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Research Article

HAMP Domain Rotation and Tilting Movements Associated with Signal Transduction in the PhoQ Sensor Kinase

Susana Matamouros, Kyle R. Hager, Samuel I. Miller
John Mekalanos, Editor
Susana Matamouros
aDepartment of Microbiology, University of Washington, Seattle, Washington, USA
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Kyle R. Hager
aDepartment of Microbiology, University of Washington, Seattle, Washington, USA
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Samuel I. Miller
aDepartment of Microbiology, University of Washington, Seattle, Washington, USA
bDepartment of Genome Sciences, University of Washington, Seattle, Washington, USA
cDepartment of Medicine, University of Washington, Seattle, Washington, USA
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John Mekalanos
Harvard Medical School
Roles: Editor
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DOI: 10.1128/mBio.00616-15
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ABSTRACT

HAMP domains are α-helical coiled coils that often transduce signals from extracytoplasmic sensing domains to cytoplasmic domains. Limited structural information has resulted in hypotheses that specific HAMP helix movement changes downstream enzymatic activity. These hypotheses were tested by mutagenesis and cysteine cross-linking analysis of the PhoQ histidine kinase, essential for resistance to antimicrobial peptides in a variety of enteric pathogens. These results support a mechanistic model in which periplasmic signals which induce an activation state generate a rotational movement accompanied by a tilt in α-helix 1 which activates kinase activity. Biochemical data and a high-confidence model of the PhoQ cytoplasmic domain indicate a possible physical interaction of the HAMP domain with the catalytic domain as necessary for kinase repression. These results support a model of PhoQ activation in which changes in the periplasmic domain lead to conformational movements in the HAMP domain helices which disrupt interaction between the HAMP and the catalytic domains, thus promoting increased kinase activity.

IMPORTANCE Most studies on the HAMP domain signaling states have been performed with chemoreceptors or the HAMP domain of Af1503. Full-length structures of the HAMP-containing histidine kinases VicK and CpxA or a hybrid between the HAMP domain of Af1503 and the EnvZ histidine kinase agree with the parallel four-helix bundle structure identified in Af1503 and provide snapshots of structural conformations experienced by HAMP domains. We took advantage of the fact that we can easily regulate the activation state of PhoQ histidine kinase to study its HAMP domain in the context of the full-length protein in living cells and provide biochemical evidence for different conformational states experienced by Salmonella enterica serovar Typhimurium PhoQ HAMP domain upon signaling.

FOOTNOTES

    • Received 13 April 2015
    • Accepted 17 April 2015
    • Published 26 May 2015
  • Copyright © 2015 Matamouros et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

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HAMP Domain Rotation and Tilting Movements Associated with Signal Transduction in the PhoQ Sensor Kinase
Susana Matamouros, Kyle R. Hager, Samuel I. Miller
mBio May 2015, 6 (3) e00616-15; DOI: 10.1128/mBio.00616-15

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HAMP Domain Rotation and Tilting Movements Associated with Signal Transduction in the PhoQ Sensor Kinase
Susana Matamouros, Kyle R. Hager, Samuel I. Miller
mBio May 2015, 6 (3) e00616-15; DOI: 10.1128/mBio.00616-15
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