. M. Cherry. 2002. Saccharomyces Genome Database. Methods Enzymol. 350:329-346.
26. Jacobs, J. S., A. R. Anderson, and R. P. Parker. 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.
27. Jacobson, A., and S. W. Peltz. 1996. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu. Rev. Biochem. 65:693-773.
28. Jacobson, A. B., and M. Zuker. 1993. Structural analysis by energy dot plot of a large mRNA. J. Mol. Biol. 233:261-269.
29. Johnston, J. R. 1994. Molecular genetics of yeast: a practical approach. Oxford University Press, New York, N.Y.
30. Keene, J. D. 2001. Ribonucleoprotein infrastructure regulating the flow of genetic information between the genome and the proteome. Proc. Natl. Acad. Sci. USA 98:7018-7024.
31. Keene, J. D., and S. A. Tenenbaum. 2002. Eukaryotic mRNPs may represent posttranscriptional operons. Mol. Cell 9:1161-1167.
32. Kief, D. R., and J. R. Warner. 1981. Hierarchy of elements regulating synthesis of ribosomal proteins in Saccharomyces cerevisiae. Mol. Cell. Biol. 1:1016-1023.
33. LaGrandeur, T. E., and R. Parker. 1998. Isolation and characterization of Dcp1, the yeast mRNA decapping enzyme. EMBO J. 17:1487-1496.
34. LaGrandeur, T. E., and R. Parker. 1999. The cis acting sequences responsible for the differential decay of the unstable MFA2 and stable PGK1 transcripts in yeast include the context or the translational start codon. RNA 5:420-433.
35. Le, S. Y., J. H. Chen, D. Konings, and J. V. Maizel, Jr. 2003. Discovering well-ordered folding patterns in nucleotide sequences. Bioinformatics 19:354-361.
36. Lehmann, E. L., and H. J. M. D'Abrera. 1998. Nonparametrics: statistical methods based on ranks, revised ed. Prentice-Hall, Englewood Cliffs, N.J.
37. Lelivelt, M. J., and M. R. Culbertson. 1999. Yeast Upf proteins for RNA surveillance affect global expression of the yeast transcriptome. Mol. Cell. Biol. 19:6710-6719.
38. Li, B., C. R. Nierras, and J. R. Warner. 1999. Transcriptional elements involved in the repression of ribosomal protein synthesis. Mol. Cell. Biol. 19:5393-5404.
39. Lindquist, S. 1981. Regulation of protein synthesis during heat shock. Nature 293:311-314.
40. Mignone, F., C. Gissi, S. Liuni, and G. Pesole. 2002. Untranslated regions of mRNAs. Genome Biol. 3:REVIEWS0004.1-REVIEWS0004.10. [Online.] http://genomebiology.com/2002/3/3/REVIEWS/0004.
41. Moore, P. A., F. A. Sagliocco, R. M. Wood, and A. J. Brown. 1991. Yeast glycolytic mRNAs are differentially regulated. Mol. Cell. Biol. 11:5330-5337.
42. Nonet, M., C. Scafe, J. Sexton, and R. Young. 1987. Eukaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis. Mol. Cell. Biol. 7:1602-1611.
43. Olivas, W., and R. Parker. 2000. The Puf3 protein is a transcript-specific regulator of mRNA degradation in yeast. EMBO J. 19:6602-6611.
44. Parker, R., and H. Song. 2004. The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11:121-127.
45. Raghavan, A., R. L. Ogilvie, C. Reilly, M. L. Abelson, S. Raghavan, J. Vasdevani, M. Krathwol, and P. R. Bohjanen. 2002. Genome-wide analysis of mRNA decay in resting and activated primary human T lymphocytes. Nucleic Acids Res. 30:5529-5538.
46. Robinson, M. D., J. Grigull, N. Mohammad, and T. R. Hughes. 2002. Fun-Spec: a web-based cluster interpreter for yeast. BMC Bioinformatics 3:35.
47. Sachs, L. 1982. Applied statistics. Springer-Verlag, New York, N.Y.
48. Shaw, R. J., and D. Reines. Saccharomyces cerevisiae transcription elongation mutants are defective in PUR5 induction in response to nucleotide depletion. Mol. Cell. Biol. 20:7427-7437.
49. Straney, D. C., and D. M. Crothers. 1987. Effect of drug-DNA interactions upon transcription initiation at the lac promoter. Biochemistry 26:1987-1995.
50. Tavazoie, S., J. D. Hughes, M. J. Campbell, R. J. Cho, and G. M. Church. 1999. Systematic determination of genetic network architecture. Nat. Genet. 22:281-285.
51. Theil, E. C. 1993. The IRE (iron regulatory element) family: structures which regulate mRNA translation or stability. Biofactors 4:87-93.
52. Tipper, D. J. 1973. Inhibition of yeast ribonucleic acid polymerases by thiolutin. J. Bacteriol. 116:245-256.
53. Tucker, M., and R. Parker. 2000. Mechanisms and control of mRNA decapping in Saccharomyces cerevisiae. Annu. Rev. Biochem. 69:571-595.
54. Tucker, M., M. A. Valencia-Sanchez, R. R. Staples, J. Chen, C. L. Denis, and R. Parker. 2001. The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae. Cell 104:377-386.
55. Tucker, M., R. R. Staples, M. A. Valencia-Sanchez, D. Muhlrad, and R. Parker. 2002. Ccr4p is the catalytic subunit of a Ccr4p/Pop2p/Notp mRNA deadenylase complex in Saccharomyces cerevisiae. EMBO J. 21:1427-1436.
56. Vasudevan, S., and S. W. Peltz. 2001. Regulated ARE-mediated mRNA decay in Saccharomyces cerevisiae. Mol. Cell 7:1191-1200.
57. Venema, J., and D. Tollervey. 1999. Ribosome synthesis in Saccharomyces cerevisiae. Annu. Rev. Genet. 33:261-311.
58. Wang, Y., C. L. Liu, J. D. Storey, R. J. Tibshirani, D. Hersehlag, and P. O. Brown. 2002. Precision and functional specificity in mRNA decay. Proc. Natl. Acad. Sci. USA 99:5860-5865.
59. Warner, J. R. 1999. The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24:437-440.
60. Wilusz, C. J., M. Wormington, and S. W. Peltz. 2001. The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell. Biol. 2:237-246.
61. Wu, L. F., T. R. Hughes, A. P. Davierwala, M. D. Robinson, R. Stoughton, and S. J. Altschuler. 2002. Large-scale prediction of Saccharomyces cerevisiae gene function using overlapping transcriptional clusters. Nat. Genet. 31:255-265.
62. Yang, Y. H., S. Dudoit, P. Luu, D. M. Lin, V. Peng, J. Ngai, and T. P. Speed. 2002. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30:e15.