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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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Membrane-mediated interactions yield the observed architecture of chemoreceptor lattices.Calculated elastic interaction energy per trimer, , in face-on honeycomb (blue), tip-on honeycomb (red), and hexagonal (black) lattices as a function of (A) center-to-center distance between neighboring trimers and (B) monolayer hydrophobic thickness and membrane tension (inset) at  nm (face-on honeycomb lattice; blue curve),  nm (hexagonal lattice; black curve), and  nm (tip-on honeycomb lattice; red curve), corresponding to the lattice spacings indicated by arrows in (A). The solid vertical line at  nm in (A) shows the trimer separation observed in face-on chemoreceptor lattices [19], [22], and dashed vertical lines in (A) indicate steric constraints on tip-on honeycomb (red) and hexagonal (black) lattice configurations. For (A) we assumed a membrane with  and a monolayer thickness  nm corresponding to the E. coli cytoplasmic membrane (shown by a dashed vertical line in (B)). For the main panel in (B) we set  and the curves in the inset were obtained with  nm. All lattice energies were calculated from pairwise nearest-neighbor interaction potentials as shown in Fig. 2.
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pcbi-1003932-g004: Membrane-mediated interactions yield the observed architecture of chemoreceptor lattices.Calculated elastic interaction energy per trimer, , in face-on honeycomb (blue), tip-on honeycomb (red), and hexagonal (black) lattices as a function of (A) center-to-center distance between neighboring trimers and (B) monolayer hydrophobic thickness and membrane tension (inset) at nm (face-on honeycomb lattice; blue curve), nm (hexagonal lattice; black curve), and nm (tip-on honeycomb lattice; red curve), corresponding to the lattice spacings indicated by arrows in (A). The solid vertical line at nm in (A) shows the trimer separation observed in face-on chemoreceptor lattices [19], [22], and dashed vertical lines in (A) indicate steric constraints on tip-on honeycomb (red) and hexagonal (black) lattice configurations. For (A) we assumed a membrane with and a monolayer thickness nm corresponding to the E. coli cytoplasmic membrane (shown by a dashed vertical line in (B)). For the main panel in (B) we set and the curves in the inset were obtained with nm. All lattice energies were calculated from pairwise nearest-neighbor interaction potentials as shown in Fig. 2.

Mentions: A simple arrangement of trimers in chemoreceptor lattices would be a close-packed hexagonal lattice structure (Fig. 4 grey insets, S4A Figure) in which each trimer has six nearest neighbors and, hence, the number of nearest-neighbor interactions is maximized. However, electron cryo-tomography has shown [19], [20] that chemoreceptor trimers are not closely packed in chemoreceptor lattices but rather form a honeycomb lattice in which each trimer has three nearest-neighbors arranged in the face-on orientation (Fig. 4 blue insets, S4B Figure), which allows formation of an extended lattice composed of chemoreceptor trimers, CheA, and CheW. To elucidate the stability of the observed face-on honeycomb-lattice architecture we calculated the energy per chemoreceptor trimer resulting from membrane-mediated interactions due to thickness deformations, , in face-on honeycomb, tip-on honeycomb (Fig. 4 red insets, S4C Figure), and hexagonal lattices. We find that, while tip-on honeycomb and hexagonal lattices can be energetically favorable for large lattice spacings, both these structures are unstable to the formation of a face-on honeycomb lattice with small lattice spacing, which provides the minimum-energy lattice architecture (Fig. 4A). This conclusion is robust with respect to variations in hydrophobic mismatch (Fig. 4B) and membrane tension (Fig. 4B inset). In contrast, cylindrical membrane inclusions, which do not exhibit directional interactions, would yield the hexagonal lattice as the minimum-energy structure. Thus, the directionality of membrane-mediated interactions stabilizes the observed face-on honeycomb lattice architecture against the tip-on honeycomb and hexagonal lattice structures. Specifically, the three-fold symmetry of trimers allows honeycomb ordering of chemoreceptor lattices, and thus further stabilization of a well-defined lattice constant through direct protein interactions with CheA and CheW [19], [20].


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

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

Membrane-mediated interactions yield the observed architecture of chemoreceptor lattices.Calculated elastic interaction energy per trimer, , in face-on honeycomb (blue), tip-on honeycomb (red), and hexagonal (black) lattices as a function of (A) center-to-center distance between neighboring trimers and (B) monolayer hydrophobic thickness and membrane tension (inset) at  nm (face-on honeycomb lattice; blue curve),  nm (hexagonal lattice; black curve), and  nm (tip-on honeycomb lattice; red curve), corresponding to the lattice spacings indicated by arrows in (A). The solid vertical line at  nm in (A) shows the trimer separation observed in face-on chemoreceptor lattices [19], [22], and dashed vertical lines in (A) indicate steric constraints on tip-on honeycomb (red) and hexagonal (black) lattice configurations. For (A) we assumed a membrane with  and a monolayer thickness  nm corresponding to the E. coli cytoplasmic membrane (shown by a dashed vertical line in (B)). For the main panel in (B) we set  and the curves in the inset were obtained with  nm. All lattice energies were calculated from pairwise nearest-neighbor interaction potentials as shown in Fig. 2.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4263354&req=5

pcbi-1003932-g004: Membrane-mediated interactions yield the observed architecture of chemoreceptor lattices.Calculated elastic interaction energy per trimer, , in face-on honeycomb (blue), tip-on honeycomb (red), and hexagonal (black) lattices as a function of (A) center-to-center distance between neighboring trimers and (B) monolayer hydrophobic thickness and membrane tension (inset) at nm (face-on honeycomb lattice; blue curve), nm (hexagonal lattice; black curve), and nm (tip-on honeycomb lattice; red curve), corresponding to the lattice spacings indicated by arrows in (A). The solid vertical line at nm in (A) shows the trimer separation observed in face-on chemoreceptor lattices [19], [22], and dashed vertical lines in (A) indicate steric constraints on tip-on honeycomb (red) and hexagonal (black) lattice configurations. For (A) we assumed a membrane with and a monolayer thickness nm corresponding to the E. coli cytoplasmic membrane (shown by a dashed vertical line in (B)). For the main panel in (B) we set and the curves in the inset were obtained with nm. All lattice energies were calculated from pairwise nearest-neighbor interaction potentials as shown in Fig. 2.
Mentions: A simple arrangement of trimers in chemoreceptor lattices would be a close-packed hexagonal lattice structure (Fig. 4 grey insets, S4A Figure) in which each trimer has six nearest neighbors and, hence, the number of nearest-neighbor interactions is maximized. However, electron cryo-tomography has shown [19], [20] that chemoreceptor trimers are not closely packed in chemoreceptor lattices but rather form a honeycomb lattice in which each trimer has three nearest-neighbors arranged in the face-on orientation (Fig. 4 blue insets, S4B Figure), which allows formation of an extended lattice composed of chemoreceptor trimers, CheA, and CheW. To elucidate the stability of the observed face-on honeycomb-lattice architecture we calculated the energy per chemoreceptor trimer resulting from membrane-mediated interactions due to thickness deformations, , in face-on honeycomb, tip-on honeycomb (Fig. 4 red insets, S4C Figure), and hexagonal lattices. We find that, while tip-on honeycomb and hexagonal lattices can be energetically favorable for large lattice spacings, both these structures are unstable to the formation of a face-on honeycomb lattice with small lattice spacing, which provides the minimum-energy lattice architecture (Fig. 4A). This conclusion is robust with respect to variations in hydrophobic mismatch (Fig. 4B) and membrane tension (Fig. 4B inset). In contrast, cylindrical membrane inclusions, which do not exhibit directional interactions, would yield the hexagonal lattice as the minimum-energy structure. Thus, the directionality of membrane-mediated interactions stabilizes the observed face-on honeycomb lattice architecture against the tip-on honeycomb and hexagonal lattice structures. Specifically, the three-fold symmetry of trimers allows honeycomb ordering of chemoreceptor lattices, and thus further stabilization of a well-defined lattice constant through direct protein interactions with CheA and CheW [19], [20].

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