Skip to main content
NCBI home page
Molecular Biology of the Cell logoLink to Molecular Biology of the Cell
. 1995 Sep;6(9):1125–1143. doi: 10.1091/mbc.6.9.1125

Glucose-dependent turnover of the mRNAs encoding succinate dehydrogenase peptides in Saccharomyces cerevisiae: sequence elements in the 5' untranslated region of the Ip mRNA play a dominant role.

G P Cereghino 1, D P Atencio 1, M Saghbini 1, J Beiner 1, I E Scheffler 1
PMCID: PMC301272  PMID: 8534911

Abstract

We have demonstrated previously that glucose repression of mitochondrial biogenesis in Saccharomyces cerevisiae involves the control of the turnover of mRNAs for the iron protein (Ip) and flavoprotein (Fp) subunits of succinate dehydrogenase (SDH). Their half-lives are > 60 min in the presence of a nonfermentable carbon source (YPG medium) and < 5 min in glucose (YPD medium). This is a rare example in yeast in which the half-lives are > 60 min in the presence of a nonfermentable carbon source (YPG medium) and < 5 min in glucose (YPD medium). This is a rare example in yeast in which the half-life of an mRNA can be controlled by manipulating external conditions. In our current studies, a series of Ip transcripts with internal deletions as well as chimeric transcripts with heterologous sequences (internally or at the ends) have been examined, and we established that the 5'-untranslated region (5' UTR) of the Ip mRNA contains a major determinant controlling its differential turnover in YPG and YPD. Furthermore, the 5' exonuclease encoded by the XRN1 gene is required for the rapid degradation of the Ip and Fp mRNAs upon the addition of glucose. In the presence of cycloheximide the nucleolytic degradation of the Ip mRNA can be slowed down by stalled ribosomes to allow the identification of intermediates. Such intermediates have lost their 5' ends but still retain their 3' UTRs. If protein synthesis is inhibited at an early initiation step by the use of a prt1 mutation (affecting the initiation factor eIF3), the Ip and Fp mRNAs are very rapidly degraded even in YPG. Significantly, the arrest of translation by the introduction of a stable hairpin loop just upstream of the initiation codon does not alter the differential stability of the transcript in YPG and YPD. These observations suggest that a signaling pathway exists in which the external carbon source can control the turnover of mRNAs of specific mitochondrial proteins. Factors must be present that control either the activity or more likely the access of a nuclease to the select mRNAs. As a result, we propose that a competition between initiation of translation and nuclease action at the 5' end of the transcript determines the half-life of the Ip mRNA.

Full text

PDF
1125

Images in this article

1130Image
on p.1130
1132Image
on p.1132
1134Image
on p.1134
1135Image
on p.1135
1136Image
on p.1136
1137Image
on p.1137
1138Image
on p.1138
1138Image
on p.1138
1139Image
on p.1139

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Atwater J. A., Wisdom R., Verma I. M. Regulated mRNA stability. Annu Rev Genet. 1990;24:519–541. doi: 10.1146/annurev.ge.24.120190.002511. [DOI] [PubMed] [Google Scholar]
  2. Barnes C. A., Singer R. A., Johnston G. C. Yeast prt1 mutations alter heat-shock gene expression through transcript fragmentation. EMBO J. 1993 Aug;12(8):3323–3332. doi: 10.1002/j.1460-2075.1993.tb06002.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beelman C. A., Parker R. Differential effects of translational inhibition in cis and in trans on the decay of the unstable yeast MFA2 mRNA. J Biol Chem. 1994 Apr 1;269(13):9687–9692. [PubMed] [Google Scholar]
  4. Bohjanen P. R., Petryniak B., June C. H., Thompson C. B., Lindsten T. AU RNA-binding factors differ in their binding specificities and affinities. J Biol Chem. 1992 Mar 25;267(9):6302–6309. [PubMed] [Google Scholar]
  5. Bohjanen P. R., Petryniak B., June C. H., Thompson C. B., Lindsten T. An inducible cytoplasmic factor (AU-B) binds selectively to AUUUA multimers in the 3' untranslated region of lymphokine mRNA. Mol Cell Biol. 1991 Jun;11(6):3288–3295. doi: 10.1128/mcb.11.6.3288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brawerman G. mRNA decay: finding the right targets. Cell. 1989 Apr 7;57(1):9–10. doi: 10.1016/0092-8674(89)90166-9. [DOI] [PubMed] [Google Scholar]
  7. Brewer G. An A + U-rich element RNA-binding factor regulates c-myc mRNA stability in vitro. Mol Cell Biol. 1991 May;11(5):2460–2466. doi: 10.1128/mcb.11.5.2460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brown A. J. Messenger RNA stability in yeast. Yeast. 1989 Jul-Aug;5(4):239–257. doi: 10.1002/yea.320050405. [DOI] [PubMed] [Google Scholar]
  9. Burke D. T., Carle G. F., Olson M. V. Cloning of large segments of exogenous DNA into yeast by means of artificial chromosome vectors. Science. 1987 May 15;236(4803):806–812. doi: 10.1126/science.3033825. [DOI] [PubMed] [Google Scholar]
  10. Bushman J. L., Asuru A. I., Matts R. L., Hinnebusch A. G. Evidence that GCD6 and GCD7, translational regulators of GCN4, are subunits of the guanine nucleotide exchange factor for eIF-2 in Saccharomyces cerevisiae. Mol Cell Biol. 1993 Mar;13(3):1920–1932. doi: 10.1128/mcb.13.3.1920. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Bähring S., Sandig V., Lieber A., Strauss M. Mapping of transcriptional start and capping points by a modified 5' RACE technique. Biotechniques. 1994 May;16(5):807–808. [PubMed] [Google Scholar]
  12. Caponigro G., Muhlrad D., Parker R. A small segment of the MAT alpha 1 transcript promotes mRNA decay in Saccharomyces cerevisiae: a stimulatory role for rare codons. Mol Cell Biol. 1993 Sep;13(9):5141–5148. doi: 10.1128/mcb.13.9.5141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Carlson M., Osmond B. C., Botstein D. Mutants of yeast defective in sucrose utilization. Genetics. 1981 May;98(1):25–40. doi: 10.1093/genetics/98.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Celenza J. L., Carlson M. A yeast gene that is essential for release from glucose repression encodes a protein kinase. Science. 1986 Sep 12;233(4769):1175–1180. doi: 10.1126/science.3526554. [DOI] [PubMed] [Google Scholar]
  15. Chapman K. B., Solomon S. D., Boeke J. D. SDH1, the gene encoding the succinate dehydrogenase flavoprotein subunit from Saccharomyces cerevisiae. Gene. 1992 Sep 1;118(1):131–136. doi: 10.1016/0378-1119(92)90260-v. [DOI] [PubMed] [Google Scholar]
  16. Cigan A. M., Foiani M., Hannig E. M., Hinnebusch A. G. Complex formation by positive and negative translational regulators of GCN4. Mol Cell Biol. 1991 Jun;11(6):3217–3228. doi: 10.1128/mcb.11.6.3217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Cleveland D. W., Yen T. J. Multiple determinants of eukaryotic mRNA stability. New Biol. 1989 Nov;1(2):121–126. [PubMed] [Google Scholar]
  18. Decker C. J., Parker R. A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev. 1993 Aug;7(8):1632–1643. doi: 10.1101/gad.7.8.1632. [DOI] [PubMed] [Google Scholar]
  19. Decker C. J., Parker R. Mechanisms of mRNA degradation in eukaryotes. Trends Biochem Sci. 1994 Aug;19(8):336–340. doi: 10.1016/0968-0004(94)90073-6. [DOI] [PubMed] [Google Scholar]
  20. Elble R. A simple and efficient procedure for transformation of yeasts. Biotechniques. 1992 Jul;13(1):18–20. [PubMed] [Google Scholar]
  21. Enssle J., Kugler W., Hentze M. W., Kulozik A. E. Determination of mRNA fate by different RNA polymerase II promoters. Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10091–10095. doi: 10.1073/pnas.90.21.10091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Estruch F., Treitel M. A., Yang X., Carlson M. N-terminal mutations modulate yeast SNF1 protein kinase function. Genetics. 1992 Nov;132(3):639–650. doi: 10.1093/genetics/132.3.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Federoff H. J., Eccleshall T. R., Marmur J. Carbon catabolite repression of maltase synthesis in Saccharomyces carlsbergensis. J Bacteriol. 1983 Oct;156(1):301–307. doi: 10.1128/jb.156.1.301-307.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Feinberg B., McLaughlin C. S., Moldave K. Analysis of temperature-sensitive mutant ts 187 of Saccharomyces cerevisiae altered in a component required for the initiation of protein synthesis. J Biol Chem. 1982 Sep 25;257(18):10846–10851. [PubMed] [Google Scholar]
  25. Foiani M., Cigan A. M., Paddon C. J., Harashima S., Hinnebusch A. G. GCD2, a translational repressor of the GCN4 gene, has a general function in the initiation of protein synthesis in Saccharomyces cerevisiae. Mol Cell Biol. 1991 Jun;11(6):3203–3216. doi: 10.1128/mcb.11.6.3203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Forsburg S. L., Guarente L. Communication between mitochondria and the nucleus in regulation of cytochrome genes in the yeast Saccharomyces cerevisiae. Annu Rev Cell Biol. 1989;5:153–180. doi: 10.1146/annurev.cb.05.110189.001101. [DOI] [PubMed] [Google Scholar]
  27. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Gross E., Goldberg D., Levitzki A. Phosphorylation of the S. cerevisiae Cdc25 in response to glucose results in its dissociation from Ras. Nature. 1992 Dec 24;360(6406):762–765. doi: 10.1038/360762a0. [DOI] [PubMed] [Google Scholar]
  29. Hanic-Joyce P. J., Singer R. A., Johnston G. C. Molecular characterization of the yeast PRT1 gene in which mutations affect translation initiation and regulation of cell proliferation. J Biol Chem. 1987 Feb 25;262(6):2845–2851. [PubMed] [Google Scholar]
  30. Herrick D., Parker R., Jacobson A. Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol Cell Biol. 1990 May;10(5):2269–2284. doi: 10.1128/mcb.10.5.2269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hershey J. W. Overview: phosphorylation and translation control. Enzyme. 1990;44(1-4):17–27. doi: 10.1159/000468744. [DOI] [PubMed] [Google Scholar]
  32. Hershey J. W. Protein phosphorylation controls translation rates. J Biol Chem. 1989 Dec 15;264(35):20823–20826. [PubMed] [Google Scholar]
  33. Hershey J. W. Translational control in mammalian cells. Annu Rev Biochem. 1991;60:717–755. doi: 10.1146/annurev.bi.60.070191.003441. [DOI] [PubMed] [Google Scholar]
  34. 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. 1993 Aug;13(8):4826–4835. doi: 10.1128/mcb.13.8.4826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Irniger S., Egli C. M., Braus G. H. Different classes of polyadenylation sites in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1991 Jun;11(6):3060–3069. doi: 10.1128/mcb.11.6.3060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kearsey S., Kipling D. Recombination and RNA processing: a common strand? Trends Cell Biol. 1991 Nov;1(5):110–112. doi: 10.1016/0962-8924(91)90101-e. [DOI] [PubMed] [Google Scholar]
  38. Keierleber C., Wittekind M., Qin S. L., McLaughlin C. S. Isolation and characterization of PRT1, a gene required for the initiation of protein biosynthesis in Saccharomyces cerevisiae. Mol Cell Biol. 1986 Dec;6(12):4419–4424. doi: 10.1128/mcb.6.12.4419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kenna M., Stevens A., McCammon M., Douglas M. G. An essential yeast gene with homology to the exonuclease-encoding XRN1/KEM1 gene also encodes a protein with exoribonuclease activity. Mol Cell Biol. 1993 Jan;13(1):341–350. doi: 10.1128/mcb.13.1.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Knutsen H. K., Taskén K. A., Eskild W., Jahnsen T., Hansson V. Half-lives of different sized mRNAs for the PKA subunit RI alpha are regulated differently in response to inhibition of transcription and translation. Biochem Biophys Res Commun. 1992 Apr 15;184(1):454–460. doi: 10.1016/0006-291x(92)91215-c. [DOI] [PubMed] [Google Scholar]
  41. Koeller D. M., Horowitz J. A., Casey J. L., Klausner R. D., Harford J. B. Translation and the stability of mRNAs encoding the transferrin receptor and c-fos. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7778–7782. doi: 10.1073/pnas.88.17.7778. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kruys V., Beutler B., Huez G. Translational control mediated by UA-rich sequences. Enzyme. 1990;44(1-4):193–202. doi: 10.1159/000468757. [DOI] [PubMed] [Google Scholar]
  43. Larimer F. W., Hsu C. L., Maupin M. K., Stevens A. Characterization of the XRN1 gene encoding a 5'-->3' exoribonuclease: sequence data and analysis of disparate protein and mRNA levels of gene-disrupted yeast cells. Gene. 1992 Oct 12;120(1):51–57. doi: 10.1016/0378-1119(92)90008-d. [DOI] [PubMed] [Google Scholar]
  44. Larimer F. W., Stevens A. Disruption of the gene XRN1, coding for a 5'----3' exoribonuclease, restricts yeast cell growth. Gene. 1990 Oct 30;95(1):85–90. doi: 10.1016/0378-1119(90)90417-p. [DOI] [PubMed] [Google Scholar]
  45. Laurent B. C., Carlson M. Yeast SNF2/SWI2, SNF5, and SNF6 proteins function coordinately with the gene-specific transcriptional activators GAL4 and Bicoid. Genes Dev. 1992 Sep;6(9):1707–1715. doi: 10.1101/gad.6.9.1707. [DOI] [PubMed] [Google Scholar]
  46. 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. 1991 Dec;5(12A):2303–2314. doi: 10.1101/gad.5.12a.2303. [DOI] [PubMed] [Google Scholar]
  47. Leeds P., Wood J. M., Lee B. S., Culbertson M. R. Gene products that promote mRNA turnover in Saccharomyces cerevisiae. Mol Cell Biol. 1992 May;12(5):2165–2177. doi: 10.1128/mcb.12.5.2165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Lesser C. F., Guthrie C. Mutational analysis of pre-mRNA splicing in Saccharomyces cerevisiae using a sensitive new reporter gene, CUP1. Genetics. 1993 Apr;133(4):851–863. doi: 10.1093/genetics/133.4.851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Levitzki A. Transmembrane signalling to adenylate cyclase in mammalian cells and in Saccharomyces cerevisiae. Trends Biochem Sci. 1988 Aug;13(8):298–301. doi: 10.1016/0968-0004(88)90122-3. [DOI] [PubMed] [Google Scholar]
  50. Lombardo A., Carine K., Scheffler I. E. Cloning and characterization of the iron-sulfur subunit gene of succinate dehydrogenase from Saccharomyces cerevisiae. J Biol Chem. 1990 Jun 25;265(18):10419–10423. [PubMed] [Google Scholar]
  51. Lombardo A., Cereghino G. P., Scheffler I. E. Control of mRNA turnover as a mechanism of glucose repression in Saccharomyces cerevisiae. Mol Cell Biol. 1992 Jul;12(7):2941–2948. doi: 10.1128/mcb.12.7.2941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Lombardo A., Scheffler I. E. Isolation and characterization of a Saccharomyces cerevisiae mutant with a disrupted gene for the IP subunit of succinate dehydrogenase. J Biol Chem. 1989 Nov 15;264(32):18874–18877. [PubMed] [Google Scholar]
  53. Lowell J. E., Rudner D. Z., Sachs A. B. 3'-UTR-dependent deadenylation by the yeast poly(A) nuclease. Genes Dev. 1992 Nov;6(11):2088–2099. doi: 10.1101/gad.6.11.2088. [DOI] [PubMed] [Google Scholar]
  54. 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. 1994 Apr 1;8(7):855–866. doi: 10.1101/gad.8.7.855. [DOI] [PubMed] [Google Scholar]
  55. Muhlrad D., Parker R. Mutations affecting stability and deadenylation of the yeast MFA2 transcript. Genes Dev. 1992 Nov;6(11):2100–2111. doi: 10.1101/gad.6.11.2100. [DOI] [PubMed] [Google Scholar]
  56. Neigeborn L., Carlson M. Mutations causing constitutive invertase synthesis in yeast: genetic interactions with snf mutations. Genetics. 1987 Feb;115(2):247–253. doi: 10.1093/genetics/115.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Ng R., Abelson J. Isolation and sequence of the gene for actin in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3912–3916. doi: 10.1073/pnas.77.7.3912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Nonet M., Scafe C., Sexton J., Young R. Eucaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis. Mol Cell Biol. 1987 May;7(5):1602–1611. doi: 10.1128/mcb.7.5.1602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Parker R., Jacobson A. Translation and a 42-nucleotide segment within the coding region of the mRNA encoded by the MAT alpha 1 gene are involved in promoting rapid mRNA decay in yeast. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2780–2784. doi: 10.1073/pnas.87.7.2780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Peltz S. W., Brewer G., Bernstein P., Hart P. A., Ross J. Regulation of mRNA turnover in eukaryotic cells. Crit Rev Eukaryot Gene Expr. 1991;1(2):99–126. [PubMed] [Google Scholar]
  61. Proudfoot N. Poly(A) signals. Cell. 1991 Feb 22;64(4):671–674. doi: 10.1016/0092-8674(91)90495-k. [DOI] [PubMed] [Google Scholar]
  62. Robinson K. M., Lemire B. D. Isolation and nucleotide sequence of the Saccharomyces cerevisiae gene for the succinate dehydrogenase flavoprotein subunit. J Biol Chem. 1992 May 15;267(14):10101–10107. [PubMed] [Google Scholar]
  63. Ronne H. Glucose repression in fungi. Trends Genet. 1995 Jan;11(1):12–17. doi: 10.1016/s0168-9525(00)88980-5. [DOI] [PubMed] [Google Scholar]
  64. Roy N., Laflamme G., Raymond V. 5' untranslated sequences modulate rapid mRNA degradation mediated by 3' AU-rich element in v-/c-fos recombinants. Nucleic Acids Res. 1992 Nov 11;20(21):5753–5762. doi: 10.1093/nar/20.21.5753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Russo P., Li W. Z., Hampsey D. M., Zaret K. S., Sherman F. Distinct cis-acting signals enhance 3' endpoint formation of CYC1 mRNA in the yeast Saccharomyces cerevisiae. EMBO J. 1991 Mar;10(3):563–571. doi: 10.1002/j.1460-2075.1991.tb07983.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Sachs A. B. Messenger RNA degradation in eukaryotes. Cell. 1993 Aug 13;74(3):413–421. doi: 10.1016/0092-8674(93)80043-e. [DOI] [PubMed] [Google Scholar]
  67. Saghbini M., Broomfield P. L., Scheffler I. E. Studies on the assembly of complex II in yeast mitochondria using chimeric human/yeast genes for the iron-sulfur protein subunit. Biochemistry. 1994 Jan 11;33(1):159–165. doi: 10.1021/bi00167a021. [DOI] [PubMed] [Google Scholar]
  68. Sagliocco F. A., Zhu D., Vega Laso M. R., McCarthy J. E., Tuite M. F., Brown A. J. Rapid mRNA degradation in yeast can proceed independently of translational elongation. J Biol Chem. 1994 Jul 15;269(28):18630–18637. [PubMed] [Google Scholar]
  69. Santiago T. C., Bettany A. J., Purvis I. J., Brown A. J. Messenger RNA stability in Saccharomyces cerevisiae: the influence of translation and poly(A) tail length. Nucleic Acids Res. 1987 Mar 25;15(6):2417–2429. doi: 10.1093/nar/15.6.2417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Savant-Bhonsale S., Cleveland D. W. Evidence for instability of mRNAs containing AUUUA motifs mediated through translation-dependent assembly of a > 20S degradation complex. Genes Dev. 1992 Oct;6(10):1927–1939. doi: 10.1101/gad.6.10.1927. [DOI] [PubMed] [Google Scholar]
  71. Schena M., Picard D., Yamamoto K. R. Vectors for constitutive and inducible gene expression in yeast. Methods Enzymol. 1991;194:389–398. doi: 10.1016/0076-6879(91)94029-c. [DOI] [PubMed] [Google Scholar]
  72. Shyu A. B., Belasco J. G., Greenberg M. E. Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay. Genes Dev. 1991 Feb;5(2):221–231. doi: 10.1101/gad.5.2.221. [DOI] [PubMed] [Google Scholar]
  73. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Stevens A. Purification and characterization of a Saccharomyces cerevisiae exoribonuclease which yields 5'-mononucleotides by a 5' leads to 3' mode of hydrolysis. J Biol Chem. 1980 Apr 10;255(7):3080–3085. [PubMed] [Google Scholar]
  75. Stevens A. mRNA-decapping enzyme from Saccharomyces cerevisiae: purification and unique specificity for long RNA chains. Mol Cell Biol. 1988 May;8(5):2005–2010. doi: 10.1128/mcb.8.5.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Surosky R. T., Strich R., Esposito R. E. The yeast UME5 gene regulates the stability of meiotic mRNAs in response to glucose. Mol Cell Biol. 1994 May;14(5):3446–3458. doi: 10.1128/mcb.14.5.3446. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Szekely E., Montgomery D. L. Glucose represses transcription of Saccharomyces cerevisiae nuclear genes that encode mitochondrial components. Mol Cell Biol. 1984 May;4(5):939–946. doi: 10.1128/mcb.4.5.939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Theodorakis N. G., Cleveland D. W. Physical evidence for cotranslational regulation of beta-tubulin mRNA degradation. Mol Cell Biol. 1992 Feb;12(2):791–799. doi: 10.1128/mcb.12.2.791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Trumbly R. J. Cloning and characterization of the CYC8 gene mediating glucose repression in yeast. Gene. 1988 Dec 15;73(1):97–111. doi: 10.1016/0378-1119(88)90316-2. [DOI] [PubMed] [Google Scholar]
  80. Trumbly R. J. Glucose repression in the yeast Saccharomyces cerevisiae. Mol Microbiol. 1992 Jan;6(1):15–21. doi: 10.1111/j.1365-2958.1992.tb00832.x. [DOI] [PubMed] [Google Scholar]
  81. Van Loon A. P., Van Eijk E., Grivell L. A. Biosynthesis of the ubiquinol-cytochrome c reductase complex in yeast. Discoordinate synthesis of the 11-kd subunit in response to increased gene copy number. EMBO J. 1983;2(10):1765–1770. doi: 10.1002/j.1460-2075.1983.tb01655.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Wahle E., Keller W. The biochemistry of 3'-end cleavage and polyadenylation of messenger RNA precursors. Annu Rev Biochem. 1992;61:419–440. doi: 10.1146/annurev.bi.61.070192.002223. [DOI] [PubMed] [Google Scholar]
  83. Williams F. E., Trumbly R. J. Characterization of TUP1, a mediator of glucose repression in Saccharomyces cerevisiae. Mol Cell Biol. 1990 Dec;10(12):6500–6511. doi: 10.1128/mcb.10.12.6500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Williams F. E., Varanasi U., Trumbly R. J. The CYC8 and TUP1 proteins involved in glucose repression in Saccharomyces cerevisiae are associated in a protein complex. Mol Cell Biol. 1991 Jun;11(6):3307–3316. doi: 10.1128/mcb.11.6.3307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Winston F., Carlson M. Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection. Trends Genet. 1992 Nov;8(11):387–391. doi: 10.1016/0168-9525(92)90300-s. [DOI] [PubMed] [Google Scholar]
  86. Wisdom R., Lee W. The protein-coding region of c-myc mRNA contains a sequence that specifies rapid mRNA turnover and induction by protein synthesis inhibitors. Genes Dev. 1991 Feb;5(2):232–243. doi: 10.1101/gad.5.2.232. [DOI] [PubMed] [Google Scholar]
  87. Yarchuk O., Jacques N., Guillerez J., Dreyfus M. Interdependence of translation, transcription and mRNA degradation in the lacZ gene. J Mol Biol. 1992 Aug 5;226(3):581–596. doi: 10.1016/0022-2836(92)90617-s. [DOI] [PubMed] [Google Scholar]
  88. You Y., Chen C. Y., Shyu A. B. U-rich sequence-binding proteins (URBPs) interacting with a 20-nucleotide U-rich sequence in the 3' untranslated region of c-fos mRNA may be involved in the first step of c-fos mRNA degradation. Mol Cell Biol. 1992 Jul;12(7):2931–2940. doi: 10.1128/mcb.12.7.2931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Zaret K. S., Sherman F. Mutationally altered 3' ends of yeast CYC1 mRNA affect transcript stability and translational efficiency. J Mol Biol. 1984 Jul 25;177(1):107–135. doi: 10.1016/0022-2836(84)90060-3. [DOI] [PubMed] [Google Scholar]
  90. de Winde J. H., Grivell L. A. Global regulation of mitochondrial biogenesis in Saccharomyces cerevisiae: ABF1 and CPF1 play opposite roles in regulating expression of the QCR8 gene, which encodes subunit VIII of the mitochondrial ubiquinol-cytochrome c oxidoreductase. Mol Cell Biol. 1992 Jun;12(6):2872–2883. doi: 10.1128/mcb.12.6.2872. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular Biology of the Cell are provided here courtesy of American Society for Cell Biology

RESOURCES