mRNA and tRNA modification states influence ribosome speed and frame maintenance during poly(lysine) peptide synthesis.
RNA modification
peptide-mediated stalling
reading frame maintenance
ribosome
translation stalling
Journal
The Journal of biological chemistry
ISSN: 1083-351X
Titre abrégé: J Biol Chem
Pays: United States
ID NLM: 2985121R
Informations de publication
Date de publication:
06 2022
06 2022
Historique:
received:
01
12
2021
revised:
27
04
2022
accepted:
28
04
2022
pubmed:
21
5
2022
medline:
30
6
2022
entrez:
20
5
2022
Statut:
ppublish
Résumé
Ribosome speed is dictated by multiple factors including substrate availability, cellular conditions, and product (peptide) formation. Translation slows during the synthesis of cationic peptide sequences, potentially influencing the expression of thousands of proteins. Available evidence suggests that ionic interactions between positively charged nascent peptides and the negatively charged ribosome exit tunnel impede translation. However, this hypothesis was difficult to test directly because of inability to decouple the contributions of amino acid charge from mRNA sequence and tRNA identity/abundance in cells. Furthermore, it is unclear if other components of the translation system central to ribosome function (e.g., RNA modification) influence the speed and accuracy of positively charged peptide synthesis. In this study, we used a fully reconstituted Escherichia coli translation system to evaluate the effects of peptide charge, mRNA sequence, and RNA modification status on the translation of lysine-rich peptides. Comparison of translation reactions on poly(lysine)-encoding mRNAs conducted with either Lys-tRNA
Identifiants
pubmed: 35595100
pii: S0021-9258(22)00479-3
doi: 10.1016/j.jbc.2022.102039
pmc: PMC9207662
pii:
doi:
Substances chimiques
Peptides
0
RNA, Messenger
0
RNA, Transfer, Lys
0
Polylysine
25104-18-1
RNA, Transfer
9014-25-9
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
102039Subventions
Organisme : NIGMS NIH HHS
ID : R35 GM128836
Pays : United States
Informations de copyright
Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Conflict of interest The authors declare that they have no conflicts of interest with the contents of this article.
Références
Proc Natl Acad Sci U S A. 2019 Nov 12;116(46):23068-23074
pubmed: 31672910
Mol Cell. 2017 Feb 16;65(4):743-750.e4
pubmed: 28065601
RNA. 2007 Aug;13(8):1245-55
pubmed: 17592039
Cell. 2004 May 28;117(5):589-99
pubmed: 15163407
J Am Chem Soc. 2019 Dec 26;141(51):19988-19993
pubmed: 31826614
Genes Dev. 2007 Mar 1;21(5):519-24
pubmed: 17344413
Mol Cell. 2005 Jan 7;17(1):61-8
pubmed: 15629717
Methods. 2008 Feb;44(2):81-6
pubmed: 18241790
RNA. 2017 May;23(5):749-761
pubmed: 28193672
Nat Methods. 2015 Aug;12(8):767-72
pubmed: 26121403
Sci Adv. 2019 Jul 03;5(7):eaax0250
pubmed: 31281898
Biomolecules. 2017 Apr 04;7(2):
pubmed: 28375166
Annu Rev Biochem. 2020 Jun 20;89:417-442
pubmed: 32569528
Nature. 2014 Aug 21;512(7514):328-32
pubmed: 24919156
Philos Trans R Soc Lond B Biol Sci. 2011 Oct 27;366(1580):2979-86
pubmed: 21930591
Elife. 2015 Feb 19;4:
pubmed: 25695637
J Mol Biol. 2008 Dec 5;384(1):73-86
pubmed: 18822297
Genes (Basel). 2019 Jan 25;10(2):
pubmed: 30691071
Nature. 2009 Jan 8;457(7226):161-6
pubmed: 19092806
Cell. 2012 Nov 21;151(5):1042-54
pubmed: 23178123
Proc Natl Acad Sci U S A. 2017 Oct 24;114(43):11434-11439
pubmed: 29073068
Methods Enzymol. 2021;658:379-406
pubmed: 34517955
ACS Chem Biol. 2017 Jun 16;12(6):1629-1635
pubmed: 28437082
Nat Methods. 2006 May;3(5):357-9
pubmed: 16628205
Nat Commun. 2016 Jan 21;7:10457
pubmed: 26791911
Biochemistry. 2014 Sep 9;53(35):5710-20
pubmed: 25094027
Annu Rev Biochem. 2018 Jun 20;87:421-449
pubmed: 29925264
EMBO J. 2001 Sep 3;20(17):4794-802
pubmed: 11532943
Cell. 2015 Feb 26;160(5):870-881
pubmed: 25703095
J Am Chem Soc. 2015 Feb 11;137(5):2107-15
pubmed: 25611135
RNA. 2018 Oct;24(10):1377-1389
pubmed: 29997263
Sci Adv. 2017 Jun 07;3(6):e1700147
pubmed: 28630923
Biochemistry. 2020 Jun 16;59(23):2154-2170
pubmed: 32407625
Biochemistry. 2004 May 25;43(20):6159-66
pubmed: 15147200
Cell. 2015 Mar 12;160(6):1111-24
pubmed: 25768907
J Bacteriol. 1993 Feb;175(3):716-22
pubmed: 7678594
Wiley Interdiscip Rev RNA. 2020 Jul;11(4):e1586
pubmed: 31960607
Sci Adv. 2015 Jul;1(6):
pubmed: 26322332
Proc Natl Acad Sci U S A. 2014 Sep 2;111(35):12740-5
pubmed: 25128388
Translation (Austin). 2016 Jan 28;4(1):e1143076
pubmed: 27335723
Trends Mol Med. 2014 Jun;20(6):306-14
pubmed: 24581449
Biochem Biophys Res Commun. 2014 Nov 21;454(3):441-5
pubmed: 25450681
J Am Chem Soc. 2017 Apr 26;139(16):5857-5864
pubmed: 28368583
Nat Struct Mol Biol. 2016 Feb;23(2):110-5
pubmed: 26751643
J Mol Biol. 1989 May 20;207(2):365-77
pubmed: 2474074
Nucleic Acids Res. 2017 Sep 6;45(15):9059-9067
pubmed: 28591780
PLoS Genet. 2012;8(3):e1002603
pubmed: 22479199
Cell. 2014 Jun 19;157(7):1619-31
pubmed: 24949973
J Mol Biol. 2020 Dec 4;432(24):166696
pubmed: 33152326
Proc Natl Acad Sci U S A. 2013 Jul 23;110(30):12289-94
pubmed: 23836657
Nat Commun. 2018 Nov 19;9(1):4865
pubmed: 30451861
Science. 2000 Aug 11;289(5481):905-20
pubmed: 10937989
EMBO J. 2020 Feb 3;39(3):e103365
pubmed: 31858614
Biochemistry. 2021 Nov 2;60(43):3223-3235
pubmed: 34652913
Nucleic Acids Res. 2021 Mar 18;49(5):2684-2699
pubmed: 33561188
Wiley Interdiscip Rev RNA. 2012 Sep-Oct;3(5):661-73
pubmed: 22715123
Nat Protoc. 2011 Jun;6(6):779-90
pubmed: 21637198
Enzymes. 2017;41:1-50
pubmed: 28601219
EMBO J. 2003 Sep 15;22(18):4770-8
pubmed: 12970189
EMBO J. 1984 Dec 1;3(12):2895-8
pubmed: 6396082
Nucleic Acids Res. 2008 May;36(8):2619-29
pubmed: 18344525
Nat Struct Mol Biol. 2019 Dec;26(12):1132-1140
pubmed: 31768042
Mol Cell Biol. 2008 May;28(10):3301-12
pubmed: 18332122
Mol Cell Biol. 2014 Nov;34(21):4062-76
pubmed: 25154418
J Biol Chem. 2009 Apr 17;284(16):10343-52
pubmed: 19204001
J Mol Biol. 2010 Mar 12;396(5):1310-8
pubmed: 20043920
Sci Adv. 2019 Jun 05;5(6):eaaw9049
pubmed: 31183409
PLoS Biol. 2013;11(3):e1001508
pubmed: 23554576
Mol Cell. 2020 Aug 20;79(4):588-602.e6
pubmed: 32615089
Annu Rev Biochem. 2021 Jun 20;90:375-401
pubmed: 33441035
Nat Commun. 2021 Aug 31;12(1):5201
pubmed: 34465779
Nucleic Acids Res. 2017 Mar 17;45(5):2865-2874
pubmed: 27799473
Nat Rev Mol Cell Biol. 2021 Jun;22(6):375-392
pubmed: 33658722