Structural and functional roles of non-bilayer lipid phases of chloroplast thylakoid membranes and mitochondrial inner membranes

Garab, Győző; Yaguzhinsky, L. S.; Dlouhý, Ondřej; Nesterov, Semen V.; Špunda, Vladimı́r; Gasanoff, Edward S.

doi:10.1016/j.plipres.2022.101163

Cited by 30 publications

(56 citation statements)

References 155 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…We would like to point out that the presently available data are in harmony with the DEM of TMs, according to which there is a dynamic exchange among the different lipid phases, whereby non-bilayer lipids may safe-guard the homeostasis of TMs and significantly contribute to their structural plasticity [ 21 ].…”

Section: Discussionmentioning

confidence: 99%

“…In fact, fully functional isolated intact TMs have been shown to contain non-bilayer lipid phases, as revealed via 31 P-NMR spectroscopy; the polymorphism of lipid phases has also been confirmed by time-resolved fluorescence spectroscopy using Merocyanine-540-stained TMs [ 17 , 18 , 19 ]. These features—the dominance of non-bilayer lipid species and the polymorphism of lipid phases—are not unique to TMs but also hold true for the other main energy-converting membrane, the inner mitochondrial membrane (IMM) [ 20 , 21 ].…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Structural Entities Associated with Different Lipid Phases of Plant Thylakoid Membranes—Selective Susceptibilities to Different Lipases and Proteases

Dlouhý

Karlický

Javornik

et al. 2022

Cells

Self Cite

View full text Add to dashboard Cite

It is well established that plant thylakoid membranes (TMs), in addition to a bilayer, contain two isotropic lipid phases and an inverted hexagonal (HII) phase. To elucidate the origin of non-bilayer lipid phases, we recorded the 31P-NMR spectra of isolated spinach plastoglobuli and TMs and tested their susceptibilities to lipases and proteases; the structural and functional characteristics of TMs were monitored using biophysical techniques and CN-PAGE. Phospholipase-A1 gradually destroyed all 31P-NMR-detectable lipid phases of isolated TMs, but the weak signal of isolated plastoglobuli was not affected. Parallel with the destabilization of their lamellar phase, TMs lost their impermeability; other effects, mainly on Photosystem-II, lagged behind the destruction of the original phases. Wheat-germ lipase selectively eliminated the isotropic phases but exerted little or no effect on the structural and functional parameters of TMs—indicating that the isotropic phases are located outside the protein-rich regions and might be involved in membrane fusion. Trypsin and Proteinase K selectively suppressed the HII phase—suggesting that a large fraction of TM lipids encapsulate stroma-side proteins or polypeptides. We conclude that—in line with the Dynamic Exchange Model—the non-bilayer lipid phases of TMs are found in subdomains separated from but interconnected with the bilayer accommodating the main components of the photosynthetic machinery.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Structural Entities Associated with Different Lipid Phases of Plant Thylakoid Membranes—Selective Susceptibilities to Different Lipases and Proteases

Dlouhý

Karlický

Javornik

et al. 2022

Cells

Self Cite

View full text Add to dashboard Cite

show abstract

“…The important role of non-bilayer structures in ATP production and in the maintenance of the structural integrity of IMM has been recently reported by us not only for mitochondria [ 30 , 34 , 49 ], but also in fully functional plant thylakoid membranes [ 49 ]. Non-bilayer structures are not only important in membrane fusion and the intermembrane exchange of lipids, which are essential processes in maintaining the functional dynamic architecture of the highly folded IMM [ 34 , 49 ], but they are also key elements in the formation of sub-compartments in the inter-cristae space near the ATP synthases, whereby they play an important role in enhancing the proton motive force and ATP synthase activity [ 30 , 34 , 49 ].…”

Section: Discussionmentioning

confidence: 99%

“…The presence of alcohols disturbs the surface of the PC membrane to create opportunities for an interaction of melittin’s R22 with the phosphate group of the PC, which facilitate melittin translocation through the membrane. Once the melittin reaches the surface of the IMM, it reacts with CL on the membrane surface to trigger a formation of intra-cristae bridges made of non-bilayer-organized CL molecules according to the mechanism described for CTs [ 22 , 30 , 34 ] and proposed for cyt c [ 49 ]. In the presence of alcohols, melittin can also react with the phosphate group of PC, which explains the involvement of PC in non-bilayer structure formation, as revealed here by 1 H-NMR spectroscopy.…”

Section: Discussionmentioning

confidence: 99%

Short-Chained Alcohols Make Membrane Surfaces Conducive for Melittin Action: Implication for the Physiological Role of Alcohols in Cells

Wang

Qin

Garab

et al. 2022

Cells

Self Cite

View full text Add to dashboard Cite

Alcohols are a part of cellular metabolism, but their physiological roles are not well understood. We investigated the effects of short-chain alcohols on Daphnia pulex and model membranes mimicking the lipid composition of eukaryotic inner mitochondrial membranes. We also studied the synergistic effects of alcohols with the bee venom membrane-active peptide, melittin, which is structurally similar to endogenous membrane-active peptides. The alcohols, from ethanol to octanol, gradually decreased the heart rate and the mitochondrial ATP synthesis of daphnia; in contrast, in combination with melittin, which exerted no sizeable effect, they gradually increased both the heart rate and the ATP synthesis. Lipid packing and the order parameter of oriented films, monitored by EPR spectroscopy of the spin-labeled probe 5-doxylstrearic acid, revealed gradual alcohol-assisted bilayer to non-bilayer transitions in the presence of melittin; further, while the alcohols decreased, in combination with melittin they increased the order parameter of the film, which is attributed to the alcohol-facilitated association of melittin with the membrane. A 1H-NMR spectroscopy of the liposomes confirmed the enhanced induction of a non-bilayer lipid phase that formed around the melittin, without the permeabilization of the liposomal membrane. Our data suggest that short-chain alcohols, in combination with endogenous peptides, regulate protein functions via modulating the lipid polymorphism of membranes.

show abstract

“…When CL in submitochondrial particles is damaged by reactive oxygen species (ROS), complexes I, III, and IV become dysfunctional, while the addition of CL restores their functions [ 52 , 53 , 54 ]. CL is also involved in the functioning of ATP synthase [ 50 , 55 ], nucleotide translocator [ 56 ], and is also necessary for the assembly and functioning of respirasomes [ 57 , 58 , 59 ]. Thus, the areas of high curvature of MIM, where the clusters of the OXPHOS system are located, are enriched in CL, which is involved in the operation of nearly all components of the OXPHOS system [ 60 ].…”

Section: Model Background and Formulationmentioning

confidence: 99%

Contribution of the Collective Excitations to the Coupled Proton and Energy Transport along Mitochondrial Cristae Membrane in Oxidative Phosphorylation System

Nesterov

Yaguzhinsky²,

Василов³

et al. 2022

Entropy

Self Cite

View full text Add to dashboard Cite

The results of many experimental and theoretical works indicate that after transport of protons across the mitochondrial inner membrane (MIM) in the oxidative phosphorylation (OXPHOS) system, they are retained on the membrane–water interface in nonequilibrium state with free energy excess due to low proton surface-to-bulk release. This well-established phenomenon suggests that proton trapping on the membrane interface ensures vectorial lateral transport of protons from proton pumps to ATP synthases (proton acceptors). Despite the key role of the proton transport in bioenergetics, the molecular mechanism of proton transfer in the OXPHOS system is not yet completely established. Here, we developed a dynamics model of long-range transport of energized protons along the MIM accompanied by collective excitation of localized waves propagating on the membrane surface. Our model is based on the new data on the macromolecular organization of the OXPHOS system showing the well-ordered structure of respirasomes and ATP synthases on the cristae membrane folds. We developed a two-component dynamics model of the proton transport considering two coupled subsystems: the ordered hydrogen bond (HB) chain of water molecules and lipid headgroups of MIM. We analytically obtained a two-component soliton solution in this model, which describes the motion of the proton kink, corresponding to successive proton hops in the HB chain, and coherent motion of a compression soliton in the chain of lipid headgroups. The local deformation in a soliton range facilitates proton jumps due to water molecules approaching each other in the HB chain. We suggested that the proton-conducting structures formed along the cristae membrane surface promote direct lateral proton transfer in the OXPHOS system. Collective excitations at the water–membrane interface in a form of two-component soliton ensure the coupled non-dissipative transport of charge carriers and elastic energy of MIM deformation to ATP synthases that may be utilized in ATP synthesis providing maximal efficiency in mitochondrial bioenergetics.

show abstract

Structural and functional roles of non-bilayer lipid phases of chloroplast thylakoid membranes and mitochondrial inner membranes

Cited by 30 publications

References 155 publications

Structural Entities Associated with Different Lipid Phases of Plant Thylakoid Membranes—Selective Susceptibilities to Different Lipases and Proteases

Structural Entities Associated with Different Lipid Phases of Plant Thylakoid Membranes—Selective Susceptibilities to Different Lipases and Proteases

Short-Chained Alcohols Make Membrane Surfaces Conducive for Melittin Action: Implication for the Physiological Role of Alcohols in Cells

Contribution of the Collective Excitations to the Coupled Proton and Energy Transport along Mitochondrial Cristae Membrane in Oxidative Phosphorylation System

Contact Info

Product

Resources

About