Structure, function, and tethering of DNA-binding domains in σ54 transcriptional activators

Vidangos, Natasha; Maris, Ann E.; Young, Anisa; Hong, Eunmi; Pelton, Jeffrey G.; Batchelor, Joseph D.; Wemmer, David E.

doi:10.1002/bip.22333

Title: Structure, function, and tethering of DNA-binding domains in σ⁵⁴ transcriptional activators

Abstract

In this paper, we compare the structure, activity, and linkage of DNA-binding domains (DBDs) from σ⁵⁴ transcriptional activators and discuss how the properties of the DBDs and the linker to the neighboring domain are affected by the overall properties and requirements of the full proteins. These transcriptional activators bind upstream of specific promoters that utilize σ⁵⁴-polymerase. Upon receiving a signal the activators assemble into hexamers, which then, through adenosine triphosphate (ATP) hydrolysis, drive a conformational change in polymerase that enables transcription initiation. We present structures of the DBDs of activators nitrogen regulatory protein C 1 (NtrC1) and Nif-like homolog 2 (Nlh2) from the thermophile Aquifex aeolicus. The structures of these domains and their relationship to other parts of the activators are discussed. These structures are compared with previously determined structures of the DBDs of NtrC4, NtrC, ZraR, and factor for inversion stimulation. The N-terminal linkers that connect the DBDs to the central domains in NtrC1 and Nlh2 were studied and found to be unstructured. Additionally, a crystal structure of full-length NtrC1 was solved, but density of the DBDs was extremely weak, further indicating that the linker between ATPase and DBDs functions as a flexible tether. Flexible linking of ATPase andmore »« less

Authors:

Vidangos, Natasha ^[1]; Maris, Ann E. ^[1]; Young, Anisa ^[1]; Hong, Eunmi ^[1]; Pelton, Jeffrey G. ^[1]; Batchelor, Joseph D. ^[1]; Wemmer, David E. ^[1]

Univ. of California, Berkeley, CA (United States). Dept. of Chemistry. QB3 Inst.

Publication Date:: Tue Jul 02 00:00:00 EDT 2013

Research Org.:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of Health (NIH) (United States); National Science Foundation (NSF)

OSTI Identifier:: 1407209

Grant/Contract Number:: AC02-05CH11231; FG05-86ER75281; GM62163; RR15756; DMB 86-09305; BBS 87-20134; BBS 01-19304

Resource Type:: Accepted Manuscript

Journal Name:: Biopolymers

Additional Journal Information:: Journal Volume: 99; Journal Issue: 12; Journal ID: ISSN 0006-3525

Publisher:: Wiley

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; bacterial transcription; sigma factor; DNA-binding domain

Citation Formats


                    Vidangos, Natasha, Maris, Ann E., Young, Anisa, Hong, Eunmi, Pelton, Jeffrey G., Batchelor, Joseph D., and Wemmer, David E. Structure, function, and tethering of DNA-binding domains in σ54 transcriptional activators.  United States: N. p., 2013. 
Web.  doi:10.1002/bip.22333.

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                    Vidangos, Natasha, Maris, Ann E., Young, Anisa, Hong, Eunmi, Pelton, Jeffrey G., Batchelor, Joseph D., & Wemmer, David E. Structure, function, and tethering of DNA-binding domains in σ54 transcriptional activators.  United States.  https://doi.org/10.1002/bip.22333

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                    Vidangos, Natasha, Maris, Ann E., Young, Anisa, Hong, Eunmi, Pelton, Jeffrey G., Batchelor, Joseph D., and Wemmer, David E. Tue .  
"Structure, function, and tethering of DNA-binding domains in σ54 transcriptional activators".  United States.  https://doi.org/10.1002/bip.22333.  https://www.osti.gov/servlets/purl/1407209.

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@article{osti_1407209,

  title        = {Structure, function, and tethering of DNA-binding domains in σ54 transcriptional activators},

  author       = {Vidangos, Natasha and Maris, Ann E. and Young, Anisa and Hong, Eunmi and Pelton, Jeffrey G. and Batchelor, Joseph D. and Wemmer, David E.},

  abstractNote = {In this paper, we compare the structure, activity, and linkage of DNA-binding domains (DBDs) from σ54 transcriptional activators and discuss how the properties of the DBDs and the linker to the neighboring domain are affected by the overall properties and requirements of the full proteins. These transcriptional activators bind upstream of specific promoters that utilize σ54-polymerase. Upon receiving a signal the activators assemble into hexamers, which then, through adenosine triphosphate (ATP) hydrolysis, drive a conformational change in polymerase that enables transcription initiation. We present structures of the DBDs of activators nitrogen regulatory protein C 1 (NtrC1) and Nif-like homolog 2 (Nlh2) from the thermophile Aquifex aeolicus. The structures of these domains and their relationship to other parts of the activators are discussed. These structures are compared with previously determined structures of the DBDs of NtrC4, NtrC, ZraR, and factor for inversion stimulation. The N-terminal linkers that connect the DBDs to the central domains in NtrC1 and Nlh2 were studied and found to be unstructured. Additionally, a crystal structure of full-length NtrC1 was solved, but density of the DBDs was extremely weak, further indicating that the linker between ATPase and DBDs functions as a flexible tether. Flexible linking of ATPase and DBDs is likely necessary to allow assembly of the active hexameric ATPase ring. Finally, the comparison of this set of activators also shows clearly that strong dimerization of the DBD only occurs when other domains do not dimerize strongly.},

  doi          = {10.1002/bip.22333},

  journal      = {Biopolymers},

  number       = 12,

  volume       = 99,

  place        = {United States},

  year         = {Tue Jul 02 00:00:00 EDT 2013},

  month        = {Tue Jul 02 00:00:00 EDT 2013}

}

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Works referencing / citing this record:

The Azoarcus anaerobius 1,3-Dihydroxybenzene (Resorcinol) Anaerobic Degradation Pathway Is Controlled by the Coordinated Activity of Two Enhancer-Binding Proteins
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Nucleic Acids Research, Vol. 44, Issue 22
DOI: 10.1093/nar/gkw1150

σ54-dependent regulome in Desulfovibrio vulgaris Hildenborough
journal, November 2015

Kazakov, Alexey E.; Rajeev, Lara; Chen, Amy
BMC Genomics, Vol. 16, Issue 1
DOI: 10.1186/s12864-015-2176-y

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Title: Structure, function, and tethering of DNA-binding domains in σ54 transcriptional activators

Abstract

Citation Formats

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Kinetics of transcription initiation directed by multiplecis-regulatory elements on theglnAp2promoter journal, November 2016

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Title: Structure, function, and tethering of DNA-binding domains in σ⁵⁴ transcriptional activators

The Azoarcus anaerobius 1,3-Dihydroxybenzene (Resorcinol) Anaerobic Degradation Pathway Is Controlled by the Coordinated Activity of Two Enhancer-Binding Proteins
journal, March 2017

Kinetics of transcription initiation directed by multiplecis-regulatory elements on theglnAp2promoter
journal, November 2016

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journal, November 2015