Home LiteratureArticle Details
PMID: 15933721 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Translation of aberrant mRNAs lacking a termination codon or with a shortened 3'-UTR is repressed after initiation in yeast.

The EMBO journal ·Vol. 24 ·No. 8 ·2005-04-20 ·Pages 1584-95

Inada T, Aiba H

Abstract

A novel mRNA surveillance for mRNA lacking a termination codon (nonstop mRNA) has been proposed in which Ski7p is thought to recognize stalled ribosomes at the 3' end of mRNA. Here we report our analysis of translation and decay of nonstop mRNAs in Saccharomyces cerevisiae. Although the reduction of nonstop mRNAs was only 4.5-fold, a level that is sufficient for residual protein synthesis, translation products of nonstop mRNAs were hardly detectable. We show that nonstop mRNAs were associated with polysomes, but not with Pab1p. We also show that ribosomes translating nonstop mRNA formed stable and heavy polysome complexes with mRNA. These data suggest that ribosome stalling at the 3' end of nonstop mRNA may block further rounds of translation, hence repressing protein synthesis. Furthermore, it was found that the 5' --> 3' decay pathway was accelerated for nonstop mRNA decay in the absence of Ski7p. We also found that translation of aberrant mRNAs with a shortened 3'-UTR was repressed, suggesting that an improper spatial distance between the termination codon and the 3' end of mRNA results in translation repression.

MeSH Terms
3' Untranslated Regions Adaptor Proteins, Signal Transducing Base Sequence Codon, Terminator Gene Expression Regulation Genes, Reporter Genetic Complementation Test Models, Genetic Molecular Sequence Data Polyribosomes/metabolism Protein Biosynthesis RNA Stability RNA, Messenger/genetics,metabolism Saccharomyces cerevisiae/genetics,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism
Chemicals
3' Untranslated Regions Adaptor Proteins, Signal Transducing Codon, Terminator RNA, Messenger SKI7 protein, S cerevisiae Saccharomyces cerevisiae Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Inada Toshifumi
Department of Molecular Biology, Graduate School of Science, Nagoya University, Nagoya, Japan. [email protected]
Aiba Hiroji
References (27)
27 references, click to expand
  1. Multiple functions for the poly(A)-binding protein in mRNA decapping and deadenylation in yeast.
    Genes Dev. 1995 Oct 1;9(19):2421-32 PMID: 7557393
  2. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds.
    Gene. 1995 Apr 14;156(1):119-22 PMID: 7737504
  3. In vitro trans translation mediated by alanine-charged 10Sa RNA.
    J Mol Biol. 1997 May 23;268(5):803-8 PMID: 9180372
  4. Characterisation of 3' end formation of the yeast HIS3 mRNA.
    Gene. 1997 Apr 29;190(1):69-76 PMID: 9185851
  5. The cis acting sequences responsible for the differential decay of the unstable MFA2 and stable PGK1 transcripts in yeast include the context of the translational start codon.
    RNA. 1999 Mar;5(3):420-33 PMID: 10094310
  6. A faux 3'-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay.
    Nature. 2004 Nov 4;432(7013):112-8 PMID: 15525991
  7. Recognition of yeast mRNAs as "nonsense containing" leads to both inhibition of mRNA translation and mRNA degradation: implications for the control of mRNA decapping.
    Mol Biol Cell. 1999 Nov;10(11):3971-8 PMID: 10564284
  8. Aberrant mRNAs with extended 3' UTRs are substrates for rapid degradation by mRNA surveillance.
    RNA. 1999 Oct;5(10):1299-307 PMID: 10573121
  9. Glucose depletion rapidly inhibits translation initiation in yeast.
    Mol Biol Cell. 2000 Mar;11(3):833-48 PMID: 10712503
  10. The SsrA-SmpB system for protein tagging, directed degradation and ribosome rescue.
    Nat Struct Biol. 2000 Jun;7(6):449-55 PMID: 10881189
  11. Detecting and measuring cotranslational protein degradation in vivo.
    Science. 2000 Sep 22;289(5487):2117-20 PMID: 11000112
  12. Role of the nonsense-mediated decay factor hUpf3 in the splicing-dependent exon-exon junction complex.
    Science. 2001 Sep 7;293(5536):1832-6 PMID: 11546873
  13. Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20.
    Cell. 2001 Sep 7;106(5):607-17 PMID: 11551508
  14. An mRNA surveillance mechanism that eliminates transcripts lacking termination codons.
    Science. 2002 Mar 22;295(5563):2258-61 PMID: 11910109
  15. Exosome-mediated recognition and degradation of mRNAs lacking a termination codon.
    Science. 2002 Mar 22;295(5563):2262-4 PMID: 11910110
  16. The exon junction complex is detected on CBP80-bound but not eIF4E-bound mRNA in mammalian cells: dynamics of mRNP remodeling.
    EMBO J. 2002 Jul 1;21(13):3536-45 PMID: 12093754
  17. One-step affinity purification of the yeast ribosome and its associated proteins and mRNAs.
    RNA. 2002 Jul;8(7):948-58 PMID: 12166649
  18. SsrA-mediated trans-translation plays a role in mRNA quality control by facilitating degradation of truncated mRNAs.
    RNA. 2003 Apr;9(4):408-18 PMID: 12649493
  19. Y14 and hUpf3b form an NMD-activating complex.
    Mol Cell. 2003 Apr;11(4):939-49 PMID: 12718880
  20. Interaction between Ski7p and Upf1p is required for nonsense-mediated 3'-to-5' mRNA decay in yeast.
    EMBO J. 2003 Aug 1;22(15):3951-9 PMID: 12881429
  21. Nonsense-mediated decay breaks the circle?
    Biochem J. 2003 Aug 1;373(Pt 3):e5-6 PMID: 12939168
  22. New insights into the formation of active nonsense-mediated decay complexes.
    Trends Biochem Sci. 2003 Sep;28(9):464-6 PMID: 13678954
  23. Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities.
    Mol Cell. 2003 Sep;12(3):675-87 PMID: 14527413
  24. Eukaryotic mRNA decapping.
    Annu Rev Biochem. 2004;73:861-90 PMID: 15189161
  25. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae.
    Nucleic Acids Res. 1993 Jul 11;21(14):3329-30 PMID: 8341614
  26. Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression.
    Nucleic Acids Res. 1994 Dec 25;22(25):5767-8 PMID: 7838736
  27. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA.
    Science. 1996 Feb 16;271(5251):990-3 PMID: 8584937
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2005-04-20
Epub
2005-00-31
Pages
1584-95
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1142571
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]