DNA selection by the master transcription factor PU.1.

CD11B CP: Molecular biology CSF1R DNA methylation DNA specificity ETS transcription factors PU.1 SPI1 epigenetic regulation non-canonical binding protein-DNA interactions

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
25 07 2023
Historique:
received: 13 12 2022
revised: 07 04 2023
accepted: 02 06 2023
medline: 31 7 2023
pubmed: 23 6 2023
entrez: 23 6 2023
Statut: ppublish

Résumé

The master transcriptional regulator PU.1/Spi-1 engages DNA sites with affinities spanning multiple orders of magnitude. To elucidate this remarkable plasticity, we have characterized 22 high-resolution co-crystallographic PU.1/DNA complexes across the addressable affinity range in myeloid gene transactivation. Over a purine-rich core (such as 5'-GGAA-3') flanked by variable sequences, affinity is negotiated by direct readout on the 5' flank via a critical glutamine (Q226) sidechain and by indirect readout on the 3' flank by sequence-dependent helical flexibility. Direct readout by Q226 dynamically specifies PU.1's characteristic preference for purines and explains the pathogenic mutation Q226E in Waldenström macroglobulinemia. The structures also reveal how disruption of Q226 mediates strand-specific inhibition by DNA methylation and the recognition of non-canonical sites, including the authentic binding sequence at the CD11b promoter. A re-synthesis of phylogenetic and structural data on the ETS family, considering the centrality of Q226 in PU.1, unifies the model of DNA selection by ETS proteins.

Identifiants

pubmed: 37352101
pii: S2211-1247(23)00682-4
doi: 10.1016/j.celrep.2023.112671
pmc: PMC10479921
mid: NIHMS1920472
pii:
doi:

Substances chimiques

proto-oncogene protein Spi-1 0
Trans-Activators 0
DNA 9007-49-2

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

112671

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM111749
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL155178
Pays : United States
Organisme : NIGMS NIH HHS
ID : R21 GM137160
Pays : United States
Organisme : NCI NIH HHS
ID : R35 CA253127
Pays : United States

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests U.S. has received research funding from GlaxoSmithKline, Bayer Healthcare, Aileron Therapeutics, and Novartis; has received compensation for consultancy services and for serving on scientific advisory boards from GlaxoSmithKline, Bayer Healthcare, Celgene, Aileron Therapeutics, Stelexis Therapeutics, and Pieris Pharmaceuticals; and has equity ownership in and is serving on the board of directors of Stelexis Therapeutics.

Références

Mol Cell. 2002 Nov;10(5):1097-105
pubmed: 12453417
BMC Genomics. 2015;16 Suppl 7:S12
pubmed: 26099425
Cell. 2013 Jan 17;152(1-2):327-39
pubmed: 23332764
Nucleic Acids Res. 2019 Apr 8;47(6):e31
pubmed: 30657937
Nat Commun. 2019 Apr 29;10(1):1930
pubmed: 31036827
Nature. 1996 Apr 4;380(6573):456-60
pubmed: 8602247
Proc Natl Acad Sci U S A. 2016 Jun 7;113(23):6508-13
pubmed: 27155014
Cell Mol Life Sci. 2018 May;75(9):1587-1612
pubmed: 29335749
Acta Crystallogr D Biol Crystallogr. 2011 Apr;67(Pt 4):235-42
pubmed: 21460441
Blood. 1997 Jul 15;90(2):489-519
pubmed: 9226149
Mol Inform. 2021 Jan;40(1):e2000144
pubmed: 32830452
Nat Genet. 2006 Jan;38(1):27-37
pubmed: 16311598
Annu Rev Biochem. 2011;80:437-71
pubmed: 21548782
Nat Rev Mol Cell Biol. 2017 Mar;18(3):159-174
pubmed: 28053348
Sci Adv. 2020 Feb 21;6(8):eaay3178
pubmed: 32128405
J Biol Chem. 1995 Oct 13;270(41):24258-63
pubmed: 7592633
Science. 2009 Apr 17;324(5925):407-10
pubmed: 19372434
J Biol Chem. 2017 Sep 29;292(39):16044-16054
pubmed: 28790174
Trends Genet. 2010 Feb;26(2):75-83
pubmed: 20074831
EMBO J. 2010 Jul 7;29(13):2147-60
pubmed: 20517297
Nucleic Acids Res. 2003 Sep 1;31(17):5108-21
pubmed: 12930962
J Mol Biol. 2000 Jan 7;295(1):85-103
pubmed: 10623510
Sci Immunol. 2022 May 20;7(71):eabm1920
pubmed: 35594339
J Mol Biol. 2003 May 9;328(4):805-19
pubmed: 12729756
Blood. 2005 Sep 1;106(5):1519-24
pubmed: 15914558
Mol Cell Biol. 1994 Jan;14(1):373-81
pubmed: 8264604
Nat Med. 2015 Oct;21(10):1172-81
pubmed: 26343801
J Clin Invest. 2017 Dec 1;127(12):4297-4313
pubmed: 29083320
Nucleic Acids Res. 2003 Jul 1;31(13):3487-90
pubmed: 12824350
Annu Rev Biochem. 2010;79:233-69
pubmed: 20334529
Nat Rev Genet. 2009 Apr;10(4):252-63
pubmed: 19274049
J Biol Chem. 1993 Mar 5;268(7):5014-20
pubmed: 8095266
Cell. 2014 Sep 11;158(6):1431-1443
pubmed: 25215497
PLoS Genet. 2019 Oct 7;15(10):e1008444
pubmed: 31589607
Nature. 1998 Apr 30;392(6679):885-8
pubmed: 9582068
Nat Methods. 2016 Jan;13(1):55-8
pubmed: 26569599
Science. 2015 Oct 16;350(6258):325-8
pubmed: 26472909
Science. 2008 Jun 13;320(5882):1496-501
pubmed: 18497260
Nat Commun. 2020 Jan 21;11(1):402
pubmed: 31964861
J Biol Chem. 2019 Jun 21;294(25):9666-9678
pubmed: 31048376
Annu Rev Cell Dev Biol. 2019 Oct 6;35:357-379
pubmed: 31283382
Nat Commun. 2019 Jun 20;10(1):2723
pubmed: 31222014
Biochemistry. 2005 May 17;44(19):7095-106
pubmed: 15882048
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501
pubmed: 20383002
J Biomol NMR. 1997 Dec;10(4):317-28
pubmed: 9460239
PLoS One. 2016 Oct 5;11(10):e0163962
pubmed: 27706213
Nat Rev Cancer. 2019 Nov;19(11):611-624
pubmed: 31511663
Blood. 1992 Feb 1;79(3):586-93
pubmed: 1531036
Nucleic Acids Res. 2018 Nov 16;46(20):10577-10588
pubmed: 30295801
Mol Cell. 2010 May 28;38(4):576-89
pubmed: 20513432
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21
pubmed: 20124702
Cancer Discov. 2019 Jun;9(6):796-811
pubmed: 31018969
Nucleic Acids Res. 2013 Jul;41(13):6391-402
pubmed: 23658224
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):125-32
pubmed: 20124692
Nat Biotechnol. 2016 Jul;34(7):760-7
pubmed: 27240196
J Biol Chem. 2014 Aug 1;289(31):21605-16
pubmed: 24952944
Biopolymers. 1997;44(4):361-403
pubmed: 9782776
Nucleic Acids Res. 2014 Jan;42(2):1379-90
pubmed: 24157839
EMBO J. 1995 Apr 18;14(8):1812-8
pubmed: 7737131
Nucleic Acids Res. 2016 May 19;44(9):4005-13
pubmed: 27079976
Cell Stem Cell. 2019 Aug 1;25(2):258-272.e9
pubmed: 31374198
Protein Sci. 1999 Oct;8(10):2098-109
pubmed: 10548056
Immunity. 2010 May 28;32(5):628-41
pubmed: 20510871
Genome Res. 2018 Oct;28(10):1508-1519
pubmed: 30171019
Proc Natl Acad Sci U S A. 1998 Sep 15;95(19):11163-8
pubmed: 9736707
J Chem Phys. 2007 Jan 7;126(1):014101
pubmed: 17212484
Nat Struct Mol Biol. 2004 Sep;11(9):812-5
pubmed: 15332082
Immunity. 2018 Oct 16;49(4):782
pubmed: 30332634
Cell. 2018 Feb 8;172(4):650-665
pubmed: 29425488
Nat Immunol. 2003 Oct;4(10):1029-36
pubmed: 12958595
J Mol Biol. 2019 Feb 1;431(3):593-614
pubmed: 30597162
Nature. 2020 Jul;583(7816):431-436
pubmed: 32581360
Nucleic Acids Res. 2004 Oct 21;32(18):5693-702
pubmed: 15498926

Auteurs

J Ross Terrell (JR)

Department of Chemistry, Georgia State University, Atlanta, GA 30303, USA.

Samuel J Taylor (SJ)

Departments of Cell Biology, Oncology, and Medicine, Ruth L. and David S. Gottesman Institute for Stem Cell Research and Regenerative Medicine, Blood Cancer Institute, and the Montefiore Einstein Cancer Center, Albert Einstein College of Medicine, Bronx, NY 10461, USA.

Amelia L Schneider (AL)

Department of Chemistry, Georgia State University, Atlanta, GA 30303, USA.

Yue Lu (Y)

Department of Chemistry, Georgia State University, Atlanta, GA 30303, USA.

Tyler N Vernon (TN)

Department of Chemistry, Georgia State University, Atlanta, GA 30303, USA.

Suela Xhani (S)

Department of Chemistry, Georgia State University, Atlanta, GA 30303, USA.

Ryan H Gumpper (RH)

Department of Chemistry, Georgia State University, Atlanta, GA 30303, USA.

Ming Luo (M)

Department of Chemistry, Georgia State University, Atlanta, GA 30303, USA; Center for Diagnostics and Therapeutics, Georgia State University, Atlanta, GA 30303, USA.

W David Wilson (WD)

Department of Chemistry, Georgia State University, Atlanta, GA 30303, USA; Center for Diagnostics and Therapeutics, Georgia State University, Atlanta, GA 30303, USA.

Ulrich Steidl (U)

Departments of Cell Biology, Oncology, and Medicine, Ruth L. and David S. Gottesman Institute for Stem Cell Research and Regenerative Medicine, Blood Cancer Institute, and the Montefiore Einstein Cancer Center, Albert Einstein College of Medicine, Bronx, NY 10461, USA. Electronic address: ulrich.steidl@einsteinmed.edu.

Gregory M K Poon (GMK)

Department of Chemistry, Georgia State University, Atlanta, GA 30303, USA; Center for Diagnostics and Therapeutics, Georgia State University, Atlanta, GA 30303, USA. Electronic address: gpoon@gsu.edu.

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Classifications MeSH