Nascent peptide-induced translation discontinuation in eukaryotes impacts biased amino acid usage in proteomes.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
02 12 2022
02 12 2022
Historique:
received:
04
02
2022
accepted:
18
11
2022
entrez:
2
12
2022
pubmed:
3
12
2022
medline:
7
12
2022
Statut:
epublish
Résumé
Robust translation elongation of any given amino acid sequence is required to shape proteomes. Nevertheless, nascent peptides occasionally destabilize ribosomes, since consecutive negatively charged residues in bacterial nascent chains can stochastically induce discontinuation of translation, in a phenomenon termed intrinsic ribosome destabilization (IRD). Here, using budding yeast and a human factor-based reconstituted translation system, we show that IRD also occurs in eukaryotic translation. Nascent chains enriched in aspartic acid (D) or glutamic acid (E) in their N-terminal regions alter canonical ribosome dynamics, stochastically aborting translation. Although eukaryotic ribosomes are more robust to ensure uninterrupted translation, we find many endogenous D/E-rich peptidyl-tRNAs in the N-terminal regions in cells lacking a peptidyl-tRNA hydrolase, indicating that the translation of the N-terminal D/E-rich sequences poses an inherent risk of failure. Indeed, a bioinformatics analysis reveals that the N-terminal regions of ORFs lack D/E enrichment, implying that the translation defect partly restricts the overall amino acid usage in proteomes.
Identifiants
pubmed: 36460666
doi: 10.1038/s41467-022-35156-x
pii: 10.1038/s41467-022-35156-x
pmc: PMC9718836
doi:
Substances chimiques
Amino Acids
0
Proteome
0
Peptides
0
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
7451Informations de copyright
© 2022. The Author(s).
Références
Mol Microbiol. 2002 Jul;45(1):123-9
pubmed: 12100553
Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8350-5
pubmed: 8710874
Nucleic Acids Res. 2012 Apr;40(8):3641-52
pubmed: 22180534
Nucleic Acids Res. 1996 Jul 1;24(13):2519-24
pubmed: 8692690
Mol Cell Biol. 2003 Feb;23(4):1368-78
pubmed: 12556496
PLoS Genet. 2015 Mar 16;11(3):e1005044
pubmed: 25775092
Anal Biochem. 1987 Apr;162(1):156-9
pubmed: 2440339
Science. 2011 Dec 16;334(6062):1524-9
pubmed: 22096102
J Cell Biol. 1994 Dec;127(5):1173-84
pubmed: 7962083
Nature. 2008 Apr 3;452(7187):598-603
pubmed: 18327250
Nat Biotechnol. 2011 Apr;29(4):361-7
pubmed: 21441928
PLoS One. 2011;6(12):e28413
pubmed: 22162769
J Biol Chem. 2014 Nov 14;289(46):31960-31971
pubmed: 25258322
PLoS One. 2011;6(4):e18556
pubmed: 21602908
PLoS Genet. 2018 Jan 16;14(1):e1007166
pubmed: 29337993
Nature. 2003 Oct 16;425(6959):686-91
pubmed: 14562095
Genes Dev. 1995 Feb 15;9(4):423-36
pubmed: 7883167
Sci Rep. 2016 Jun 03;6:26941
pubmed: 27256590
Nucleic Acids Res. 2002 Mar 15;30(6):e23
pubmed: 11884642
J Mol Biol. 2008 Dec 5;384(1):73-86
pubmed: 18822297
PLoS Biol. 2011 Jan 18;9(1):e1000581
pubmed: 21267063
Trends Biochem Sci. 2017 Jan;42(1):5-15
pubmed: 27746049
Mol Cell. 2010 Oct 8;40(1):138-46
pubmed: 20932481
Cell. 2012 Nov 21;151(5):1042-54
pubmed: 23178123
Proc Natl Acad Sci U S A. 2006 Aug 22;103(34):12707-12
pubmed: 16908835
Proc Natl Acad Sci U S A. 1967 Oct;58(4):1782-9
pubmed: 4867673
Nature. 2006 Mar 23;440(7083):561-4
pubmed: 16554824
Nature. 2018 May;557(7705):446-451
pubmed: 29632312
Annu Rev Biochem. 2018 Jun 20;87:351-390
pubmed: 29195049
Annu Rev Biochem. 2018 Jun 20;87:421-449
pubmed: 29925264
Nucleic Acids Res. 2019 May 7;47(8):4198-4210
pubmed: 30805621
Proc Natl Acad Sci U S A. 2016 Feb 16;113(7):E829-38
pubmed: 26831095
Nat Commun. 2017 Jul 31;8(1):159
pubmed: 28757607
Mol Cell. 2013 Jul 11;51(1):35-45
pubmed: 23727016
Methods Enzymol. 2011;498:349-61
pubmed: 21601685
Nat Methods. 2014 Mar;11(3):319-24
pubmed: 24487582
Mol Cell. 2018 Oct 18;72(2):286-302.e8
pubmed: 30244831
Annu Rev Biochem. 2013;82:171-202
pubmed: 23746254
Nat Commun. 2018 Jun 6;9(1):2197
pubmed: 29875445
Mol Cell. 2017 Apr 20;66(2):194-205.e5
pubmed: 28392174
Genome Biol. 2011 Nov 03;12(11):R110
pubmed: 22050731
Proc Natl Acad Sci U S A. 2003 Nov 11;100(23):13207-12
pubmed: 14576278
RNA. 1996 Feb;2(2):153-70
pubmed: 8601282
Mol Cell Biol. 2000 Nov;20(21):7971-9
pubmed: 11027267
Philos Trans R Soc Lond B Biol Sci. 2017 Mar 19;372(1716):
pubmed: 28138069
J Mol Biol. 1968 Aug 28;36(1):83-9
pubmed: 4939622
Nucleic Acids Res. 2014 Jan;42(Database issue):D859-64
pubmed: 24185699
Mol Cell. 2016 Jul 7;63(1):72-85
pubmed: 27392146
EMBO J. 1988 Nov;7(11):3559-69
pubmed: 2850168
Nature. 1981 Feb 26;289(5800):751-8
pubmed: 7007895
Curr Opin Struct Biol. 2011 Apr;21(2):274-82
pubmed: 21316217
EMBO J. 1996 Jun 3;15(11):2826-33
pubmed: 8654380
Nucleic Acids Res. 2017 Jul 7;45(12):7326-7338
pubmed: 28549188
J Bacteriol. 1979 Jan;137(1):694-6
pubmed: 368041
Cell. 2000 Aug 18;102(4):511-20
pubmed: 10966112
G3 (Bethesda). 2014 Mar 20;4(3):389-98
pubmed: 24374639
Biochemistry. 2021 Nov 2;60(43):3223-3235
pubmed: 34652913
Nat Rev Mol Cell Biol. 2021 Mar;22(3):196-213
pubmed: 33510441
Elife. 2019 Jun 27;8:
pubmed: 31246176
Bioinformatics. 2010 Apr 1;26(7):966-8
pubmed: 20147306
J Mol Biol. 2016 May 22;428(10 Pt B):2203-16
pubmed: 27038511
EMBO J. 2006 Nov 29;25(23):5492-503
pubmed: 17082762
Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):16707-12
pubmed: 12475929
Curr Opin Struct Biol. 1995 Jun;5(3):360-71
pubmed: 7583634
EMBO J. 2021 Dec 1;40(23):e108299
pubmed: 34672004
Nat Chem Biol. 2009 Dec;5(12):920-8
pubmed: 19915539
Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):333-8
pubmed: 11782551
J Biol Chem. 2009 Apr 17;284(16):10343-52
pubmed: 19204001
PLoS Biol. 2013;11(3):e1001508
pubmed: 23554576
Nat Struct Mol Biol. 2019 May;26(5):343-349
pubmed: 31011209
Mol Cell. 2017 Nov 2;68(3):528-539.e5
pubmed: 29100053
Mol Cell Biol. 1997 Mar;17(3):1580-94
pubmed: 9032286
J Biol Chem. 2021 Aug;297(2):100945
pubmed: 34246632
J Biol Chem. 2004 Aug 13;279(33):34421-30
pubmed: 15192104
Genome Res. 2003 Sep;13(9):2129-41
pubmed: 12952881
Genes Dev. 1995 Feb 15;9(4):437-54
pubmed: 7883168
Science. 2009 Dec 4;326(5958):1412-5
pubmed: 19933110