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PMID: 9469820 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

The yeast transcription factor genes YAP1 and YAP2 are subject to differential control at the levels of both translation and mRNA stability.

Nucleic acids research ·Vol. 26 ·No. 5 ·1998-03-01 ·Pages 1150-9

Vilela C, Linz B, Rodrigues-Pousada C, McCarthy JE

Abstract

Two forms of post-transcriptional control direct differential expression of the Saccharomyces cerevisiae genes encoding the AP1-like transcription factors Yap1p and Yap2p. The mRNAs of these genes contain respectively one (YAP1 uORF) and two (YAP2 uORF1 and uORF2) upstream open reading frames. uORF-mediated modulation of post-termination events on the 5'-untranslated region (5'-UTR) directs differential control not only of translation but also of mRNA decay. Translational control is defined by two types of uORF function. The YAP1 -type uORF allows scanning 40S subunits to proceed via leaky scanning and re-initiation to the major ORF, whereas the YAP2 -type acts to block ribosomal scanning by promoting efficient termination. At the same time, the YAP2 uORFs define a new type of mRNA destabilizing element. Both post-termination ribosome scanning behaviour and mRNA decay are influenced by the coding sequence and mRNA context of the respective uORFs, including downstream elements. Our data indicate that release of post-termination ribosomes promotes largely upf -independent accelerated decay. It follows that translational termination on the 5'-UTR of a mature, non-aberrant yeast mRNA can trigger destabilization via a different pathway to that used to rid the cell of mRNAs containing premature stop codons. This route of control of non-aberrant mRNA decay influences the stress response in yeast. It is also potentially relevant to expression of the sizable number of eukaryotic mRNAs that are now recognized to contain uORFs.

MeSH Terms
Base Sequence DNA, Fungal/genetics DNA-Binding Proteins/genetics Drug Stability Fungal Proteins/genetics Gene Expression Regulation, Fungal Genes, Fungal Molecular Sequence Data Open Reading Frames Protein Biosynthesis RNA Processing, Post-Transcriptional RNA, Fungal/genetics,metabolism RNA, Messenger/genetics,metabolism Saccharomyces cerevisiae/genetics,metabolism Saccharomyces cerevisiae Proteins Transcription Factors/genetics
Chemicals
CAD1 protein, S cerevisiae DNA, Fungal DNA-Binding Proteins Fungal Proteins RNA, Fungal RNA, Messenger Saccharomyces cerevisiae Proteins Transcription Factors YAP1 protein, S cerevisiae
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Vilela C
Posttranscriptional Control Group, Department of Biomolecular Sciences, University of Manchester Institute of Science and Technology (UMIST), PO Box 88, Manchester M60 1QD, UK.
Linz B
Rodrigues-Pousada C
McCarthy J E
References (54)
54 references, click to expand
  1. Migration of 40 S ribosomal subunits on messenger RNA in the presence of edeine.
    J Biol Chem. 1978 Sep 25;253(18):6568-77 PMID: 681367
  2. Sequence of the small subunit of yeast carbamyl phosphate synthetase and identification of its catalytic domain.
    J Biol Chem. 1984 Aug 10;259(15):9790-8 PMID: 6086650
  3. Evidence for translational regulation of the activator of general amino acid control in yeast.
    Proc Natl Acad Sci U S A. 1984 Oct;81(20):6442-6 PMID: 6387704
  4. Yeast regulatory gene PPR1. I. Nucleotide sequence, restriction map and codon usage.
    J Mol Biol. 1984 Dec 5;180(2):239-50 PMID: 6096561
  5. Structure of yeast LEU4. The 5' flanking region contains features that predict two modes of control and two productive translation starts.
    J Biol Chem. 1986 Apr 15;261(11):5160-7 PMID: 2420798
  6. Multiple upstream AUG codons mediate translational control of GCN4.
    Cell. 1986 Apr 25;45(2):201-7 PMID: 3516411
  7. Sequence and expression of the dCMP deaminase gene (DCD1) of Saccharomyces cerevisiae.
    Mol Cell Biol. 1986 May;6(5):1711-21 PMID: 3023902
  8. The leader peptide of yeast gene CPA1 is essential for the translational repression of its expression.
    Cell. 1987 Jun 19;49(6):805-13 PMID: 3555844
  9. Saccharomyces cerevisiae positive regulatory gene PET111 encodes a mitochondrial protein that is translated from an mRNA with a long 5' leader.
    Mol Cell Biol. 1987 Aug;7(8):2728-34 PMID: 2823103
  10. Transcriptional activation by the SV40 AP-1 recognition element in yeast is mediated by a factor similar to AP-1 that is distinct from GCN4.
    Cell. 1988 Apr 22;53(2):321-30 PMID: 2834068
  11. The scanning model for translation: an update.
    J Cell Biol. 1989 Feb;108(2):229-41 PMID: 2645293
  12. Yeast YAP1 encodes a novel form of the jun family of transcriptional activator proteins.
    Genes Dev. 1989 Mar;3(3):283-92 PMID: 2542125
  13. Identification and characterization of HAP4: a third component of the CCAAT-bound HAP2/HAP3 heteromer.
    Genes Dev. 1989 Aug;3(8):1166-78 PMID: 2676721
  14. Inhibition of translational initiation in Saccharomyces cerevisiae by secondary structure: the roles of the stability and position of stem-loops in the mRNA leader.
    Mol Microbiol. 1993 Aug;9(3):521-32 PMID: 8412699
  15. Overexpression of YAP2, coding for a new yAP protein, and YAP1 in Saccharomyces cerevisiae alleviates growth inhibition caused by 1,10-phenanthroline.
    J Biol Chem. 1993 Nov 5;268(31):23640-5 PMID: 8226890
  16. Effect of sequence context at stop codons on efficiency of reinitiation in GCN4 translational control.
    Mol Cell Biol. 1994 Jan;14(1):606-18 PMID: 8264629
  17. Translational repression by the human iron-regulatory factor (IRF) in Saccharomyces cerevisiae.
    Nucleic Acids Res. 1993 Nov 25;21(23):5316-22 PMID: 8265343
  18. YAP1 dependent activation of TRX2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydroperoxides.
    EMBO J. 1994 Feb 1;13(3):655-64 PMID: 8313910
  19. Stress-induced transcriptional activation mediated by YAP1 and YAP2 genes that encode the Jun family of transcriptional activators in Saccharomyces cerevisiae.
    Mol Gen Genet. 1994 Feb;242(3):250-6 PMID: 8107671
  20. Functional dissection of the yeast Cyc8-Tup1 transcriptional co-repressor complex.
    Nature. 1994 Jun 30;369(6483):758-61 PMID: 8008070
  21. Nonsense-mediated mRNA decay in yeast.
    Prog Nucleic Acid Res Mol Biol. 1994;47:271-98 PMID: 8016322
  22. Rapid mRNA degradation in yeast can proceed independently of translational elongation.
    J Biol Chem. 1994 Jul 15;269(28):18630-7 PMID: 8034611
  23. GSH1, which encodes gamma-glutamylcysteine synthetase, is a target gene for yAP-1 transcriptional regulation.
    Mol Cell Biol. 1994 Sep;14(9):5832-9 PMID: 7915005
  24. Cadmium tolerance mediated by the yeast AP-1 protein requires the presence of an ATP-binding cassette transporter-encoding gene, YCF1.
    J Biol Chem. 1994 Dec 23;269(51):32592-7 PMID: 7798263
  25. Translational control of GCN4: an in vivo barometer of initiation-factor activity.
    Trends Biochem Sci. 1994 Oct;19(10):409-14 PMID: 7817398
  26. Identification and characterization of a sequence motif involved in nonsense-mediated mRNA decay.
    Mol Cell Biol. 1995 Apr;15(4):2231-44 PMID: 7891717
  27. 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. 1995 Apr 14;270(15):8936-43 PMID: 7721802
  28. Effects of cadmium and of YAP1 and CAD1/YAP2 genes on iron metabolism in the yeast Saccharomyces cerevisiae.
    Microbiology. 1995 Nov;141 ( Pt 11):2937-43 PMID: 8535522
  29. Utilizing the GCN4 leader region to investigate the role of the sequence determinants in nonsense-mediated mRNA decay.
    EMBO J. 1996 Jun 3;15(11):2810-9 PMID: 8654378
  30. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells.
    Annu Rev Biochem. 1996;65:693-739 PMID: 8811193
  31. Yeast glutathione reductase is required for protection against oxidative stress and is a target gene for yAP-1 transcriptional regulation.
    Mol Microbiol. 1996 Jul;21(1):171-9 PMID: 8843443
  32. Amino acid substitutions in membrane-spanning domains of Hol1, a member of the major facilitator superfamily of transporters, confer nonselective cation uptake in Saccharomyces cerevisiae.
    J Bacteriol. 1996 Dec;178(24):7197-205 PMID: 8955402
  33. Making sense of nonsense in yeast.
    Trends Biochem Sci. 1996 Nov;21(11):433-8 PMID: 8987399
  34. Characterization of the yeast transcriptome.
    Cell. 1997 Jan 24;88(2):243-51 PMID: 9008165
  35. Saccharomyces cerevisiae exhibits a yAP-1-mediated adaptive response to malondialdehyde.
    J Bacteriol. 1997 Feb;179(4):1096-101 PMID: 9023189
  36. Disruption of ribosomal scanning on the 5'-untranslated region, and not restriction of translational initiation per se, modulates the stability of nonaberrant mRNAs in the yeast Saccharomyces cerevisiae.
    J Biol Chem. 1997 Apr 4;272(14):9131-40 PMID: 9083042
  37. Yap, a novel family of eight bZIP proteins in Saccharomyces cerevisiae with distinct biological functions.
    Mol Cell Biol. 1997 Dec;17(12):6982-93 PMID: 9372930
  38. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier.
    Curr Genet. 1989 Dec;16(5-6):339-46 PMID: 2692852
  39. PET genes of Saccharomyces cerevisiae.
    Microbiol Rev. 1990 Sep;54(3):211-25 PMID: 2215420
  40. Suppression of ribosomal reinitiation at upstream open reading frames in amino acid-starved cells forms the basis for GCN4 translational control.
    Mol Cell Biol. 1991 Jan;11(1):486-96 PMID: 1986242
  41. The SNQ3 gene of Saccharomyces cerevisiae confers hyper-resistance to several functionally unrelated chemicals.
    Curr Genet. 1991 Jun;19(6):429-33 PMID: 1878996
  42. Identification and characterization of a Saccharomyces cerevisiae gene (PAR1) conferring resistance to iron chelators.
    Eur J Biochem. 1991 Sep 1;200(2):487-93 PMID: 1889413
  43. An analysis of vertebrate mRNA sequences: intimations of translational control.
    J Cell Biol. 1991 Nov;115(4):887-903 PMID: 1955461
  44. AUG codons in the RNA leader sequences of the yeast PET genes CBS1 and SCO1 have no influence on translation efficiency.
    Curr Genet. 1991 Dec;20(6):465-9 PMID: 1782674
  45. Control of translation initiation in Saccharomyces cerevisiae.
    Mol Microbiol. 1992 Jun;6(11):1413-9 PMID: 1625572
  46. Isolation and characterization of additional genes influencing resistance to various mutagens in the yeast Saccharomyces cerevisiae.
    Curr Genet. 1992 Apr;21(4-5):319-24 PMID: 1525860
  47. cis- and trans-acting suppressors of a translation initiation defect at the cyc1 locus of Saccharomyces cerevisiae.
    Genetics. 1992 Sep;132(1):97-112 PMID: 1327957
  48. Molecular biology of translation in yeast.
    Antonie Van Leeuwenhoek. 1992 Aug;62(1-2):47-62 PMID: 1444336
  49. The SCH9 protein kinase mRNA contains a long 5' leader with a small open reading frame.
    Yeast. 1993 Jan;9(1):21-32 PMID: 8442384
  50. Inhibition of translational initiation in the yeast Saccharomyces cerevisiae as a function of the stability and position of hairpin structures in the mRNA leader.
    J Biol Chem. 1993 Mar 25;268(9):6453-62 PMID: 8454618
  51. TIF4631 and TIF4632: two yeast genes encoding the high-molecular-weight subunits of the cap-binding protein complex (eukaryotic initiation factor 4F) contain an RNA recognition motif-like sequence and carry out an essential function.
    Mol Cell Biol. 1993 Aug;13(8):4860-74 PMID: 8336723
  52. Yeast bZip proteins mediate pleiotropic drug and metal resistance.
    J Biol Chem. 1993 Sep 5;268(25):18850-8 PMID: 8360174
  53. mRNA destabilization triggered by premature translational termination depends on at least three cis-acting sequence elements and one trans-acting factor.
    Genes Dev. 1993 Sep;7(9):1737-54 PMID: 8370523
  54. The 5' untranslated region of the PPR1 regulatory gene dictates rapid mRNA decay in yeast.
    Gene. 1993 Sep 6;131(1):43-51 PMID: 8370540
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
0305-1048
Published
1998-03-01
Pages
1150-9
Language
English
Region
England
NLM ID
0411011
PMCID
PMC147385
Subset
IM
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