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. 2000 Dec;6(12):1773–1780. doi: 10.1017/s135583820000145x

The odyssey of a regulated transcript.

J Vilardell 1, P Chartrand 1, R H Singer 1, J R Warner 1
PMCID: PMC1370047  PMID: 11142377

Abstract

The transcript of the Saccharomyces cerevisiae gene, RPL30, is subject to regulated splicing and regulated translation, due to a structure that interacts with its own product, ribosomal protein L30. We have followed the fate of the regulated RPL30 transcripts in vivo. Initially, these transcripts abortively enter the splicing pathway, forming an unusually stable association with U1 snRNP. A large proportion of the unspliced molecules, however, are found in the cytoplasm. Most of these are still bound by L30, as only a small fraction are engaged in translation. Eventually, the unspliced RPL30 transcripts escape the grasp of L30, associate with ribosomes, and fall prey to nonsense mediated decay.

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Selected References

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  1. Alksne L. E., Warner J. R. A novel cloning strategy reveals the gene for the yeast homologue to Escherichia coli ribosomal protein S12. J Biol Chem. 1993 May 25;268(15):10813–10819. [PubMed] [Google Scholar]
  2. Caponigro G., Parker R. Mechanisms and control of mRNA turnover in Saccharomyces cerevisiae. Microbiol Rev. 1996 Mar;60(1):233–249. doi: 10.1128/mr.60.1.233-249.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dabeva M. D., Post-Beittenmiller M. A., Warner J. R. Autogenous regulation of splicing of the transcript of a yeast ribosomal protein gene. Proc Natl Acad Sci U S A. 1986 Aug;83(16):5854–5857. doi: 10.1073/pnas.83.16.5854. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dabeva M. D., Warner J. R. Ribosomal protein L32 of Saccharomyces cerevisiae regulates both splicing and translation of its own transcript. J Biol Chem. 1993 Sep 15;268(26):19669–19674. [PubMed] [Google Scholar]
  5. Dabeva M. D., Warner J. R. The yeast ribosomal protein L32 and its gene. J Biol Chem. 1987 Nov 25;262(33):16055–16059. [PubMed] [Google Scholar]
  6. Eng F. J., Warner J. R. Structural basis for the regulation of splicing of a yeast messenger RNA. Cell. 1991 May 31;65(5):797–804. doi: 10.1016/0092-8674(91)90387-e. [DOI] [PubMed] [Google Scholar]
  7. Gottschalk A., Tang J., Puig O., Salgado J., Neubauer G., Colot H. V., Mann M., Séraphin B., Rosbash M., Lührmann R. A comprehensive biochemical and genetic analysis of the yeast U1 snRNP reveals five novel proteins. RNA. 1998 Apr;4(4):374–393. [PMC free article] [PubMed] [Google Scholar]
  8. 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 U S A. 1993 Aug 1;90(15):7034–7038. doi: 10.1073/pnas.90.15.7034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hennigan A. N., Jacobson A. Functional mapping of the translation-dependent instability element of yeast MATalpha1 mRNA. Mol Cell Biol. 1996 Jul;16(7):3833–3843. doi: 10.1128/mcb.16.7.3833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Holstege F. C., Jennings E. G., Wyrick J. J., Lee T. I., Hengartner C. J., Green M. R., Golub T. R., Lander E. S., Young R. A. Dissecting the regulatory circuitry of a eukaryotic genome. Cell. 1998 Nov 25;95(5):717–728. doi: 10.1016/s0092-8674(00)81641-4. [DOI] [PubMed] [Google Scholar]
  11. Jacobson A., Peltz S. W. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu Rev Biochem. 1996;65:693–739. doi: 10.1146/annurev.bi.65.070196.003401. [DOI] [PubMed] [Google Scholar]
  12. Legrain P., Rosbash M. Some cis- and trans-acting mutants for splicing target pre-mRNA to the cytoplasm. Cell. 1989 May 19;57(4):573–583. doi: 10.1016/0092-8674(89)90127-x. [DOI] [PubMed] [Google Scholar]
  13. Li B., Nierras C. R., Warner J. R. Transcriptional elements involved in the repression of ribosomal protein synthesis. Mol Cell Biol. 1999 Aug;19(8):5393–5404. doi: 10.1128/mcb.19.8.5393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Li B., Vilardell J., Warner J. R. An RNA structure involved in feedback regulation of splicing and of translation is critical for biological fitness. Proc Natl Acad Sci U S A. 1996 Feb 20;93(4):1596–1600. doi: 10.1073/pnas.93.4.1596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Long R. M., Elliott D. J., Stutz F., Rosbash M., Singer R. H. Spatial consequences of defective processing of specific yeast mRNAs revealed by fluorescent in situ hybridization. RNA. 1995 Dec;1(10):1071–1078. [PMC free article] [PubMed] [Google Scholar]
  16. Mager W. H., Planta R. J., Ballesta J. G., Lee J. C., Mizuta K., Suzuki K., Warner J. R., Woolford J. A new nomenclature for the cytoplasmic ribosomal proteins of Saccharomyces cerevisiae. Nucleic Acids Res. 1997 Dec 15;25(24):4872–4875. doi: 10.1093/nar/25.24.4872. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mao H., White S. A., Williamson J. R. A novel loop-loop recognition motif in the yeast ribosomal protein L30 autoregulatory RNA complex. Nat Struct Biol. 1999 Dec;6(12):1139–1147. doi: 10.1038/70081. [DOI] [PubMed] [Google Scholar]
  18. McCracken S., Fong N., Yankulov K., Ballantyne S., Pan G., Greenblatt J., Patterson S. D., Wickens M., Bentley D. L. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature. 1997 Jan 23;385(6614):357–361. doi: 10.1038/385357a0. [DOI] [PubMed] [Google Scholar]
  19. Nakielny S., Dreyfuss G. Transport of proteins and RNAs in and out of the nucleus. Cell. 1999 Dec 23;99(7):677–690. doi: 10.1016/s0092-8674(00)81666-9. [DOI] [PubMed] [Google Scholar]
  20. Rout M. P., Blobel G., Aitchison J. D. A distinct nuclear import pathway used by ribosomal proteins. Cell. 1997 May 30;89(5):715–725. doi: 10.1016/s0092-8674(00)80254-8. [DOI] [PubMed] [Google Scholar]
  21. Samarsky D. A., Fournier M. J., Singer R. H., Bertrand E. The snoRNA box C/D motif directs nucleolar targeting and also couples snoRNA synthesis and localization. EMBO J. 1998 Jul 1;17(13):3747–3757. doi: 10.1093/emboj/17.13.3747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schaap P. J., van't Riet J., Woldringh C. L., Raué H. A. Identification and functional analysis of the nuclear localization signals of ribosomal protein L25 from Saccharomyces cerevisiae. J Mol Biol. 1991 Sep 5;221(1):225–237. doi: 10.1016/0022-2836(91)80216-h. [DOI] [PubMed] [Google Scholar]
  23. Swida U., Thüroff E., Steinert E., Käufer N. F. A non-conserved sequence in the 5'region of the CYH2 intron from Saccharomyces cerevisiae controls splicing efficiency of the pre-mRNA. Yeast. 1988 Sep;4(3):209–217. doi: 10.1002/yea.320040306. [DOI] [PubMed] [Google Scholar]
  24. Thomas B. J., Rothstein R. Elevated recombination rates in transcriptionally active DNA. Cell. 1989 Feb 24;56(4):619–630. doi: 10.1016/0092-8674(89)90584-9. [DOI] [PubMed] [Google Scholar]
  25. Underwood M. R., Fried H. M. Characterization of nuclear localizing sequences derived from yeast ribosomal protein L29. EMBO J. 1990 Jan;9(1):91–99. doi: 10.1002/j.1460-2075.1990.tb08084.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Vijayraghavan U., Company M., Abelson J. Isolation and characterization of pre-mRNA splicing mutants of Saccharomyces cerevisiae. Genes Dev. 1989 Aug;3(8):1206–1216. doi: 10.1101/gad.3.8.1206. [DOI] [PubMed] [Google Scholar]
  27. Vilardell J., Warner J. R. Regulation of splicing at an intermediate step in the formation of the spliceosome. Genes Dev. 1994 Jan;8(2):211–220. doi: 10.1101/gad.8.2.211. [DOI] [PubMed] [Google Scholar]
  28. Vilardell J., Yu S. J., Warner J. R. Multiple functions of an evolutionarily conserved RNA binding domain. Mol Cell. 2000 Apr;5(4):761–766. doi: 10.1016/s1097-2765(00)80255-5. [DOI] [PubMed] [Google Scholar]
  29. Warner J. R. Distribution of newly formed ribosomal proteins in HeLa cell fractions. J Cell Biol. 1979 Mar;80(3):767–772. doi: 10.1083/jcb.80.3.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Warner J. R. The economics of ribosome biosynthesis in yeast. Trends Biochem Sci. 1999 Nov;24(11):437–440. doi: 10.1016/s0968-0004(99)01460-7. [DOI] [PubMed] [Google Scholar]

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