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The role of membrane-mediated interactions in the assembly and architecture of chemoreceptor lattices.

Haselwandter CA, Wingreen NS - PLoS Comput. Biol. (2014)

Bottom Line: In common with other membrane proteins, chemoreceptor trimers are expected to deform the surrounding lipid bilayer, inducing membrane-mediated anisotropic interactions between neighboring trimers.Our model of bilayer-chemoreceptor interactions also helps to explain the observed dependence of chemotactic signaling on lipid bilayer properties.Finally, we consider the possibility that membrane-mediated interactions might contribute to cooperativity among neighboring chemoreceptor trimers.

View Article: PubMed Central - PubMed

Affiliation: Departments of Physics & Astronomy and Biological Sciences, University of Southern California, Los Angeles, California, United States of America.

ABSTRACT
In vivo fluorescence microscopy and electron cryo-tomography have revealed that chemoreceptors self-assemble into extended honeycomb lattices of chemoreceptor trimers with a well-defined relative orientation of trimers. The signaling response of the observed chemoreceptor lattices is remarkable for its extreme sensitivity, which relies crucially on cooperative interactions among chemoreceptor trimers. In common with other membrane proteins, chemoreceptor trimers are expected to deform the surrounding lipid bilayer, inducing membrane-mediated anisotropic interactions between neighboring trimers. Here we introduce a biophysical model of bilayer-chemoreceptor interactions, which allows us to quantify the role of membrane-mediated interactions in the assembly and architecture of chemoreceptor lattices. We find that, even in the absence of direct protein-protein interactions, membrane-mediated interactions can yield assembly of chemoreceptor lattices at very dilute trimer concentrations. The model correctly predicts the observed honeycomb architecture of chemoreceptor lattices as well as the observed relative orientation of chemoreceptor trimers, suggests a series of "gateway" states for chemoreceptor lattice assembly, and provides a simple mechanism for the localization of large chemoreceptor lattices to the cell poles. Our model of bilayer-chemoreceptor interactions also helps to explain the observed dependence of chemotactic signaling on lipid bilayer properties. Finally, we consider the possibility that membrane-mediated interactions might contribute to cooperativity among neighboring chemoreceptor trimers.

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Schematic of membrane-mediated interactions between chemoreceptor trimers.(A) If the hydrophobic thickness of the unperturbed lipid monolayer, , does not match the hydrophobic thickness of chemoreceptor trimers, , the lipid bilayer locally deforms in the vicinity of chemoreceptor trimers, yielding membrane-mediated interactions between trimers. (B) The three-fold symmetry of chemoreceptor trimers induces directionality of membrane-mediated interactions between trimers. The trimer configurations in the left and right panels correspond to tip-on and face-on orientations, respectively, with thickness deformations of the bilayer membrane in the vicinity of trimers illustrated by density maps (see S2 Figure for a three-dimensional illustration of thickness deformations). We denote by  the center-to-center distance between trimers. In our calculations, we used chemoreceptor trimers of the indicated perturbed cylindrical shape with width  nm.
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pcbi-1003932-g001: Schematic of membrane-mediated interactions between chemoreceptor trimers.(A) If the hydrophobic thickness of the unperturbed lipid monolayer, , does not match the hydrophobic thickness of chemoreceptor trimers, , the lipid bilayer locally deforms in the vicinity of chemoreceptor trimers, yielding membrane-mediated interactions between trimers. (B) The three-fold symmetry of chemoreceptor trimers induces directionality of membrane-mediated interactions between trimers. The trimer configurations in the left and right panels correspond to tip-on and face-on orientations, respectively, with thickness deformations of the bilayer membrane in the vicinity of trimers illustrated by density maps (see S2 Figure for a three-dimensional illustration of thickness deformations). We denote by the center-to-center distance between trimers. In our calculations, we used chemoreceptor trimers of the indicated perturbed cylindrical shape with width nm.

Mentions: In our analysis of membrane-mediated interactions between chemoreceptor trimers we follow the standard membrane-mechanical framework [31]–[33] for describing bilayer-protein interactions, and model chemoreceptor trimers as rigid membrane inclusions inducing elastic deformations in the surrounding lipid bilayer membrane. Such deformations can take the form of thickness deformations (Fig. 1A), which originate from a hydrophobic thickness mismatch between chemoreceptors and the lipid bilayer, and midplane (curvature) deformations (S1 Figure), which may be induced by a conical shape of chemoreceptor trimers resulting from a tilt in the transmembrane helices. To leading order, the elastic energies associated with thickness and midplane deformations decouple from each other, and can therefore be analyzed separately (see S1 Text section 1). We focus here on bilayer-chemoreceptor interactions and, hence, only consider the transmembrane regions of trimers in our model, with the peri- and cytoplasmic regions of trimers in Fig. 1A and S1 Figure only being shown for illustration.


The role of membrane-mediated interactions in the assembly and architecture of chemoreceptor lattices.

Haselwandter CA, Wingreen NS - PLoS Comput. Biol. (2014)

Schematic of membrane-mediated interactions between chemoreceptor trimers.(A) If the hydrophobic thickness of the unperturbed lipid monolayer, , does not match the hydrophobic thickness of chemoreceptor trimers, , the lipid bilayer locally deforms in the vicinity of chemoreceptor trimers, yielding membrane-mediated interactions between trimers. (B) The three-fold symmetry of chemoreceptor trimers induces directionality of membrane-mediated interactions between trimers. The trimer configurations in the left and right panels correspond to tip-on and face-on orientations, respectively, with thickness deformations of the bilayer membrane in the vicinity of trimers illustrated by density maps (see S2 Figure for a three-dimensional illustration of thickness deformations). We denote by  the center-to-center distance between trimers. In our calculations, we used chemoreceptor trimers of the indicated perturbed cylindrical shape with width  nm.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4263354&req=5

pcbi-1003932-g001: Schematic of membrane-mediated interactions between chemoreceptor trimers.(A) If the hydrophobic thickness of the unperturbed lipid monolayer, , does not match the hydrophobic thickness of chemoreceptor trimers, , the lipid bilayer locally deforms in the vicinity of chemoreceptor trimers, yielding membrane-mediated interactions between trimers. (B) The three-fold symmetry of chemoreceptor trimers induces directionality of membrane-mediated interactions between trimers. The trimer configurations in the left and right panels correspond to tip-on and face-on orientations, respectively, with thickness deformations of the bilayer membrane in the vicinity of trimers illustrated by density maps (see S2 Figure for a three-dimensional illustration of thickness deformations). We denote by the center-to-center distance between trimers. In our calculations, we used chemoreceptor trimers of the indicated perturbed cylindrical shape with width nm.
Mentions: In our analysis of membrane-mediated interactions between chemoreceptor trimers we follow the standard membrane-mechanical framework [31]–[33] for describing bilayer-protein interactions, and model chemoreceptor trimers as rigid membrane inclusions inducing elastic deformations in the surrounding lipid bilayer membrane. Such deformations can take the form of thickness deformations (Fig. 1A), which originate from a hydrophobic thickness mismatch between chemoreceptors and the lipid bilayer, and midplane (curvature) deformations (S1 Figure), which may be induced by a conical shape of chemoreceptor trimers resulting from a tilt in the transmembrane helices. To leading order, the elastic energies associated with thickness and midplane deformations decouple from each other, and can therefore be analyzed separately (see S1 Text section 1). We focus here on bilayer-chemoreceptor interactions and, hence, only consider the transmembrane regions of trimers in our model, with the peri- and cytoplasmic regions of trimers in Fig. 1A and S1 Figure only being shown for illustration.

Bottom Line: In common with other membrane proteins, chemoreceptor trimers are expected to deform the surrounding lipid bilayer, inducing membrane-mediated anisotropic interactions between neighboring trimers.Our model of bilayer-chemoreceptor interactions also helps to explain the observed dependence of chemotactic signaling on lipid bilayer properties.Finally, we consider the possibility that membrane-mediated interactions might contribute to cooperativity among neighboring chemoreceptor trimers.

View Article: PubMed Central - PubMed

Affiliation: Departments of Physics & Astronomy and Biological Sciences, University of Southern California, Los Angeles, California, United States of America.

ABSTRACT
In vivo fluorescence microscopy and electron cryo-tomography have revealed that chemoreceptors self-assemble into extended honeycomb lattices of chemoreceptor trimers with a well-defined relative orientation of trimers. The signaling response of the observed chemoreceptor lattices is remarkable for its extreme sensitivity, which relies crucially on cooperative interactions among chemoreceptor trimers. In common with other membrane proteins, chemoreceptor trimers are expected to deform the surrounding lipid bilayer, inducing membrane-mediated anisotropic interactions between neighboring trimers. Here we introduce a biophysical model of bilayer-chemoreceptor interactions, which allows us to quantify the role of membrane-mediated interactions in the assembly and architecture of chemoreceptor lattices. We find that, even in the absence of direct protein-protein interactions, membrane-mediated interactions can yield assembly of chemoreceptor lattices at very dilute trimer concentrations. The model correctly predicts the observed honeycomb architecture of chemoreceptor lattices as well as the observed relative orientation of chemoreceptor trimers, suggests a series of "gateway" states for chemoreceptor lattice assembly, and provides a simple mechanism for the localization of large chemoreceptor lattices to the cell poles. Our model of bilayer-chemoreceptor interactions also helps to explain the observed dependence of chemotactic signaling on lipid bilayer properties. Finally, we consider the possibility that membrane-mediated interactions might contribute to cooperativity among neighboring chemoreceptor trimers.

Show MeSH
Related in: MedlinePlus