Lateral stress relaxation and collapse in lipid monolayers

Pocivavsek, Luka; Frey, Shelli L.; Krishan, Kapilanjan; Gavrilov, Kseniya; Ruchala, Piotr; Waring, Alan J.; Walther, Frans J.; Dennin, Michael; Witten, Thomas A.; Lee, Ka Yee C.

doi:10.1039/b804611e

Cited by 65 publications

(88 citation statements)

References 51 publications

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“…At high surface pressures, a high surface viscosity coupled with an elastic response may slow the kinetics of 3D buckling that occurs on monolayer collapse, wherein jerking motions may reflect overcoming the elastic response (32)(33)(34). Understanding the effects of cholesterol will enable these ideas to be tested by providing a simple way to alter monolayer mechanical properties by orders of magnitude with only subtle changes in lung surfactant composition and pressure-area isotherms.…”

Section: Discussionmentioning

confidence: 99%

Effect of cholesterol nanodomains on monolayer morphology and dynamics

Kim

Choi

Zell

et al. 2013

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

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At low mole fractions, cholesterol segregates into 10-to 100-nmdiameter nanodomains dispersed throughout primarily dipalmitoylphosphatidylcholine (DPPC) domains in mixed DPPC:cholesterol monolayers. The nanodomains consist of 6:1 DPPC:cholesterol "complexes" that decorate and lengthen DPPC domain boundaries, consistent with a reduced line tension, λ. The surface viscosity of the monolayer, η s , decreases exponentially with the area fraction of the nanodomains at fixed surface pressure over the 0.1-to 10-Hz range of frequencies common to respiration. At fixed cholesterol fraction, the surface viscosity increases exponentially with surface pressure in similar ways for all cholesterol fractions. This increase can be explained with a free-area model that relates η s to the pure DPPC monolayer compressibility and collapse pressure. The elastic modulus, G′, initially decreases with cholesterol fraction, consistent with the decrease in λ expected from the line-active nanodomains, in analogy to 3D emulsions. However, increasing cholesterol further causes a sharp increase in G′ between 4 and 5 mol% cholesterol owing to an evolution in the domain morphology, so that the monolayer is elastic rather than viscous over 0.1-10 Hz. Understanding the effects of small mole fractions of cholesterol should help resolve the controversial role cholesterol plays in human lung surfactants and may give clues as to how cholesterol influences raft formation in cell membranes.surface rheology | isotherms | free-volume model | AFM M inute fractions of cholesterol lead to dramatic changes in dipalmitoylphosphatidylcholine (DPPC) monolayer morphology (Figs. 1-3) (1, 2) and have equally dramatic effects on monolayer dynamic properties. One weight percent cholesterol reduces the surface viscosity, η s , of DPPC monolayers by an order of magnitude, and 2 wt% reduces η s by two orders of magnitude . Atomic force microscopy (AFM) images and microrheological data show that the cholesterol is segregated to lineactive, locally disordered nanodomains that are dispersed in and separate ordered, primarily DPPC domains. As a result, the monolayer retains many of the features of pure DPPC monolayers including a high collapse pressure, high compressibility, and so on, while having significantly lower surface viscosity. This surface viscosity effect suggests a role for cholesterol in lung surfactant (LS), a lipid-protein monolayer necessary to reduce the surface tension in the lung alveoli during respiration (Fig. S1) (3, 4). At present, even the existence of cholesterol in native LS is questioned, because the lung lavage required to harvest LS inevitably causes blood and cell debris to be coextracted, potentially contaminating LS with cholesterol (5). This lack of consensus over the role of cholesterol is reflected in the composition of replacement lung surfactants for neonatal respiratory distress syndrome (NRDS), which occurs in 20,000-30,000 premature births each year (6). Survanta and Curosurf, two clinically approved animalextract replacement surfact...

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Section: Discussionmentioning

confidence: 99%

Effect of cholesterol nanodomains on monolayer morphology and dynamics

Kim

Choi

Zell

et al. 2013

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

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“…Our theory and experiment both show a disordered hexagonal arrangement of the trilayer areas. This type of pattern may be present on other films that collapse repeatedly into multilayers and are sufficiently influenced by thermal fluctuations, such as in biological (12,13) or Langmuir films (14,15). It should be noted that these patterns may not be visually discernable.…”

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confidence: 97%

Incommensurate phases of a supported nanoparticle film subjected to uniaxial compression

Chua¹,

Leahy²,

Zhang³

et al. 2012

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

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We investigate experimentally and theoretically the sequence of phases that occurs when a self-assembled monolayer of gold nanoparticles supported on a fluid is compressed uniaxially in a Langmuir trough. Uniaxial compression of the monolayer results in the appearance of lines that have been shown to be regions of trilayer. These lines exhibit complex patterns that depend on the extent of compression. We show that these patterns can be understood in terms of an equilibrium statistical mechanical theory, originally developed in the context of commensurate-incommensurate transitions in krypton monolayers adsorbed on graphite, in which there is an energy cost to line deformations and to line intersections. Even though line intersections are energetically costly, they lower the free energy because they cause the entropy of the system to increase when the density of lines is low enough. Our analytic and Monte Carlo analyses of the model demonstrate that the model exhibits two-phase coexistence. Our experimental observations are qualitatively consistent with the predictions of the model.

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“…While the corresponding FM images (data not shown) of the pure lipid monolayer at the same pressure show large, round condensed domains embedded in a bright liquid expanded matrix, the deposited monolayer shows a considerable amount of condensed lipid in the bright, fluid region. The effect of these nanoscale condensed domains on the membrane's material properties has been discussed in a previous paper (50).…”

Section: L338 Importance Of Sp-b Nh2-terminal Insertion Sequencementioning

confidence: 99%

Functional importance of the NH₂-terminal insertion sequence of lung surfactant protein B

Frey

Pocivavsek

Waring

et al. 2010

American Journal of Physiology-Lung Cellular and Molecular Phys

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Lung surfactant protein B (SP-B) is required for proper surface activity of pulmonary surfactant. In model lung surfactant lipid systems composed of saturated and unsaturated lipids, the unsaturated lipids are removed from the film at high compression. It is thought that SP-B helps anchor these lipids closely to the monolayer in three-dimensional cylindrical structures termed "nanosilos" seen by atomic force microscopy imaging of deposited monolayers at high surface pressures. Here we explore the role of the SP-B NH2 terminus in the formation and stability of these cylindrical structures, specifically the distribution of lipid stack height, width, and density with four SP-B truncation peptides: SP-B 1-25, SP-B 9 -25, SP-B 11-25, and SP-B 1-25Nflex (prolines 2 and 4 substituted with alanine). The first nine amino acids, termed the insertion sequence and the interface seeking tryptophan residue 9, are shown to stabilize the formation of nanosilos while an increase in the insertion sequence flexibility (SP-B 1-25Nflex) may improve peptide functionality. This provides a functional understanding of the insertion sequence beyond anchoring the protein to the two-dimensional membrane lining the lung, as it also stabilizes formation of nanosilos, creating reversible repositories for fluid lipids at high compression. In lavaged, surfactant-deficient rats, instillation of a mixture of SP-B 1-25 (as a monomer or dimer) and synthetic lung lavage lipids quickly improved oxygenation and dynamic compliance, whereas SP-B 11-25 surfactants showed oxygenation and dynamic compliance values similar to that of lipids alone, demonstrating a positive correlation between formation of stable, but reversible, nanosilos and in vivo efficacy.

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Lateral stress relaxation and collapse in lipid monolayers

Cited by 65 publications

References 51 publications

Effect of cholesterol nanodomains on monolayer morphology and dynamics

Effect of cholesterol nanodomains on monolayer morphology and dynamics

Incommensurate phases of a supported nanoparticle film subjected to uniaxial compression

Functional importance of the NH₂-terminal insertion sequence of lung surfactant protein B

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Lateral stress relaxation and collapse in lipid monolayers

Cited by 65 publications

References 51 publications

Effect of cholesterol nanodomains on monolayer morphology and dynamics

Effect of cholesterol nanodomains on monolayer morphology and dynamics

Incommensurate phases of a supported nanoparticle film subjected to uniaxial compression

Functional importance of the NH2-terminal insertion sequence of lung surfactant protein B

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Functional importance of the NH₂-terminal insertion sequence of lung surfactant protein B