Cargando…

Nucleotide-induced asymmetry within ATPase activator ring drives σ54–RNAP interaction and ATP hydrolysis

It is largely unknown how the typical homomeric ring geometry of ATPases associated with various cellular activities enables them to perform mechanical work. Small-angle solution X-ray scattering, crystallography, and electron microscopy (EM) reconstructions revealed that partial ATP occupancy cause...

Descripción completa

Detalles Bibliográficos
Autores principales: Sysoeva, Tatyana A., Chowdhury, Saikat, Guo, Liang, Nixon, B. Tracy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3841738/
https://www.ncbi.nlm.nih.gov/pubmed/24240239
http://dx.doi.org/10.1101/gad.229385.113
_version_ 1782292839160348672
author Sysoeva, Tatyana A.
Chowdhury, Saikat
Guo, Liang
Nixon, B. Tracy
author_facet Sysoeva, Tatyana A.
Chowdhury, Saikat
Guo, Liang
Nixon, B. Tracy
author_sort Sysoeva, Tatyana A.
collection PubMed
description It is largely unknown how the typical homomeric ring geometry of ATPases associated with various cellular activities enables them to perform mechanical work. Small-angle solution X-ray scattering, crystallography, and electron microscopy (EM) reconstructions revealed that partial ATP occupancy caused the heptameric closed ring of the bacterial enhancer-binding protein (bEBP) NtrC1 to rearrange into a hexameric split ring of striking asymmetry. The highly conserved and functionally crucial GAFTGA loops responsible for interacting with σ54–RNA polymerase formed a spiral staircase. We propose that splitting of the ensemble directs ATP hydrolysis within the oligomer, and the ring's asymmetry guides interaction between ATPase and the complex of σ54 and promoter DNA. Similarity between the structure of the transcriptional activator NtrC1 and those of distantly related helicases Rho and E1 reveals a general mechanism in homomeric ATPases whereby complex allostery within the ring geometry forms asymmetric functional states that allow these biological motors to exert directional forces on their target macromolecules.
format Online
Article
Text
id pubmed-3841738
institution National Center for Biotechnology Information
language English
publishDate 2013
publisher Cold Spring Harbor Laboratory Press
record_format MEDLINE/PubMed
spelling pubmed-38417382014-05-15 Nucleotide-induced asymmetry within ATPase activator ring drives σ54–RNAP interaction and ATP hydrolysis Sysoeva, Tatyana A. Chowdhury, Saikat Guo, Liang Nixon, B. Tracy Genes Dev Research Paper It is largely unknown how the typical homomeric ring geometry of ATPases associated with various cellular activities enables them to perform mechanical work. Small-angle solution X-ray scattering, crystallography, and electron microscopy (EM) reconstructions revealed that partial ATP occupancy caused the heptameric closed ring of the bacterial enhancer-binding protein (bEBP) NtrC1 to rearrange into a hexameric split ring of striking asymmetry. The highly conserved and functionally crucial GAFTGA loops responsible for interacting with σ54–RNA polymerase formed a spiral staircase. We propose that splitting of the ensemble directs ATP hydrolysis within the oligomer, and the ring's asymmetry guides interaction between ATPase and the complex of σ54 and promoter DNA. Similarity between the structure of the transcriptional activator NtrC1 and those of distantly related helicases Rho and E1 reveals a general mechanism in homomeric ATPases whereby complex allostery within the ring geometry forms asymmetric functional states that allow these biological motors to exert directional forces on their target macromolecules. Cold Spring Harbor Laboratory Press 2013-11-15 /pmc/articles/PMC3841738/ /pubmed/24240239 http://dx.doi.org/10.1101/gad.229385.113 Text en © 2013 Sysoeva et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/3.0/ This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genesdev.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 3.0 Unported), as described at http://creativecommons.org/licenses/by-nc/3.0/.
spellingShingle Research Paper
Sysoeva, Tatyana A.
Chowdhury, Saikat
Guo, Liang
Nixon, B. Tracy
Nucleotide-induced asymmetry within ATPase activator ring drives σ54–RNAP interaction and ATP hydrolysis
title Nucleotide-induced asymmetry within ATPase activator ring drives σ54–RNAP interaction and ATP hydrolysis
title_full Nucleotide-induced asymmetry within ATPase activator ring drives σ54–RNAP interaction and ATP hydrolysis
title_fullStr Nucleotide-induced asymmetry within ATPase activator ring drives σ54–RNAP interaction and ATP hydrolysis
title_full_unstemmed Nucleotide-induced asymmetry within ATPase activator ring drives σ54–RNAP interaction and ATP hydrolysis
title_short Nucleotide-induced asymmetry within ATPase activator ring drives σ54–RNAP interaction and ATP hydrolysis
title_sort nucleotide-induced asymmetry within atpase activator ring drives σ54–rnap interaction and atp hydrolysis
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3841738/
https://www.ncbi.nlm.nih.gov/pubmed/24240239
http://dx.doi.org/10.1101/gad.229385.113
work_keys_str_mv AT sysoevatatyanaa nucleotideinducedasymmetrywithinatpaseactivatorringdrivess54rnapinteractionandatphydrolysis
AT chowdhurysaikat nucleotideinducedasymmetrywithinatpaseactivatorringdrivess54rnapinteractionandatphydrolysis
AT guoliang nucleotideinducedasymmetrywithinatpaseactivatorringdrivess54rnapinteractionandatphydrolysis
AT nixonbtracy nucleotideinducedasymmetrywithinatpaseactivatorringdrivess54rnapinteractionandatphydrolysis