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Conformational shifts in a chemoreceptor helical hairpin control kinase signaling in Escherichia coli

Published on Jul 17, 2019in Proceedings of the National Academy of Sciences of the United States of America 9.58
· DOI :10.1073/pnas.1902521116
Qun Gao (Sichuan Agricultural University), Anchun Cheng (Sichuan Agricultural University), John S. Parkinson43
Estimated H-index: 43
(UofU: University of Utah)
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Abstract
Motile Escherichia coli cells use chemoreceptor signaling arrays to track chemical gradients with exquisite precision. Highly conserved residues in the cytoplasmic hairpin tip of chemoreceptor molecules promote assembly of trimer-based signaling complexes and modulate the activity of their CheA kinase partners. To explore hairpin tip output states in the serine receptor Tsr, we characterized the signaling consequences of amino acid replacements at the salt-bridge residue pair E385-R388. All mutant receptors assembled trimers and signaling complexes, but most failed to support serine chemotaxis in soft agar assays. Small side-chain replacements at either residue produced OFF- or ON-shifted outputs that responded to serine stimuli in wild-type fashion, suggesting that these receptors, like the wild-type, operate as two-state signaling devices. Larger aliphatic or aromatic side chains caused slow or partial kinase control responses that proved dependent on the connections between core signaling units that promote array cooperativity. In a mutant lacking one of two key adapter-kinase contacts (interface 2), those mutant receptors exhibited more wild-type behaviors. Lastly, mutant receptors with charged amino acid replacements assembled signaling complexes that were locked in kinase-ON (E385K|R) or kinase-OFF (R388D|E) output. The hairpin tips of mutant receptors with these more aberrant signaling properties probably have nonnative structures or dynamic behaviors. Our results suggest that chemoeffector stimuli and adaptational modifications influence the cooperative connections between core signaling units. This array remodeling process may involve activity-dependent changes in the relative strengths of interface 1 and 2 interactions between the CheW and CheA.P5 components of receptor core signaling complexes.
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References81
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Caralyn E. Flack (UofU: University of Utah), John S. Parkinson43
Estimated H-index: 43
(UofU: University of Utah)
Environmental awareness is an essential attribute for all organisms. The chemotaxis system of Escherichia coli provides a powerful experimental model for the investigation of stimulus detection and signaling mechanisms at the molecular level. These bacteria sense chemical gradients with transmembrane proteins [methyl-accepting chemotaxis proteins (MCPs)] that have an extracellular ligand-binding domain and intracellular histidine kinases, adenylate cyclases, methyl-accepting proteins, and phosph...
Published on Feb 26, 2018in Journal of Bacteriology 3.23
Xueye Ding (YZU: Yangzhou University), Qiang He (YZU: Yangzhou University)+ 2 AuthorsXiqing Wang (YZU: Yangzhou University)
ABSTRACT The histidine kinase CheA plays a central role in signal integration, conversion, and amplification in the bacterial chemotaxis signal transduction pathway. The kinase activity is regulated in chemotaxis signaling complexes formed via the interactions among CheA9s regulatory domain (P5), the coupling protein CheW, and transmembrane chemoreceptors. Despite recent advancements in the understanding of the architecture of the signaling complex, the molecular mechanism underlying this regula...
Published on Feb 1, 2018in Journal of Molecular Biology 5.07
Germán E. Piñas2
Estimated H-index: 2
(UofU: University of Utah),
Michael D. DeSantis1
Estimated H-index: 1
(UofU: University of Utah),
John S. Parkinson43
Estimated H-index: 43
(UofU: University of Utah)
Abstract In Escherichia coli chemosensory arrays, transmembrane receptors, a histidine autokinase CheA, and a scaffolding protein CheW interact to form an extended hexagonal lattice of signaling complexes. One interaction, previously assigned a crucial signaling role, occurs between chemoreceptors and the CheW-binding P5 domain of CheA. Structural studies showed a receptor helix fitting into a hydrophobic cleft at the boundary between P5 subdomains. Our work aimed to elucidate the in vivo roles ...
Published on Jan 1, 2018
Peter Ames16
Estimated H-index: 16
(UofU: University of Utah),
John S. Parkinson43
Estimated H-index: 43
(UofU: University of Utah)
Published on Dec 12, 2017in eLife 7.55
Johannes M. Keegstra3
Estimated H-index: 3
,
Keita Kamino1
Estimated H-index: 1
+ 3 AuthorsThomas S. Shimizu16
Estimated H-index: 16
Many sophisticated computer programs use random number generators to help solve challenging problems. These problems range from achieving secure communication across the Internet to deciding how best to invest in the stock market. Much research in recent years has found that randomness is also widespread in living cells, where it is often called “noise”. For example, the activity of some genes is so unpredictable to the extent that it appears random. Yet, relatively little is known about how suc...
Published on Dec 12, 2017in eLife 7.55
Remy Colin8
Estimated H-index: 8
(MPG: Max Planck Society),
Christelle Rosazza1
Estimated H-index: 1
(MPG: Max Planck Society)
+ 1 AuthorsVictor Sourjik37
Estimated H-index: 37
(MPG: Max Planck Society)
Cellular networks are intrinsically subject to stochastic fluctuations, but analysis of the resulting noise remained largely limited to gene expression. The pathway controlling chemotaxis of Escherichia coli provides one example where posttranslational signaling noise has been deduced from cellular behavior. This noise was proposed to result from stochasticity in chemoreceptor methylation, and it is believed to enhance environment exploration by bacteria. Here we combined single-cell FRET measur...
Published on Dec 11, 2017in Journal of Bacteriology 3.23
Narahari Akkaladevi , Filiz Bunyak17
Estimated H-index: 17
+ 2 AuthorsGerald L. Hazelbauer22
Estimated H-index: 22
Published on Sep 21, 2017in Journal of Physical Chemistry B 2.92
Maryam Kashefi1
Estimated H-index: 1
,
Lynmarie K. Thompson18
Estimated H-index: 18
Bacteria employ remarkable membrane-bound nanoarrays to sense their environment and direct their swimming. Arrays consist of chemotaxis receptor trimers of dimers that are bridged at their membrane-distal tips by rings of two cytoplasmic proteins, a kinase CheA and a coupling protein CheW. It is not clear how ligand binding to the periplasmic domain of the receptor deactivates the CheA kinase bound to the cytoplasmic tip ∼300 A away, but the mechanism is thought to involve changes in dynamics wi...
Published on Jul 25, 2017in Biochemistry 2.95
Andrea Pedetta2
Estimated H-index: 2
,
Diego A. Massazza6
Estimated H-index: 6
+ 1 AuthorsClaudia A. Studdert8
Estimated H-index: 8
Bacterial chemoreceptors are dimeric membrane proteins that transmit signals from a periplasmic ligand-binding domain to the interior of the cells. The highly conserved cytoplasmic domain consists of a long hairpin that in the dimer forms a four-helix coiled-coil bundle. The central region of the bundle couples changes in helix packing that occur in the membrane proximal region to the signaling tip, controlling the activity of an associated histidine kinase. This subdomain contains certain glyci...
Published on Apr 1, 2017in Biophysical Journal 3.67
Nattakan Sukomon3
Estimated H-index: 3
(Cornell University),
Joanne Widom14
Estimated H-index: 14
(Cornell University)
+ 2 AuthorsBrian R. Crane49
Estimated H-index: 49
(Cornell University)
HAMP domains are dimeric, four-helix bundles that transduce conformational signals in bacterial receptors. Genetic studies of the Escherichia coli serine receptor (Tsr) provide an opportunity to understand HAMP conformational behavior in terms of functional output. To increase its stability, the Tsr HAMP domain was spliced into a poly-HAMP unit from the Pseudomonas aeruginosa Aer2 receptor. Within the chimera, the Tsr HAMP undergoes a thermal melting transition at a temperature much lower than t...
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