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PMID: 14573473 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Mutations in eukaryotic release factors 1 and 3 act as general nonsense suppressors in Drosophila.

Genetics ·Vol. 165 ·No. 2 ·2003-10-00 ·Pages 601-12

Chao AT, Dierick HA, Addy TM, Bejsovec A

Abstract

In a screen for suppressors of the Drosophila wingless(PE4) nonsense allele, we isolated mutations in the two components that form eukaryotic release factor. eRF1 and eRF3 comprise the translation termination complex that recognizes stop codons and catalyzes the release of nascent polypeptide chains from ribosomes. Mutations disrupting the Drosophila eRF1 and eRF3 show a strong maternal-effect nonsense suppression due to readthrough of stop codons and are zygotically lethal during larval stages. We tested nonsense mutations in wg and in other embryonically acting genes and found that different stop codons can be suppressed but only a subset of nonsense alleles are subject to suppression. We suspect that the context of the stop codon is significant: nonsense alleles sensitive to suppression by eRF1 and eRF3 encode stop codons that are immediately followed by a cytidine. Such suppressible alleles appear to be intrinsically weak, with a low level of readthrough that is enhanced when translation termination is disrupted. Thus the eRF1 and eRF3 mutations provide a tool for identifying nonsense alleles that are leaky. Our findings have important implications for assigning null mutant phenotypes and for selecting appropriate alleles to use in suppressor screens.

MeSH Terms
Alleles Amino Acid Sequence Animals Codon, Nonsense/genetics,metabolism Drosophila/genetics,metabolism Drosophila Proteins/genetics,metabolism Molecular Sequence Data Peptide Termination Factors/genetics,metabolism Proto-Oncogene Proteins/genetics,metabolism Wnt1 Protein
Chemicals
Codon, Nonsense Drosophila Proteins Peptide Termination Factors Proto-Oncogene Proteins Wnt1 Protein eRF1 protein, Drosophila peptide-chain-release factor 3 wg protein, Drosophila
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Chao Anna T
Department of Biology, Duke University, Durham, North Carolina 27708-1000, USA.
Dierick Herman A
Addy Tracie M
Bejsovec Amy
References (38)
38 references, click to expand
  1. Genetic characterization of cytological region 77A-D harboring the presenilin gene of Drosophila melanogaster.
    Genetics. 1999 Dec;153(4):1789-97 PMID: 10581285
  2. The leaky UGA termination codon of tobacco rattle virus RNA is suppressed by tobacco chloroplast and cytoplasmic tRNAs(Trp) with CmCA anticodon.
    EMBO J. 1992 Nov;11(11):4167-73 PMID: 1396598
  3. Analysis of genetic mosaics in developing and adult Drosophila tissues.
    Development. 1993 Apr;117(4):1223-37 PMID: 8404527
  4. Polypeptide chain termination in Saccharomyces cerevisiae.
    Curr Genet. 1994 May;25(5):385-95 PMID: 8082183
  5. Signaling activities of the Drosophila wingless gene are separately mutable and appear to be transduced at the cell surface.
    Genetics. 1995 Jan;139(1):309-20 PMID: 7705631
  6. Translational termination efficiency in mammals is influenced by the base following the stop codon.
    Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5431-5 PMID: 7777525
  7. Context effects on misreading and suppression at UAG codons in human cells.
    Mol Cell Biol. 1995 Dec;15(12):6593-600 PMID: 8524224
  8. Two distinct temperature-sensitive alleles at the elav locus of Drosophila are suppressed nonsense mutations of the same tryptophan codon.
    Genetics. 1995 Nov;141(3):1101-11 PMID: 8582616
  9. Sensitivity of sup35 and sup45 suppressor mutants in Saccharomyces cerevisiae to the anti-microtubule drug benomyl.
    Curr Genet. 1996 Jun;30(1):44-9 PMID: 8662208
  10. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF.
    Cell. 1997 Mar 21;88(6):789-99 PMID: 9118222
  11. Release factor RF3 in E.coli accelerates the dissociation of release factors RF1 and RF2 from the ribosome in a GTP-dependent manner.
    EMBO J. 1997 Jul 1;16(13):4126-33 PMID: 9233821
  12. Wingless signaling generates pattern through two distinct mechanisms.
    Development. 1997 Oct;124(19):3727-36 PMID: 9367428
  13. UGA read-through artifacts--when popular gene expression systems need a pATCH.
    Biotechniques. 1998 May;24(5):789-94 PMID: 9591128
  14. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs.
    Genes Dev. 1998 Jun 1;12(11):1665-77 PMID: 9620853
  15. Drosophila Tcf and Groucho interact to repress Wingless signalling activity.
    Nature. 1998 Oct 8;395(6702):604-8 PMID: 9783586
  16. Functional analysis of Wingless reveals a link between intercellular ligand transport and dorsal-cell-specific signaling.
    Development. 1998 Dec;125(23):4729-38 PMID: 9806921
  17. A screen for mutations that prevent lethality caused by expression of activated sevenless and Ras1 in the Drosophila embryo.
    Dev Genet. 1998;23(4):347-61 PMID: 9883586
  18. Mutations in the highly conserved GGQ motif of class 1 polypeptide release factors abolish ability of human eRF1 to trigger peptidyl-tRNA hydrolysis.
    RNA. 1999 Aug;5(8):1014-20 PMID: 10445876
  19. Drosophila APC2 is a cytoskeletally-associated protein that regulates wingless signaling in the embryonic epidermis.
    J Cell Biol. 1999 Sep 20;146(6):1303-18 PMID: 10491393
  20. Depletion of a Drosophila homolog of yeast Sup35p disrupts spindle assembly, chromosome segregation, and cytokinesis during male meiosis.
    Cell Motil Cytoskeleton. 1998;39(4):286-302 PMID: 9556329
  21. Biosynthesis of selenoproteins--an overview.
    Biofactors. 2000;11(1-2):77-8 PMID: 10705967
  22. The genome sequence of Drosophila melanogaster.
    Science. 2000 Mar 24;287(5461):2185-95 PMID: 10731132
  23. The early evolution of the genetic code.
    Cell. 2000 Jun 9;101(6):569-72 PMID: 10892641
  24. Translational termination comes of age.
    Trends Biochem Sci. 2000 Nov;25(11):561-6 PMID: 11084369
  25. Endless possibilities: translation termination and stop codon recognition.
    Microbiology. 2001 Feb;147(Pt 2):255-69 PMID: 11158343
  26. Decoding apparatus for eukaryotic selenocysteine insertion.
    EMBO Rep. 2000 Aug;1(2):158-63 PMID: 11265756
  27. Impact of the six nucleotides downstream of the stop codon on translation termination.
    EMBO Rep. 2001 Sep;2(9):787-93 PMID: 11520858
  28. Class-1 translation termination factors: invariant GGQ minidomain is essential for release activity and ribosome binding but not for stop codon recognition.
    Nucleic Acids Res. 2001 Oct 1;29(19):3982-7 PMID: 11574680
  29. A posttermination ribosomal complex is the guanine nucleotide exchange factor for peptide release factor RF3.
    Cell. 2001 Oct 5;107(1):115-24 PMID: 11595190
  30. Predominance of six different hexanucleotide recoding signals 3' of read-through stop codons.
    Nucleic Acids Res. 2002 May 1;30(9):2011-7 PMID: 11972340
  31. Genetic control of cuticle formation during embryonic development of Drosophila melanogaster.
    Genetics. 2002 May;161(1):171-82 PMID: 12019232
  32. A selenoprotein in the plant kingdom. Mass spectrometry confirms that an opal codon (UGA) encodes selenocysteine in Chlamydomonas reinhardtii gluththione peroxidase.
    J Biol Chem. 2002 Jul 19;277(29):25983-91 PMID: 11973339
  33. Design of the Genetics of Early Onset Cardiovascular Disease (GENECARD) study.
    Am Heart J. 2003 Apr;145(4):602-13 PMID: 12679755
  34. Identification of an amber nonsense mutation in the rosy516 gene by germline transformation of an amber suppressor tRNA gene.
    EMBO J. 1988 Aug;7(8):2579-84 PMID: 3142765
  35. P-element-mediated enhancer detection: a versatile method to study development in Drosophila.
    Genes Dev. 1989 Sep;3(9):1288-300 PMID: 2558050
  36. The signal for the termination of protein synthesis in procaryotes.
    Nucleic Acids Res. 1990 Apr 25;18(8):2079-86 PMID: 2186375
  37. Nonsense suppression of the major rhodopsin gene of Drosophila.
    Genetics. 1992 Mar;130(3):585-95 PMID: 1551579
  38. Deletion analysis of the SUP35 gene of the yeast Saccharomyces cerevisiae reveals two non-overlapping functional regions in the encoded protein.
    Mol Microbiol. 1993 Mar;7(5):683-92 PMID: 8469113
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2003-10-00
Pages
601-12
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1462801
Subset
IM
Grants
NIGMS NIH HHS · R01 GM059068 · United States
NIGMS NIH HHS · GM-59068 · United States
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