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EcoSal Plus

Domain 5:

Responding to the Environment

EnvZ/OmpR Two-Component Signaling: An Archetype System That Can Function Noncanonically

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • Authors: Linda J. Kenney1,2, and Ganesh S. Anand3
  • Editor: James M. Slauch4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Mechanobiology Institute, T-Lab, National University of Singapore, Singapore; 2: Department of Biochemistry & Molecular Biology, University of Texas Medical Branch, Galveston, TX 77555; 3: Department of Biological Sciences, National University of Singapore, Singapore; 4: The School of Molecular and Cellular Biology, University of Illinois at Urbana-Champaign, Urbana, IL
  • Received 05 January 2019 Accepted 02 December 2019 Published 30 January 2020
  • Address correspondence to Linda J. Kenney, [email protected]; Ganesh S. Anand, [email protected]
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  • Abstract:

    Two-component regulatory systems represent the major paradigm for signal transduction in prokaryotes. The simplest systems are composed of a sensor kinase and a response regulator. The sensor is often a membrane protein that senses a change in environmental conditions and is autophosphorylated by ATP on a histidine residue. The phosphoryl group is transferred onto an aspartate of the response regulator, which activates the regulator and alters its output, usually resulting in a change in gene expression. In this review, we present a historical view of the archetype EnvZ/OmpR two-component signaling system, and then we provide a new view of signaling based on our recent experiments. EnvZ responds to cytoplasmic signals that arise from changes in the extracellular milieu, and OmpR acts canonically (requiring phosphorylation) to regulate the porin genes and noncanonically (without phosphorylation) to activate the acid stress response. Herein, we describe how insights gleaned from stimulus recognition and response in EnvZ are relevant to nearly all sensor kinases and response regulators.

  • Citation: Kenney L, Anand G. 2020. EnvZ/OmpR Two-Component Signaling: An Archetype System That Can Function Noncanonically, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0001-2019

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/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0001-2019
2020-01-30
2020-11-24

Abstract:

Two-component regulatory systems represent the major paradigm for signal transduction in prokaryotes. The simplest systems are composed of a sensor kinase and a response regulator. The sensor is often a membrane protein that senses a change in environmental conditions and is autophosphorylated by ATP on a histidine residue. The phosphoryl group is transferred onto an aspartate of the response regulator, which activates the regulator and alters its output, usually resulting in a change in gene expression. In this review, we present a historical view of the archetype EnvZ/OmpR two-component signaling system, and then we provide a new view of signaling based on our recent experiments. EnvZ responds to cytoplasmic signals that arise from changes in the extracellular milieu, and OmpR acts canonically (requiring phosphorylation) to regulate the porin genes and noncanonically (without phosphorylation) to activate the acid stress response. Herein, we describe how insights gleaned from stimulus recognition and response in EnvZ are relevant to nearly all sensor kinases and response regulators.

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Figures

Image of Figure 1
Figure 1

At low osmolality and neutral pH, OmpF is the major porin in the outer membrane. At high osmolality, transcription is repressed and OmpC becomes the predominant porin. EnvZ autophosphorylation is stimulated by increasing osmolality, driving phosphotransfer to OmpR, dimerization, and high-affinity binding to DNA.

Citation: Kenney L, Anand G. 2020. EnvZ/OmpR Two-Component Signaling: An Archetype System That Can Function Noncanonically, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0001-2019
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Image of Figure 2
Figure 2

The periplasmic domain of an EnvZ dimer protrudes above the membrane, which is shown as a space-filling model (membrane from PDB ID: 3J00, EnvZ dimer frrom PDB: 4CTI) ( 190 ). The transmembrane domains (TMs) connect to the four-helix bundle formed from a dimer of two monomers (in purple and orange); a single His sidechain (phosphorylation site) is highlighted in red. The ATP binding domains flank His.

Citation: Kenney L, Anand G. 2020. EnvZ/OmpR Two-Component Signaling: An Archetype System That Can Function Noncanonically, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0001-2019
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Image of Figure 3
Figure 3

EnvZ binds ATP and is autophosphorylated at His. Phosphorylated EnvZ transfers the phosphoryl group to OmpR. OmpR∼P binds with higher affinity to the porin promoters and activates transcription. At high concentrations, EnvZ can catalyze OmpR∼P dephosphorylation.

Citation: Kenney L, Anand G. 2020. EnvZ/OmpR Two-Component Signaling: An Archetype System That Can Function Noncanonically, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0001-2019
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Image of Figure 4
Figure 4

Because the RR is in great molar excess compared to the HK, all of the HK would be complexed . ATP binds to the HK and autophosphorylates, driving phosphoryl transfer and dimerization of the complexed RR. The RR∼P is then stimulated to activate its downstream pathway, usually through enhanced DNA binding. The phosphorylated RR dimer can undergo dephosphorylation to then rebind to the HK.

Citation: Kenney L, Anand G. 2020. EnvZ/OmpR Two-Component Signaling: An Archetype System That Can Function Noncanonically, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0001-2019
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Image of Figure 5
Figure 5

Key residues that contribute to phosphorylation are highlighted. (B) Ribbon diagram of the NMR structure of the C-terminal domain of OmpR in one orientation (left) and rotated 90° (right) (reprinted with permission from reference 95 ).

Citation: Kenney L, Anand G. 2020. EnvZ/OmpR Two-Component Signaling: An Archetype System That Can Function Noncanonically, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0001-2019
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Image of Figure 6
Figure 6

OmpR is a two-domain protein; the N-terminal phosphorylation or receiver domain is joined to the C-terminal DNA binding effector domain via a flexible linker. (A) The protein is shown in the uncomplexed state (B) phosphorylated, (C) bound to DNA in the unphosphorylated state, and (D) bound to DNA while phosphorylated. The arrows depict transitions between these four states. Further complicating the scheme is the dimerization of OmpR (not depicted for simplicity). OmpR is a monomer in solution, and phosphorylation or interaction with EnvZ drives dimerization. In panels B, C, and D, the conformation of the linker is altered by phosphorylation, DNA binding, or both events.

Citation: Kenney L, Anand G. 2020. EnvZ/OmpR Two-Component Signaling: An Archetype System That Can Function Noncanonically, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0001-2019
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Figure 7

OmpR∼P binds as a dimer to sites located between –100 and –40 upstream of the transcription start site. The sites between –100 and –80 (F1 and C1) are the highest affinity for OmpR and OmpR∼P. Phosphorylation is required for occupancy of the lower-affinity sites F2-F3 and C2-C3. An additional site at (F4) is required for repression between –380 and –350, and repression is predicted to occur via loop formation assisted by the DNA bending protein IHF. Presumably, the loop then occludes and prevents RNA polymerase binding and subsequent activation of transcription, leading to repression.

Citation: Kenney L, Anand G. 2020. EnvZ/OmpR Two-Component Signaling: An Archetype System That Can Function Noncanonically, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0001-2019
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Image of Figure 8
Figure 8

High-resolution structures of the His neighborhood under conditions of low osmolality (by NMR PDB ID:1JOY) (A) and high osmolality (by X-ray crystallography PDB ID: 4KP4). (B) The osmolality-dependent conformational change is associated with helix stabilization across the four-helix bundle subdomain. (C) An inset shows the local disorder within the His-containing helix. The imidazole ring nitrogens (blue) are anchored by competing H-bonds with the Ala backbone carbonyl group and Asp side chain (red dashed lines) to maintain low basal levels of His phsophorylation. (D) Osmolality-induced helical backbone stabilization strengthens the backbone H-bond between the Ala carbonyl and aids in positioning the Asp side chain for enhanced His phosphorylation at Nε.

Citation: Kenney L, Anand G. 2020. EnvZ/OmpR Two-Component Signaling: An Archetype System That Can Function Noncanonically, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0001-2019
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Image of Figure 9
Figure 9

Evidence for DNA compaction is evident in panels in the third row, where the green outlines the nucleoid edges. OmpR was distributed around the nucleoid edges (outlined in green) in LB, whereas it was more uniformly distributed in Tris buffer. In acidic (MES, pH 5.6) and hypotonic (0.5× M9) conditions, OmpR was recruited to the plasma membrane (scale bar = 1 μm). The number of images used for averaging cell length was 19 cells length 3.75 to 4.25 μm (A), 20 cells length 2.0 to 2.5 μm (B), 15 cells length 1.75 to 2.25 μm (C), and 13 cells length 1.5 to 2.0 μm (D). Reprinted from reference 39 under the terms of the Creative Commons CC BY license.

Citation: Kenney L, Anand G. 2020. EnvZ/OmpR Two-Component Signaling: An Archetype System That Can Function Noncanonically, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0001-2019
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