Tsr4 and Nap1, two novel members of the ribosomal protein chaperOME.
Amino Acid Sequence
Models, Molecular
Molecular Chaperones
/ isolation & purification
Nucleosome Assembly Protein 1
/ physiology
Organelle Biogenesis
Protein Binding
Protein Biosynthesis
Protein Conformation
Protein Domains
Protein Interaction Mapping
Recombinant Fusion Proteins
/ metabolism
Ribosomal Proteins
/ metabolism
Ribosomes
/ metabolism
Saccharomyces cerevisiae
/ metabolism
Saccharomyces cerevisiae Proteins
/ isolation & purification
Sequence Alignment
Sequence Homology, Amino Acid
Journal
Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011
Informations de publication
Date de publication:
26 07 2019
26 07 2019
Historique:
accepted:
19
04
2019
revised:
15
04
2019
received:
28
01
2019
pubmed:
8
5
2019
medline:
7
1
2020
entrez:
8
5
2019
Statut:
ppublish
Résumé
Dedicated chaperones protect newly synthesized ribosomal proteins (r-proteins) from aggregation and accompany them on their way to assembly into nascent ribosomes. Currently, only nine of the ∼80 eukaryotic r-proteins are known to be guarded by such chaperones. In search of new dedicated r-protein chaperones, we performed a tandem-affinity purification based screen and looked for factors co-enriched with individual small subunit r-proteins. We report the identification of Nap1 and Tsr4 as direct binding partners of Rps6 and Rps2, respectively. Both factors promote the solubility of their r-protein clients in vitro. While Tsr4 is specific for Rps2, Nap1 has several interaction partners including Rps6 and two other r-proteins. Tsr4 binds co-translationally to the essential, eukaryote-specific N-terminal extension of Rps2, whereas Nap1 interacts with a large, mostly eukaryote-specific binding surface of Rps6. Mutation of the essential Tsr4 and deletion of the non-essential Nap1 both enhance the 40S synthesis defects of the corresponding r-protein mutants. Our findings highlight that the acquisition of eukaryote-specific domains in r-proteins was accompanied by the co-evolution of proteins specialized to protect these domains and emphasize the critical role of r-protein chaperones for the synthesis of eukaryotic ribosomes.
Identifiants
pubmed: 31062022
pii: 5486275
doi: 10.1093/nar/gkz317
pmc: PMC6648895
doi:
Substances chimiques
Molecular Chaperones
0
NAP1 protein, S cerevisiae
0
Nucleosome Assembly Protein 1
0
Recombinant Fusion Proteins
0
Ribosomal Proteins
0
Saccharomyces cerevisiae Proteins
0
TSR4 protein, S cerevisiae
0
Types de publication
Comparative Study
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
6984-7002Informations de copyright
© The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research.
Références
Science. 2011 Dec 16;334(6062):1524-9
pubmed: 22096102
Mol Cell Biol. 2005 May;25(9):3802-13
pubmed: 15831484
Yeast. 2004 Aug;21(11):947-62
pubmed: 15334558
J Biol Chem. 1991 Apr 15;266(11):7025-9
pubmed: 2016313
Mol Cell. 2007 Nov 9;28(3):446-57
pubmed: 17996708
Mol Cell Proteomics. 2014 Sep;13(9):2513-26
pubmed: 24942700
Nat Commun. 2015 Jun 26;6:7494
pubmed: 26112308
Nucleic Acids Res. 2009 Apr;37(6):e45
pubmed: 19237396
Annu Rev Biochem. 2019 Jun 20;88:281-306
pubmed: 30566372
EMBO J. 2002 Dec 2;21(23):6527-38
pubmed: 12456659
Curr Biol. 2001 Nov 27;11(23):1885-90
pubmed: 11728313
Nature. 2003 Oct 16;425(6959):686-91
pubmed: 14562095
Mol Cell. 2015 Jun 4;58(5):854-62
pubmed: 25936803
J Biol Chem. 1992 Oct 15;267(29):20980-6
pubmed: 1400414
Mol Cell Biol. 1997 Sep;17(9):5146-55
pubmed: 9271392
PLoS Genet. 2015 Oct 08;11(10):e1005565
pubmed: 26447800
Mol Cell Biol. 2001 Feb;21(4):1260-71
pubmed: 11158312
Trends Biochem Sci. 2017 Aug;42(8):640-654
pubmed: 28579196
J Biol Chem. 2017 Jan 13;292(2):585-596
pubmed: 27913624
Mol Cell Biol. 2016 Nov 28;36(24):3019-3032
pubmed: 27697862
Yeast. 1998 Jul;14(10):953-61
pubmed: 9717241
FASEB J. 2007 May;21(7):1294-310
pubmed: 17317729
Science. 2012 Nov 2;338(6107):666-71
pubmed: 23118189
J Biol Chem. 2003 Nov 7;278(45):44574-83
pubmed: 12928440
PLoS Biol. 2009 Oct;7(10):e1000213
pubmed: 19806183
Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1248-53
pubmed: 16432217
Elife. 2017 Feb 28;6:
pubmed: 28244370
J Biol Chem. 2006 Jun 16;281(24):16462-72
pubmed: 16531623
Nat Commun. 2016 Feb 02;7:10336
pubmed: 26831757
J Cell Biol. 1995 Aug;130(3):675-85
pubmed: 7622567
J Cell Biol. 2010 Apr 5;189(1):57-68
pubmed: 20368618
Elife. 2014 Aug 21;3:e03473
pubmed: 25144938
Proc Natl Acad Sci U S A. 2013 Sep 17;110(38):15253-8
pubmed: 24003121
PLoS One. 2019 Jan 17;14(1):e0203415
pubmed: 30653518
Nat Commun. 2018 Sep 10;9(1):3669
pubmed: 30201955
Bioessays. 2017 Jan;39(1):1-12
pubmed: 27859409
Nat Struct Mol Biol. 2017 Nov;24(11):944-953
pubmed: 28945246
Mol Cell Biol. 2008 Feb;28(4):1313-25
pubmed: 18086883
Nat Commun. 2017 Dec 20;8(1):2213
pubmed: 29263326
Genes Cells. 2016 Mar;21(3):252-63
pubmed: 26841755
J Biol Chem. 2005 Jan 21;280(3):1817-25
pubmed: 15516689
Nature. 2006 Mar 30;440(7084):637-43
pubmed: 16554755
Mol Cell Biol. 2000 Nov;20(21):7971-9
pubmed: 11027267
Science. 2008 Oct 3;322(5898):104-10
pubmed: 18719252
Wiley Interdiscip Rev RNA. 2019 Jan;10(1):e1516
pubmed: 30406965
Bioinformatics. 2002 Jan;18(1):207-8
pubmed: 11836235
Sci Rep. 2016 Nov 07;6:36714
pubmed: 27819319
Nature. 2006 Mar 30;440(7084):631-6
pubmed: 16429126
Nat Struct Mol Biol. 2017 Nov;24(11):954-964
pubmed: 28967883
EMBO J. 2002 Feb 1;21(3):377-86
pubmed: 11823430
Curr Opin Struct Biol. 2014 Feb;24:165-9
pubmed: 24524803
PLoS Biol. 2014 May 13;12(5):e1001860
pubmed: 24823650
Mol Cell. 2005 Oct 28;20(2):263-75
pubmed: 16246728
PLoS One. 2011 Jan 20;6(1):e16194
pubmed: 21283762
J Cell Biol. 1993 Mar;120(6):1305-20
pubmed: 8449978
Anal Chem. 1996 Mar 1;68(5):850-8
pubmed: 8779443
Biochem Biophys Res Commun. 2015 Sep 18;465(2):200-5
pubmed: 26241676
J Cell Biol. 2010 Apr 5;189(1):69-81
pubmed: 20368619
Yeast. 1998 Mar 30;14(5):471-7
pubmed: 9559554
Elife. 2016 Dec 08;5:
pubmed: 27929371
EMBO J. 2016 Jul 1;35(13):1465-82
pubmed: 27225933
Annu Rev Biochem. 2015;84:93-129
pubmed: 25706898
Mol Cell Biol. 2003 Sep;23(18):6672-84
pubmed: 12944491
Nat Commun. 2017 Feb 02;8:14354
pubmed: 28148929
Trends Biochem Sci. 1999 Nov;24(11):437-40
pubmed: 10542411
J Biol Chem. 2008 Nov 21;283(47):32412-8
pubmed: 18728017
J Biol Chem. 2012 Jun 22;287(26):21806-15
pubmed: 22570489
Biochem Cell Biol. 2006 Aug;84(4):549-58
pubmed: 16936827
Genetics. 2013 Nov;195(3):643-81
pubmed: 24190922
PLoS One. 2016 Jan 25;11(1):e0147631
pubmed: 26807849
J Cell Biol. 1997 Jul 14;138(1):119-30
pubmed: 9214386