Structural characterization of B. subtilis m1A22 tRNA methyltransferase TrmK: insights into tRNA recognition.


Journal

Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011

Informations de publication

Date de publication:
21 05 2019
Historique:
accepted: 26 03 2019
revised: 04 03 2019
received: 13 12 2018
pubmed: 2 4 2019
medline: 26 11 2019
entrez: 2 4 2019
Statut: ppublish

Résumé

1-Methyladenosine (m1A) is a modified nucleoside found at positions 9, 14, 22 and 58 of tRNAs, which arises from the transfer of a methyl group onto the N1-atom of adenosine. The yqfN gene of Bacillus subtilis encodes the methyltransferase TrmK (BsTrmK) responsible for the formation of m1A22 in tRNA. Here, we show that BsTrmK displays a broad substrate specificity, and methylates seven out of eight tRNA isoacceptor families of B. subtilis bearing an A22. In addition to a non-Watson-Crick base-pair between the target A22 and a purine at position 13, the formation of m1A22 by BsTrmK requires a full-length tRNA with intact tRNA elbow and anticodon stem. We solved the crystal structure of BsTrmK showing an N-terminal catalytic domain harbouring the typical Rossmann-like fold of Class-I methyltransferases and a C-terminal coiled-coil domain. We used NMR chemical shift mapping to drive the docking of BstRNASer to BsTrmK in complex with its methyl-donor cofactor S-adenosyl-L-methionine (SAM). In this model, validated by methyltransferase activity assays on BsTrmK mutants, both domains of BsTrmK participate in tRNA binding. BsTrmK recognises tRNA with very few structural changes in both partner, the non-Watson-Crick R13-A22 base-pair positioning the A22 N1-atom close to the SAM methyl group.

Identifiants

pubmed: 30931478
pii: 5424071
doi: 10.1093/nar/gkz230
pmc: PMC6511850
doi:

Substances chimiques

Anticodon 0
RNA Recognition Motif Proteins 0
S-Adenosylmethionine 7LP2MPO46S
RNA, Transfer 9014-25-9
tRNA Methyltransferases EC 2.1.1.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4736-4750

Informations de copyright

© The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research.

Références

Proc Natl Acad Sci U S A. 2008 May 13;105(19):6876-81
pubmed: 18451029
J Phys Chem B. 2009 Feb 12;113(6):1743-55
pubmed: 19152254
Nat Methods. 2010 Apr;7(4):291-4
pubmed: 20190761
J Biomol NMR. 1998 Aug;12(2):345-8
pubmed: 21136330
Nucleic Acids Res. 2010 Oct;38(19):6533-43
pubmed: 20525789
Nucleic Acids Res. 2009 Jan;37(Database issue):D159-62
pubmed: 18957446
Nucleic Acids Res. 2010 Oct;38(18):6206-18
pubmed: 20483913
Nucleic Acids Res. 2016 Jan 29;44(2):940-53
pubmed: 26673726
RNA. 2013 Aug;19(8):1137-46
pubmed: 23793893
Biophys Chem. 2016 Mar;210:27-34
pubmed: 26189113
Proteins. 2007 Dec 1;69(4):726-33
pubmed: 17803234
J Am Chem Soc. 2003 Feb 19;125(7):1731-7
pubmed: 12580598
RNA. 2018 Aug;24(8):1080-1092
pubmed: 29848639
Science. 2016 Mar 25;351(6280):aad6253
pubmed: 27013737
J Mol Graph. 1996 Feb;14(1):33-8, 27-8
pubmed: 8744570
BMC Struct Biol. 2011 Dec 14;11:48
pubmed: 22168821
Nucleic Acids Res. 2002 Jul 15;30(14):3152-62
pubmed: 12136097
Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W665-7
pubmed: 15215472
J Biol Chem. 2015 Feb 27;290(9):5912-25
pubmed: 25593312
Cell. 2003 May 2;113(3):383-94
pubmed: 12732145
Science. 1994 Mar 11;263(5152):1404-10
pubmed: 8128220
Life (Basel). 2016 Jan 12;6(1):
pubmed: 26771646
Nucleic Acids Res. 2003 Apr 15;31(8):2148-56
pubmed: 12682365
Nucleic Acids Res. 2004 Feb 11;32(3):1018-27
pubmed: 14960715
Nucleic Acids Res. 2012 Dec;40(22):11583-93
pubmed: 23042678
Prog Nucl Magn Reson Spectrosc. 2011 Oct;59(3):271-92
pubmed: 21920222
Comput Appl Biosci. 1994 Jun;10(3):273-5
pubmed: 7922682
Bioinformatics. 2011 Jun 1;27(11):1575-7
pubmed: 21471012
Nucleic Acids Res. 2018 Jan 4;46(D1):D303-D307
pubmed: 29106616
Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):12648-53
pubmed: 14566049
Methods. 2019 Mar 1;156:91-101
pubmed: 30395967
Protein Sci. 2010 Mar;19(3):617-24
pubmed: 20052680
Nucleic Acids Res. 2005 Jan 1;33(Database issue):D139-40
pubmed: 15608164
Methods Mol Biol. 2016;1320:37-57
pubmed: 26227036
RNA. 2003 May;9(5):574-85
pubmed: 12702816
Nucleic Acids Res. 1998 Jan 1;26(1):316-9
pubmed: 9399863
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501
pubmed: 20383002
Nucleic Acids Res. 2008 Jun;36(10):3252-62
pubmed: 18420655
Nucleic Acids Res. 1977 Jun;4(6):1769-82
pubmed: 408794
Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10037-41
pubmed: 11517324
Biomol NMR Assign. 2016 Oct;10(2):253-7
pubmed: 27098549
J Mol Biol. 2015 Dec 4;427(24):3862-76
pubmed: 26470919
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21
pubmed: 20124702
J Mol Biol. 2008 Mar 21;377(2):535-50
pubmed: 18262540
Nucleic Acids Res. 2004 Jan 22;32(2):465-76
pubmed: 14739239
Biomolecules. 2017 Feb 21;7(1):
pubmed: 28230814
Wiley Interdiscip Rev RNA. 2012 Jan-Feb;3(1):37-61
pubmed: 21957054
Sci Rep. 2016 Sep 01;6:32562
pubmed: 27582183
Nucleic Acids Res. 1995 Nov 11;23(21):4312-9
pubmed: 7501451
Biochemistry. 1999 Oct 5;38(40):13338-46
pubmed: 10529209
Genes (Basel). 2019 Jan 30;10(2):
pubmed: 30704107
Nucleic Acids Res. 1978 Aug;5(8):3033-42
pubmed: 99729
Cell. 2001 Dec 28;107(7):929-39
pubmed: 11779468

Auteurs

Clément Dégut (C)

Laboratoire de Cristallographie et RMN biologiques, CNRS, Université Paris Descartes, Sorbonne Paris Cité, 4 avenue de l'Observatoire, 75006 Paris, France.

Martine Roovers (M)

Institut de Recherches Labiris, B-1070 Bruxelles, Belgium.

Pierre Barraud (P)

Laboratoire de Cristallographie et RMN biologiques, CNRS, Université Paris Descartes, Sorbonne Paris Cité, 4 avenue de l'Observatoire, 75006 Paris, France.
Laboratoire d'Expression génétique microbienne, CNRS, Univ. Paris Diderot, Sorbonne Paris Cité, Institut de Biologie Physico-Chimique, IBPC, 13 rue Pierre et Marie Curie, 75005 Paris, France.

Franck Brachet (F)

Laboratoire de Cristallographie et RMN biologiques, CNRS, Université Paris Descartes, Sorbonne Paris Cité, 4 avenue de l'Observatoire, 75006 Paris, France.

André Feller (A)

Laboratoire de Microbiologie, Université libre de Bruxelles (ULB), 6041 Gosselies, Belgium.

Valéry Larue (V)

Laboratoire de Cristallographie et RMN biologiques, CNRS, Université Paris Descartes, Sorbonne Paris Cité, 4 avenue de l'Observatoire, 75006 Paris, France.

Abdalla Al Refaii (A)

Laboratoire de Microbiologie, Université libre de Bruxelles (ULB), 6041 Gosselies, Belgium.

Joël Caillet (J)

Laboratoire d'Expression génétique microbienne, CNRS, Univ. Paris Diderot, Sorbonne Paris Cité, Institut de Biologie Physico-Chimique, IBPC, 13 rue Pierre et Marie Curie, 75005 Paris, France.

Louis Droogmans (L)

Laboratoire de Microbiologie, Université libre de Bruxelles (ULB), 6041 Gosselies, Belgium.

Carine Tisné (C)

Laboratoire de Cristallographie et RMN biologiques, CNRS, Université Paris Descartes, Sorbonne Paris Cité, 4 avenue de l'Observatoire, 75006 Paris, France.
Laboratoire d'Expression génétique microbienne, CNRS, Univ. Paris Diderot, Sorbonne Paris Cité, Institut de Biologie Physico-Chimique, IBPC, 13 rue Pierre et Marie Curie, 75005 Paris, France.

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Classifications MeSH