Literature DB >> 19616560

Highly cooperative recruitment of Ets-1 and release of autoinhibition by Pax5.

Daniel Fitzsimmons1, Kara Lukin, Ryan Lutz, Colin W Garvie, Cynthia Wolberger, James Hagman.   

Abstract

Pax5 (paired box binding factor 5) is a critical regulator of transcription and lineage commitment in B lymphocytes. In B cells, mb-1 (Ig-alpha/immunoglobulin-associated alpha) promoter transcription is activated by Pax5 through its recruitment of E74-like transforming sequence (Ets) family proteins to a composite site, the P5-EBS (Pax5-Ets binding site). Previously, X-ray crystallographic analysis revealed a network of contacts between the DNA-binding domains of Pax5 and Ets-1 while bound to the P5-EBS. Here, we report that Pax5 assembles these ternary complexes via highly cooperative interactions that overcome the autoinhibition of Ets-1. Using recombinant proteins, we calculated K(d(app)) values for the binding of Pax5, Ets-1, and GA-binding proteins, separately or together, to the P5-EBS. By itself, Pax5 binds the P5-EBS with high affinity (K(d) approximately equal 2 nM). Ets-1(331-440) bound the P5-EBS by itself with low affinity (K(d)=136 nM). However, autoinhibited Ets-1(280-440) alone does not bind detectably to the suboptimal sequences of the P5-EBS. Recruitment of Ets-1(331-440) or Ets-1(280-440) resulted in highly efficient ternary complex assembly with Pax5. Pax5 counteracts autoinhibition and increases binding of Ets-1 of the mb-1 promoter by >1000-fold. Mutation of Pax5 Gln22 to alanine (Q22A) enhances promoter binding by Pax5; however, Q22A greatly reduces recruitment of Ets-1(331-440) and Ets-1(280-440) by Pax5 (8.9- or >300-fold, respectively). Thus, Gln22 of Pax5 is essential for overcoming Ets-1 autoinhibition. Pax5 wild type and Q22A each recruited GA-binding protein alpha/beta1 to the mb-1 promoter with similar affinities, but recruitment was less efficient than that of Ets-1 (reduced by approximately 8-fold). Our results suggest a mechanism that allows Pax5 to overcome autoinhibition of Ets-1 DNA binding. In summary, these data illustrate requirements for partnerships between Ets proteins and Pax5.

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Year:  2009        PMID: 19616560      PMCID: PMC2763353          DOI: 10.1016/j.jmb.2009.07.028

Source DB:  PubMed          Journal:  J Mol Biol        ISSN: 0022-2836            Impact factor:   5.469


  44 in total

1.  The alpha and beta subunits of the GA-binding protein form a stable heterodimer in solution. Revised model of heterotetrameric complex assembly.

Authors:  Y Chinenov; M Henzl; M E Martin
Journal:  J Biol Chem       Date:  2000-03-17       Impact factor: 5.157

2.  Phosphorylation represses Ets-1 DNA binding by reinforcing autoinhibition.

Authors:  D O Cowley; B J Graves
Journal:  Genes Dev       Date:  2000-02-01       Impact factor: 11.361

3.  Structural studies of Ets-1/Pax5 complex formation on DNA.

Authors:  C W Garvie; J Hagman; C Wolberger
Journal:  Mol Cell       Date:  2001-12       Impact factor: 17.970

4.  Inhibitory module of Ets-1 allosterically regulates DNA binding through a dipole-facilitated phosphate contact.

Authors:  Hong Wang; Lawrence P McIntosh; Barbara J Graves
Journal:  J Biol Chem       Date:  2001-10-31       Impact factor: 5.157

5.  Activation of the early B-cell-specific mb-1 (Ig-alpha) gene by Pax-5 is dependent on an unmethylated Ets binding site.

Authors:  Holly Maier; Jeff Colbert; Daniel Fitzsimmons; Dawn R Clark; James Hagman
Journal:  Mol Cell Biol       Date:  2003-03       Impact factor: 4.272

Review 6.  Autoinhibitory domains: modular effectors of cellular regulation.

Authors:  Miles A Pufall; Barbara J Graves
Journal:  Annu Rev Cell Dev Biol       Date:  2002-04-02       Impact factor: 13.827

7.  Structural analysis of the autoinhibition of Ets-1 and its role in protein partnerships.

Authors:  Colin W Garvie; Miles A Pufall; Barbara J Graves; Cynthia Wolberger
Journal:  J Biol Chem       Date:  2002-09-06       Impact factor: 5.157

8.  Expression profiles frame the promoter specificity dilemma of the ETS family of transcription factors.

Authors:  Peter C Hollenhorst; David A Jones; Barbara J Graves
Journal:  Nucleic Acids Res       Date:  2004-10-21       Impact factor: 16.971

9.  Highly conserved amino acids in Pax and Ets proteins are required for DNA binding and ternary complex assembly.

Authors:  D Fitzsimmons; R Lutz; W Wheat; H M Chamberlin; J Hagman
Journal:  Nucleic Acids Res       Date:  2001-10-15       Impact factor: 16.971

10.  Requirements for selective recruitment of Ets proteins and activation of mb-1/Ig-alpha gene transcription by Pax-5 (BSAP).

Authors:  Holly Maier; Rachel Ostraat; Sarah Parenti; Daniel Fitzsimmons; Lawrence J Abraham; Colin W Garvie; James Hagman
Journal:  Nucleic Acids Res       Date:  2003-10-01       Impact factor: 16.971

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  14 in total

Review 1.  Molecular mechanisms of ETS transcription factor-mediated tumorigenesis.

Authors:  Adwitiya Kar; Arthur Gutierrez-Hartmann
Journal:  Crit Rev Biochem Mol Biol       Date:  2013-09-25       Impact factor: 8.250

2.  Multiple DNA-binding modes for the ETS family transcription factor PU.1.

Authors:  Shingo Esaki; Marina G Evich; Noa Erlitzki; Markus W Germann; Gregory M K Poon
Journal:  J Biol Chem       Date:  2017-08-08       Impact factor: 5.157

Review 3.  Signatures of DNA target selectivity by ETS transcription factors.

Authors:  Gregory M K Poon; Hye Mi Kim
Journal:  Transcription       Date:  2017-03-16

4.  Autoinhibition of ETV6 DNA Binding Is Established by the Stability of Its Inhibitory Helix.

Authors:  Soumya De; Mark Okon; Barbara J Graves; Lawrence P McIntosh
Journal:  J Mol Biol       Date:  2016-02-23       Impact factor: 5.469

5.  Steric mechanism of auto-inhibitory regulation of specific and non-specific DNA binding by the ETS transcriptional repressor ETV6.

Authors:  Soumya De; Anson C K Chan; H Jerome Coyne; Niraja Bhachech; Ulrike Hermsdorf; Mark Okon; Michael E P Murphy; Barbara J Graves; Lawrence P McIntosh
Journal:  J Mol Biol       Date:  2013-12-12       Impact factor: 5.469

6.  Gene deregulation and chronic activation in natural killer cells deficient in the transcription factor ETS1.

Authors:  Kevin Ramirez; Katherine J Chandler; Christina Spaulding; Sasan Zandi; Mikael Sigvardsson; Barbara J Graves; Barbara L Kee
Journal:  Immunity       Date:  2012-05-17       Impact factor: 31.745

7.  Mechanism of cognate sequence discrimination by the ETS-family transcription factor ETS-1.

Authors:  Kenneth Huang; Suela Xhani; Amanda V Albrecht; Van L T Ha; Shingo Esaki; Gregory M K Poon
Journal:  J Biol Chem       Date:  2019-05-02       Impact factor: 5.157

8.  ETV4 and AP1 Transcription Factors Form Multivalent Interactions with three Sites on the MED25 Activator-Interacting Domain.

Authors:  Simon L Currie; Jedediah J Doane; Kathryn S Evans; Niraja Bhachech; Bethany J Madison; Desmond K W Lau; Lawrence P McIntosh; Jack J Skalicky; Kathleen A Clark; Barbara J Graves
Journal:  J Mol Biol       Date:  2017-07-17       Impact factor: 5.469

Review 9.  Review of Ets1 structure, function, and roles in immunity.

Authors:  Lee Ann Garrett-Sinha
Journal:  Cell Mol Life Sci       Date:  2013-01-05       Impact factor: 9.261

10.  ETS variant transcription factor 5 and c-Myc cooperate in derepressing the human telomerase gene promoter via composite ETS/E-box motifs.

Authors:  Fan Zhang; Shuwen Wang; Jiyue Zhu
Journal:  J Biol Chem       Date:  2020-06-09       Impact factor: 5.157

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