Increased fidelity of protein synthesis extends lifespan.

RPS23 aging archaea mTOR protein synthesis proteostasis ribosome translation translation accuracy translation fidelity

Journal

Cell metabolism
ISSN: 1932-7420
Titre abrégé: Cell Metab
Pays: United States
ID NLM: 101233170

Informations de publication

Date de publication:
02 11 2021
Historique:
received: 04 08 2020
revised: 06 05 2021
accepted: 30 08 2021
pubmed: 16 9 2021
medline: 8 4 2022
entrez: 15 9 2021
Statut: ppublish

Résumé

Loss of proteostasis is a fundamental process driving aging. Proteostasis is affected by the accuracy of translation, yet the physiological consequence of having fewer protein synthesis errors during multi-cellular organismal aging is poorly understood. Our phylogenetic analysis of RPS23, a key protein in the ribosomal decoding center, uncovered a lysine residue almost universally conserved across all domains of life, which is replaced by an arginine in a small number of hyperthermophilic archaea. When introduced into eukaryotic RPS23 homologs, this mutation leads to accurate translation, as well as heat shock resistance and longer life, in yeast, worms, and flies. Furthermore, we show that anti-aging drugs such as rapamycin, Torin1, and trametinib reduce translation errors, and that rapamycin extends further organismal longevity in RPS23 hyperaccuracy mutants. This implies a unified mode of action for diverse pharmacological anti-aging therapies. These findings pave the way for identifying novel translation accuracy interventions to improve aging.

Identifiants

pubmed: 34525330
pii: S1550-4131(21)00417-4
doi: 10.1016/j.cmet.2021.08.017
pmc: PMC8570412
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2288-2300.e12

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM135599
Pays : United States
Organisme : Cancer Research UK
ID : C416/A25145
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C7893/A28990
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UP_1102/6
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UP_1605/6
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 201487
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 102532/Z/12/Z
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/V006916/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 102531/Z/13/A
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M02492X/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC-A654-5QC80
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn
Type : CommentIn
Type : CommentIn

Informations de copyright

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

Proc Natl Acad Sci U S A. 2012 Jan 10;109(2):413-8
pubmed: 22160674
Genetics. 2018 Feb;208(2):473-490
pubmed: 29378809
J Mol Biol. 2005 May 13;348(4):801-15
pubmed: 15843014
J Bacteriol. 1997 Jan;179(2):417-22
pubmed: 8990293
Nat Rev Genet. 2016 Oct 14;17(11):704-714
pubmed: 27739533
Nat Methods. 2014 Jan;11(1):100-5
pubmed: 24240321
Nature. 2010 Mar 25;464(7288):504-12
pubmed: 20336132
Philos Trans R Soc Lond B Biol Sci. 2017 Mar 19;372(1716):
pubmed: 28138068
Biochim Biophys Acta. 1984 Nov 22;783(2):166-70
pubmed: 6388640
Nucleic Acids Res. 2014 Dec 1;42(21):13353-69
pubmed: 25378320
Cell. 2009 Oct 2;139(1):149-60
pubmed: 19804760
Philos Trans R Soc Lond B Biol Sci. 2011 Oct 27;366(1580):2979-86
pubmed: 21930591
PLoS One. 2012;7(7):e40569
pubmed: 22808195
Trends Biochem Sci. 2014 Aug;39(8):355-62
pubmed: 25023410
Nat Methods. 2013 Sep;10(9):877-9
pubmed: 23852451
Cell. 2013 Jun 6;153(6):1194-217
pubmed: 23746838
PLoS One. 2018 Jan 12;13(1):e0190105
pubmed: 29329306
RNA. 2010 Sep;16(9):1797-808
pubmed: 20651030
Bioinformatics. 2018 Jul 15;34(14):2490-2492
pubmed: 29506019
Annu Rev Biochem. 2005;74:129-77
pubmed: 15952884
Wiley Interdiscip Rev RNA. 2020 May;11(3):e1578
pubmed: 31755249
Genome Biol. 2007;8(10):R216
pubmed: 17927810
Aging Cell. 2013 Aug;12(4):563-73
pubmed: 23551936
J Mol Biol. 1998 Sep 11;282(1):13-24
pubmed: 9733638
Nature. 2009 Oct 29;461(7268):1234-42
pubmed: 19838167
Exp Gerontol. 1997 May-Jun;32(3):333-46
pubmed: 9193901
Nat Commun. 2016 Dec 20;7:13521
pubmed: 27995908
Aging Cell. 2007 Feb;6(1):95-110
pubmed: 17266679
PLoS Genet. 2014 Dec 04;10(12):e1004752
pubmed: 25474471
Annu Rev Biochem. 2015;84:435-64
pubmed: 25784053
Cell. 2019 Apr 18;177(3):622-638.e22
pubmed: 31002797
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Proc Natl Acad Sci U S A. 2018 Jul 17;115(29):E6731-E6740
pubmed: 29967153
J Mol Biol. 2007 Dec 7;374(4):1065-76
pubmed: 17967466
Cell. 2008 Apr 18;133(2):292-302
pubmed: 18423200
Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9538-41
pubmed: 8415737
Nat Rev Microbiol. 2010 Dec;8(12):849-56
pubmed: 21079633
Cell. 2002 Nov 27;111(5):721-32
pubmed: 12464183
Nat Rev Mol Cell Biol. 2019 Jul;20(7):421-435
pubmed: 30733602
Nucleic Acids Res. 2019 Jul 2;47(W1):W256-W259
pubmed: 30931475
Science. 2006 Mar 10;311(5766):1471-4
pubmed: 16469881
J Mol Biol. 2011 Jul 1;410(1):1-9
pubmed: 21575643
Science. 2016 Jul 1;353(6294):aac4354
pubmed: 27365453
Nature. 2013 Jan 17;493(7432):338-45
pubmed: 23325216
Mol Cell. 2018 Nov 1;72(3):469-481.e7
pubmed: 30293783
Elife. 2013 Dec 03;2:e01179
pubmed: 24302569
Cell Metab. 2016 Jun 14;23(6):1004-1012
pubmed: 27304502
Nature. 2017 Jun 1;546(7656):113-117
pubmed: 28538735
Cell Metab. 2018 Jun 05;27(6):1309-1322.e6
pubmed: 29754951
Mol Cell. 2013 Feb 7;49(3):411-21
pubmed: 23395271
Aging (Albany NY). 2018 Dec 18;10(12):4269-4288
pubmed: 30562164
Nature. 2018 Sep;561(7721):45-56
pubmed: 30185958
Cell. 2015 Jul 2;162(1):72-83
pubmed: 26119340
Nature. 2017 Dec 14;552(7684):263-267
pubmed: 29186112
Science. 2001 Apr 6;292(5514):104-6
pubmed: 11292874
Commun Biol. 2020 Feb 6;3(1):58
pubmed: 32029867
Nat Cell Biol. 2008 Nov;10(11):1241-7
pubmed: 18978832
Nature. 2006 Sep 7;443(7107):50-5
pubmed: 16906134
Nat Genet. 2005 Aug;37(8):894-8
pubmed: 16041374
Cell. 2008 Jul 25;134(2):341-52
pubmed: 18662548
J Biol Chem. 2007 May 11;282(19):14056-64
pubmed: 17360704
Biol Open. 2017 Aug 15;6(8):1229-1234
pubmed: 28642244
Cell Metab. 2011 Jul 6;14(1):55-66
pubmed: 21723504
Nature. 2019 Jul;571(7764):183-192
pubmed: 31292558
J Mol Biol. 1972 Jul 28;68(3):547-50
pubmed: 4560854
Brief Bioinform. 2019 Jul 19;20(4):1160-1166
pubmed: 28968734
Cell. 2009 Feb 20;136(4):746-62
pubmed: 19239893
Cell Metab. 2010 Jan;11(1):35-46
pubmed: 20074526
Science. 2001 May 4;292(5518):897-902
pubmed: 11340196
Open Biol. 2017 Jan;7(1):
pubmed: 28100667
Curr Biol. 2019 Mar 4;29(5):737-749.e5
pubmed: 30773367
J Gerontol A Biol Sci Med Sci. 2007 Oct;62(10):1071-81
pubmed: 17921418
Mol Biol Evol. 2020 Sep 1;37(9):2727-2733
pubmed: 32365179
J Mol Biol. 1969 Jan 14;39(1):95-112
pubmed: 4938819
Philos Trans R Soc Lond B Biol Sci. 2018 Sep 10;373(1758):
pubmed: 30201839
Nat Methods. 2017 Jun;14(6):587-589
pubmed: 28481363
Aging Cell. 2017 Oct;16(5):988-993
pubmed: 28707419
Sci Signal. 2013 Apr 16;6(271):ra24
pubmed: 23592839
Nat Rev Mol Cell Biol. 2007 Jul;8(7):519-29
pubmed: 17565364
PLoS One. 2012;7(7):e40410
pubmed: 22792305
Mol Cell. 2010 Jul 9;39(1):110-20
pubmed: 20603079
Trends Biochem Sci. 2003 May;28(5):259-66
pubmed: 12765838
BMC Biotechnol. 2016 Nov 8;16(1):76
pubmed: 27825338
Nat Methods. 2009 Apr;6(4):275-7
pubmed: 19305406

Auteurs

Victoria Eugenia Martinez-Miguel (VE)

UCL Cancer Institute, Paul O'Gorman Building, University College London, 72 Huntley Street, London WC1E 6DD, UK.

Celia Lujan (C)

UCL Cancer Institute, Paul O'Gorman Building, University College London, 72 Huntley Street, London WC1E 6DD, UK.

Tristan Espie-Caullet (T)

UCL Cancer Institute, Paul O'Gorman Building, University College London, 72 Huntley Street, London WC1E 6DD, UK.

Daniel Martinez-Martinez (D)

MRC London Institute of Medical Sciences, Du Cane Road, London W12 0NN, UK; Institute of Clinical Sciences, Imperial College London, Hammersmith Hospital Campus, Du Cane Road, London W12 0NN, UK.

Saul Moore (S)

MRC London Institute of Medical Sciences, Du Cane Road, London W12 0NN, UK; Institute of Clinical Sciences, Imperial College London, Hammersmith Hospital Campus, Du Cane Road, London W12 0NN, UK.

Cassandra Backes (C)

MRC London Institute of Medical Sciences, Du Cane Road, London W12 0NN, UK; Institute of Clinical Sciences, Imperial College London, Hammersmith Hospital Campus, Du Cane Road, London W12 0NN, UK.

Suam Gonzalez (S)

School of Health, Sport and Bioscience, University of East London, Water Lane, London E15 4LZ, UK.

Evgeniy R Galimov (ER)

MRC London Institute of Medical Sciences, Du Cane Road, London W12 0NN, UK; Institute of Clinical Sciences, Imperial College London, Hammersmith Hospital Campus, Du Cane Road, London W12 0NN, UK.

André E X Brown (AEX)

MRC London Institute of Medical Sciences, Du Cane Road, London W12 0NN, UK; Institute of Clinical Sciences, Imperial College London, Hammersmith Hospital Campus, Du Cane Road, London W12 0NN, UK.

Mario Halic (M)

Department of Structural Biology, St. Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Kazunori Tomita (K)

Centre for Genome Engineering and Maintenance, College of Health, Medicine and Life Sciences, Brunel University London, London UB8 3PH, UK.

Charalampos Rallis (C)

School of Health, Sport and Bioscience, University of East London, Water Lane, London E15 4LZ, UK.

Tobias von der Haar (T)

Kent Fungal Group, School of Biosciences, Division of Natural Sciences, University of Kent, Canterbury CT2 7NJ, UK.

Filipe Cabreiro (F)

MRC London Institute of Medical Sciences, Du Cane Road, London W12 0NN, UK; Institute of Clinical Sciences, Imperial College London, Hammersmith Hospital Campus, Du Cane Road, London W12 0NN, UK; Cologne Excellence Cluster for Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, Joseph Stelzmann Strasse 26, 50931 Cologne, Germany. Electronic address: f.cabreiro@imperial.ac.uk.

Ivana Bjedov (I)

UCL Cancer Institute, Paul O'Gorman Building, University College London, 72 Huntley Street, London WC1E 6DD, UK; Department of Medical Physics and Biomedical Engineering, University College London, Malet Place Engineering Building, Gower Street, London WC1E 6BT, UK. Electronic address: i.bjedov@ucl.ac.uk.

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