Molecular Convergence of Bacterial and Eukaryotic Surface Order

Kaiser, Hermann Josef; Surma, Michał A.; Mayer, Florian; Levental, Ilya; Grzybek, Michał; Klemm, Robin W.; Cruz, Sandrine Da; Meisinger, Chris; Müller, Volker; Simons, Kai; Lingwood, Daniel

doi:10.1074/jbc.m111.276444

Cited by 51 publications

(42 citation statements)

References 49 publications

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“…1B), suggesting a mechanistic connection. However, these synthetic liposomes are limited models for live cell membranes, most importantly because they lack cholesterol and integral membrane proteins, which make up a major fraction of surface area in biological membranes and contribute dramatically to their stabilities (56). However, the quantitative agreement between the onset concentration of both maximal cell injury (Fig.…”

Section: Discussionmentioning

confidence: 99%

Bile Acids Modulate Signaling by Functional Perturbation of Plasma Membrane Domains

Zhou

Maxwell

Sezgin

et al. 2013

Journal of Biological Chemistry

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101

112

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Background: Bile acids (BAs) affect cellular membranes. Results: BAs stabilize domains in plasma membranes, leading to reorganization of membrane proteins and signaling perturbations. Conclusion: BAs affect cell function by modulating the stability of plasma membrane nanodomains. Significance: These results suggest mechanisms for regulation of functional membrane domains and nonreceptor-mediated BA signaling.

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Section: Discussionmentioning

confidence: 99%

Bile Acids Modulate Signaling by Functional Perturbation of Plasma Membrane Domains

Zhou

Maxwell

Sezgin

et al. 2013

Journal of Biological Chemistry

Self Cite

101

112

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“…However, the biological signifi cance of the hydroxylation remains unclear. In S. cerevisiae , complex sphingolipids corresponding living cells could prevent the membrane from packing ( 32,42 ). The amount of immobile molecules markedly increased in the sur2 ⌬ csg1 ⌬ csh1 ⌬ mutant with the decrease in ergosterol content containing the P13 fraction ( Fig.…”

Section: Discussionmentioning

confidence: 99%

Loss of hydroxyl groups from the ceramide moiety can modify the lateral diffusion of membrane proteins in S. cerevisiae

Uemura

Shishido

Tani

et al. 2014

Journal of Lipid Research

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“…Evidence for lipid-dependent functional domains has been reported for Bacillus subtilis (29), and there is evidence for lateral membrane heterogeneity in Gloeobacter violaceus (30), a hopanoid-producing cyanobacterium. Interestingly, it has been suggested that the averaged order of eukaryotic plasma membranes and bacterial inner membranes lacking hopanoids converge (31). These studies imply that bacteria that lack hopanoids may use alternate mechanisms for achieving lateral heterogeneity and modulating membrane order.…”

Section: Cholesterol and Diplopterol Modulate The Order And Phase Behmentioning

confidence: 99%

Functional convergence of hopanoids and sterols in membrane ordering

Sáenz

Sezgin

Schwille

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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164

136

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Liquid-ordered phases are one of two biochemically active membrane states, which until now were thought to be a unique consequence of the interactions between eukaryotic membrane lipids. The formation of a liquid-ordered phase depends crucially on the ordering properties of sterols. However, it is not known whether this capacity exists in organisms that lack sterols, such as bacteria. We show that diplopterol, the simplest bacterial hopanoid, has similar properties and that hopanoids are bacterial "sterol surrogates" with the ability to order saturated lipids and to form a liquid-ordered phase in model membranes. These observations suggest that the evolution of an ordered biochemically active liquid membrane could have evolved before the oxygenation of Earth's surface and the emergence of sterols.lipid order | polycyclic isoprenoids | bacterial membrane organization | membrane phase evolution | organic geochemistry T he capacity for sterols to modulate the ordering of lipids forms the basis for a membrane organizing principle in eukaryotes (1). The emergence of sterol-like ordering was likely a critical step in the evolution of biological membranes, allowing cells to control fluidity without compromising membrane integrity and providing a means to compartmentalize membranes into functional domains (2-4). It is not known, however, to what extent such membrane-ordering properties span the domains of life. Prokaryotes generally lack sterols; however, some bacteria produce hopanoids (5, 6), which are structurally similar (Fig. 1A) (7), and their cyclization is catalyzed by related enzymes (8). These similarities inspired the hypothesis that hopanoids are bacterial sterol surrogates (9) and led us to examine whether hopanoids might share the properties of sterols in membranes. Results and DiscussionEffects of Cholesterol and Diplopterol on the Phase Behavior and Ordering of Sphingomyelin in Model Membranes. Sterols and sphingolipids are closely associated in eukaryotic membranes, and the nature of their interactions has been extensively characterized. Therefore, we chose to test whether diplopterol behaves similarly to cholesterol in this well-defined system. Sterols interact with sphingolipids in vitro to form a liquid-ordered (L o ) phase that represents a thermodynamic intermediate between liquid-disordered (L d ) and crystalline gel phases (Fig. 1B) (10). The interactions leading to the formation of a L o phase derive from the ability of sterols to simultaneously inhibit the formation of the gel phase (by intercalating between sphingolipids and preventing their crystallization) and to order saturated acyl chains. To test whether these properties are also exhibited by hopanoids, we examined the effect of diplopterol on N-stearoyl-D-erythro-sphingosylphosphorylcholine (SM; Fig. S1), a synthetic sphingolipid.Monolayer experiments provide an approach to study the gelliquid phase transition of SM. Lipids are spread out over an airwater interface to form a monolayer and lateral pressure (measured as surface tension) is...

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Molecular Convergence of Bacterial and Eukaryotic Surface Order

Cited by 51 publications

References 49 publications

Bile Acids Modulate Signaling by Functional Perturbation of Plasma Membrane Domains

Bile Acids Modulate Signaling by Functional Perturbation of Plasma Membrane Domains

Loss of hydroxyl groups from the ceramide moiety can modify the lateral diffusion of membrane proteins in S. cerevisiae

Functional convergence of hopanoids and sterols in membrane ordering

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