Thermal migration of molecular lipid films as a contactless fabrication strategy for lipid nanotube networks

Gözen, İrep; Shaali, Mehrnaz; Ainla, Alar; Ortmen, Bahanur; Põldsalu, Inga; Kustanovich, Kiryl; Jeffries, Gavin D. M.; Konkoli, Zoran; Dommersnes, Paul; Jesorka, Aldo

doi:10.1039/c3lc50391g

Cited by 13 publications

(16 citation statements)

References 26 publications

(26 reference statements)

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“…In a previous study, the transformation of a Y-junction to a small vesicle, due to chemical chelator-induced depinning of Ca 2+ , has been already shown 23 . In the current study, the Ca 2+ de-pinning and reversal of membrane adhesion is not caused by chelators, but is due to the temperature increase 9 . The compartments are also observed exclusively at junction points (Fig.…”

Section: Discussionmentioning

confidence: 49%

Rapid growth and fusion of protocells in surface-adhered membrane networks

Köksal

Liese

Xue

et al. 2020

Preprint

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Elevated temperatures might have promoted the nucleation, growth and replication of protocells on the early Earth. Recent reports have shown evidence that moderately high temperatures not only permit protocell assembly at the origin of life, but could have actively supported it. Here we show the fast nucleation and growth of vesicular compartments from autonomously formed lipid networks on solid surfaces, induced by a moderate increase in temperature. Branches of the networks, initially consisting of self-assembled interconnected nanotubes, rapidly swell into microcompartments which can spontaneously encapsulate RNA fragments. The increase in temperature further causes fusion of adjacent networkconnected compartments, resulting in the redistribution of the RNA. The experimental observations and the mathematical model indicate that the presence of nanotubular interconnections between protocells facilitates the fusion process.The important role of solid surface support for the autonomous formation of primitive protocells has been suggested earlier in the context of the origin of life 1,2 . Hanczyc, Szostak et al. showed that vesicle formation from fatty acids was significantly enhanced in the presence of solid particle surfaces consisting of natural minerals or synthetic materials 1,2 . Particularly the silicate-based minerals accelerated the vesicle generation.In a recent report, we showed the autonomous formation and growth of surface adhered protocell populations as a result of a sequence of topological transformations on a solid substrate 3 . Briefly, upon contact with a mineral-like solid substrate, a lipid reservoir spreads as a double bilayer membrane. The distal membrane (upper -with respect to the surface-) ruptures and forms a carpet of lipid nanotubes. Over the course of a few hours, fragments of these nanotubes swell into giant, strictly unilamellar vesicular compartments. This relatively slow process is entirely self-driven and only requires a lipid reservoir as source, a solid surface, and surrounding aqueous media. The resulting structure consists of thousands of lipid compartments, which are physically connected to each other via a

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Section: Discussionmentioning

confidence: 49%

Rapid growth and fusion of protocells in surface-adhered membrane networks

Köksal

Liese

Xue

et al. 2020

Preprint

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“…LCHFs accommodate temperatures between 40 and 90 °C, which could have promoted the formation of prebiotic membrane compartments 43 . In our study, temperature increase weakens membrane-surface adhesion and causes immediate surface de-wetting 17 , facilitating the subcompartment formation. Furthermore, it causes the membrane fluidity to increase, and enhances fusion 44,45 .…”

Section: Temperature-enhanced Formationmentioning

confidence: 57%

“…Temperature has a strong influence on membrane viscosity and membrane-surface adhesion 17 . When the temperature was locally increased from 20 °C (room temperature) to 40 °C, the basal membrane started to de-wet the surface, forming subcompartments twice as rapidly.…”

Section: Temperature-enhanced Subcompartmentalizationmentioning

confidence: 99%

Subcompartmentalization and pseudo-division of model protocells

Spustová

Köksal

Ainla

et al. 2020

Preprint

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Membrane enclosed intracellular compartments have been exclusively associated with the eukaryotes, represented by the highly compartmentalized last eukaryotic common ancestor. Recent evidence showing the presence of membranous compartments with specific functions in archaea and bacteria makes it conceivable that the last universal common ancestor and its hypothetical precursor, the protocell, could have exhibited compartmentalization. To our knowledge, there are no experimental studies yet that have tested this hypothesis. We report on an autonomous subcompartmentalization mechanism for protocells which results in the transformation of initial subcompartments to daughter protocells. The process is solely determined by the fundamental materials properties and interfacial events, and do not require biological machinery or chemical energy supply. In the light of our findings, we propose that similar events could have taken place under early Earth conditions, leading to the development of compartmentalized cells and potentially, primitive division.The origin of the eukaryotic cell is closely associated with the development of subcompartments, which create specific micro-environments to spatially or temporally regulate biochemical reactions, simultaneously. Until recently, cellular compartmentalization was associated solely with eukaryotic systems. Recent evidence shows that membrane-enclosed compartments also exist in other domains of life, such as in Archaea and Bacteria 1,2 . Archaea, for example, have acidocalcisomes, the membrane enclosed electron-dense granular organelles rich in calcium and phosphate, which is crucial for osmoregulation and calcium homeostasis 3 . In Cyanobacteria, membrane-bound thylakoids 4 , have been identified as compartments in which the light-dependent reactions of photosynthesis take place.Despite the differences between eukaryotic and prokaryotic compartments in terms of structural and functional complexity, the presence of membranous compartments in Procaryota 1 establishes a possibility of compartments having existed in protocells, and being evolutionarily conserved. There is essentially no experimental material, however, on how compartments could have consistently emerged from membranes in a prebiotic environment lacking membrane-shaping and -stabilizing proteins.Membrane-less laboratory models of cytoplasmic suborganization have been developed inside synthetic cells, i.e. giant unilamellar vesicles 5 . These models require moderately elaborate chemical systems. A few examples of the utilized materials and mechanisms to induce compartment formation involve thermo-responsive hydrogels 6 , pH driven protein (human serum albumin) localization 7 or a poly(ethylene glycol)-dextran aqueous two-phase system 8 . One study which report on the membrane-based multi-vesiculation inside amphiphilic compartments, has employed protein-ligand couples to induce this behavior, i.e. biotin-avidin conjugates 9 . Membrane-enveloped subcompartment formation in biological systems is therefore considered t...

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“…Similar to the processes observed in biological cells, reshaping of GUVs can occur in response to external stimuli. For example, GUV shrinkage, budding, or formation of tubular extensions can result from changes in osmolarity or temperature, or through exposure to oligonucleotides, nanoparticles or proteins such as BAR domains or clathrin [2][3][4][5][6][7][8] . To adequately mimic cell processes, it is of utmost importance that cell model systems include key molecular components that would be present in a living cell.…”

Section: Generation Of Interconnected Vesicles In a Liposomal Cell Modelmentioning

confidence: 99%

Generation of interconnected vesicles in a liposomal cell model

Doosti

Fjällborg

Kustanovich

et al. 2020

Sci Rep

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We introduce an experimental method based upon a glass micropipette microinjection technique for generating a multitude of interconnected vesicles (IVs) in the interior of a single giant unilamellar phospholipid vesicle (GUV) serving as a cell model system. The GUV membrane, consisting of a mixture of soybean polar lipid extract and anionic phosphatidylserine, is adhered to a multilamellar lipid vesicle that functions as a lipid reservoir. Continuous IV formation was achieved by bringing a micropipette in direct contact with the outer GUV surface and subjecting it to a localized stream of a Ca2+ solution from the micropipette tip. IVs are rapidly and sequentially generated and inserted into the GUV interior and encapsulate portions of the micropipette fluid content. The IVs remain connected to the GUV membrane and are interlinked by short lipid nanotubes and resemble beads on a string. The vesicle chain-growth from the GUV membrane is maintained for as long as there is the supply of membrane material and Ca2+ solution, and the size of the individual IVs is controlled by the diameter of the micropipette tip. We also demonstrate that the IVs can be co-loaded with high concentrations of neurotransmitter and protein molecules and displaying a steep calcium ion concentration gradient across the membrane. These characteristics are analogous to native secretory vesicles and could, therefore, serve as a model system for studying secretory mechanisms in biological systems.

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Thermal migration of molecular lipid films as a contactless fabrication strategy for lipid nanotube networks

Cited by 13 publications

References 26 publications

Rapid growth and fusion of protocells in surface-adhered membrane networks

Rapid growth and fusion of protocells in surface-adhered membrane networks

Subcompartmentalization and pseudo-division of model protocells

Generation of interconnected vesicles in a liposomal cell model

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