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Frederick Heberle

Barbara Eicher, Drew Marquardt, Frederick A Heberle, Ilse Letofsky-Papst, Gerald N Rechberger, Marie-Sousai Appavou, John Katsaras, Georg Pabst
We measured the effect of intrinsic lipid curvature, J0, on structural properties of asymmetric vesicles made of palmitoyl-oleoyl-phosphatidylethanolamine (POPE; J0<0) and palmitoyl-oleoyl-phosphatidylcholine (POPC; J0∼0). Electron microscopy and dynamic light scattering were used to determine vesicle size and morphology, and x-ray and neutron scattering, combined with calorimetric experiments and solution NMR, yielded insights into leaflet-specific lipid packing and melting processes. Below the lipid melting temperature we observed strong interleaflet coupling in asymmetric vesicles with POPE inner bilayer leaflets and outer leaflets enriched in POPC...
January 9, 2018: Biophysical Journal
Milka Doktorova, Frederick A Heberle, Richard L Kingston, George Khelashvili, Michel A Cuendet, Yi Wen, John Katsaras, Gerald W Feigenson, Volker M Vogt, Robert A Dick
Binding of the retroviral structural protein Gag to the cellular plasma membrane is mediated by the protein's matrix (MA) domain. Prominent among MA-PM interactions is electrostatic attraction between the positively charged MA domain and the negatively charged plasma membrane inner leaflet. Previously, we reported that membrane association of HIV-1 Gag, as well as purified Rous sarcoma virus (RSV) MA and Gag, depends strongly on the presence of acidic lipids and is enhanced by cholesterol (Chol). The mechanism underlying this enhancement was unclear...
November 7, 2017: Biophysical Journal
Graham J Taylor, Frederick A Heberle, Jason S Seinfeld, John Katsaras, C Patrick Collier, Stephen A Sarles
In-plane lipid organization and phase separation in natural membranes play key roles in regulating many cellular processes. Highly cooperative, first-order phase transitions in model membranes consisting of few lipid components are well understood and readily detectable via calorimetry, densitometry, and fluorescence. However, far less is known about natural membranes containing numerous lipid species and high concentrations of cholesterol, for which thermotropic transitions are undetectable by the above-mentioned techniques...
September 5, 2017: Langmuir: the ACS Journal of Surfaces and Colloids
Frederick A Heberle, Georg Pabst
Biomimetic lipid vesicles are indispensable tools for gaining insight into the biophysics of cell physiology on the molecular level. The level of complexity of these model systems has steadily increased, and now spans from domain-forming lipid mixtures to asymmetric lipid bilayers. Here, we review recent progress in the development and application of elastic neutron and X-ray scattering techniques for studying these systems in situ and under physiologically relevant conditions on the nanometer to sub-nanometer length scales...
August 2017: Biophysical Reviews
Rebecca D Usery, Thais A Enoki, Sanjula P Wickramasinghe, Michael D Weiner, Wen-Chyan Tsai, Mary B Kim, Shu Wang, Thomas L Torng, David G Ackerman, Frederick A Heberle, John Katsaras, Gerald W Feigenson
To better understand animal cell plasma membranes, we studied simplified models, namely four-component lipid bilayer mixtures. Here we describe the domain size transition in the region of coexisting liquid-disordered (Ld) + liquid-ordered (Lo) phases. This transition occurs abruptly in composition space with domains increasing in size by two orders of magnitude, from tens of nanometers to microns. We measured the line tension between coexisting Ld and Lo domains close to the domain size transition for a variety of lipid mixtures, finding that in every case the transition occurs at a line tension of ∼0...
April 11, 2017: Biophysical Journal
Barbara Eicher, Frederick A Heberle, Drew Marquardt, Gerald N Rechberger, John Katsaras, Georg Pabst
Low- and high-resolution models describing the internal transbilayer structure of asymmetric lipid vesicles have been developed. These models can be used for the joint analysis of small-angle neutron and X-ray scattering data. The models describe the underlying scattering length density/electron density profiles either in terms of slabs or through the so-called scattering density profile, previously applied to symmetric lipid vesicles. Both models yield structural details of asymmetric membranes, such as the individual area per lipid, and the hydrocarbon thickness of the inner and outer bilayer leaflets...
April 1, 2017: Journal of Applied Crystallography
Drew Marquardt, Frederick A Heberle, Tatiana Miti, Barbara Eicher, Erwin London, John Katsaras, Georg Pabst
We measured the transbilayer diffusion of 1,2-dipalmitoyl-sn-glycero-3-phosphocholine (DPPC) in large unilamellar vesicles, in both the gel (Lβ') and fluid (Lα) phases. The choline resonance of headgroup-protiated DPPC exchanged into the outer leaflet of headgroup-deuterated DPPC-d13 vesicles was monitored using (1)H NMR spectroscopy, coupled with the addition of a paramagnetic shift reagent. This allowed us to distinguish between the inner and outer bilayer leaflet of DPPC, to determine the flip-flop rate as a function of temperature...
April 18, 2017: Langmuir: the ACS Journal of Surfaces and Colloids
Drew Marquardt, Frederick A Heberle, Denise V Greathouse, Roger E Koeppe, Robert F Standaert, Brad J Van Oosten, Thad A Harroun, Jacob J Kinnun, Justin A Williams, Stephen R Wassall, John Katsaras
Cholesterol is an essential biomolecule of animal cell membranes, and an important precursor for the biosynthesis of certain hormones and vitamins. It is also thought to play a key role in cell signaling processes associated with functional plasma membrane microdomains (domains enriched in cholesterol), commonly referred to as rafts. In all of these diverse biological phenomena, the transverse location of cholesterol in the membrane is almost certainly an important structural feature. Using a combination of neutron scattering and solid-state (2)H NMR, we have determined the location and orientation of cholesterol in phosphatidylcholine (PC) model membranes having fatty acids of different lengths and degrees of unsaturation...
November 1, 2016: Soft Matter
Yan Xia, Kamil Charubin, Drew Marquardt, Frederick A Heberle, John Katsaras, Jianhui Tian, Xiaolin Cheng, Ying Liu, Mu-Ping Nieh
Molecular transfer between nanoparticles has been considered to have important implications regarding nanoparticle stability. Recently, the interparticle spontaneous lipid transfer rate constant for discoidal bicelles was found to be very different from spherical, unilamellar vesicles (ULVs). Here, we investigate the mechanism responsible for this discrepancy. Analysis of the data indicates that lipid transfer is entropically favorable, but enthalpically unfavorable with an activation energy that is independent of bicelle size and long- to short-chain lipid molar ratio...
September 27, 2016: Langmuir: the ACS Journal of Surfaces and Colloids
Frederick A Heberle, Drew Marquardt, Milka Doktorova, Barbara Geier, Robert F Standaert, Peter Heftberger, Benjamin Kollmitzer, Jonathan D Nickels, Robert A Dick, Gerald W Feigenson, John Katsaras, Erwin London, Georg Pabst
Cell membranes possess a complex three-dimensional architecture, including nonrandom lipid lateral organization within the plane of a bilayer leaflet, and compositional asymmetry between the two leaflets. As a result, delineating the membrane structure-function relationship has been a highly challenging task. Even in simplified model systems, the interactions between bilayer leaflets are poorly understood, due in part to the difficulty of preparing asymmetric model membranes that are free from the effects of residual organic solvent or osmotic stress...
May 24, 2016: Langmuir: the ACS Journal of Surfaces and Colloids
Yan Xia, Ming Li, Kamil Charubin, Ying Liu, Frederick A Heberle, John Katsaras, Benxin Jing, Yingxi Zhu, Mu-Ping Nieh
We report on studies of lipid transfer rates between different morphology nanoparticles and lipids with different length acyl chains. The lipid transfer rate of dimyristoylphosphatidylcholine (di-C14, DMPC) in discoidal "bicelles" (0.156 h(-1)) is 2 orders of magnitude greater than that of DMPC vesicles (ULVs) (1.1 × 10(-3) h(-1)). For both bicellar and ULV morphologies, increasing the acyl chain length by two carbons [going from di-C14 DMPC to di-C16, dipalmitoylphosphatidylcholine (DPPC)] causes lipid transfer rates to decrease by more than 2 orders of magnitude...
December 1, 2015: Langmuir: the ACS Journal of Surfaces and Colloids
Norbert Kučerka, Brad van Oosten, Jianjun Pan, Frederick A Heberle, Thad A Harroun, John Katsaras
Following our previous efforts in determining the structures of commonly used PC, PG, and PS bilayers, we continue our studies of fully hydrated, fluid phase PE bilayers. The newly designed parsing scheme for PE bilayers was based on extensive MD simulations, and is utilized in the SDP analysis of both X-ray and neutron (contrast varied) scattering measurements. Obtained experimental scattering form factors are directly compared to our simulation results, and can serve as a benchmark for future developed force fields...
February 5, 2015: Journal of Physical Chemistry. B
Jianjun Pan, Drew Marquardt, Frederick A Heberle, Norbert Kučerka, John Katsaras
We recently published two papers detailing the structures of fluid phase phosphatidylglycerol (PG) lipid bilayers (Kučerka et al., 2012 J. Phys. Chem. B 116: 232-239; Pan et al., 2012 Biochim. Biophys. Acta Biomembr. 1818: 2135-2148), which were determined using the scattering density profile model. This hybrid experimental/computational technique utilizes molecular dynamics simulations to parse a lipid bilayer into components whose volume probabilities follow simple analytical functional forms. Given the appropriate scattering densities, these volume probabilities are then translated into neutron scattering length density (NSLD) and electron density (ED) profiles, which are used to jointly refine experimentally obtained small angle neutron and X-ray scattering data...
November 2014: Biochimica et Biophysica Acta
Jianjun Pan, Xiaolin Cheng, Luca Monticelli, Frederick A Heberle, Norbert Kučerka, D Peter Tieleman, John Katsaras
Phosphatidylserine (PS) lipids play essential roles in biological processes, including enzyme activation and apoptosis. We report on the molecular structure and atomic scale interactions of a fluid bilayer composed of 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphatidylserine (POPS). A scattering density profile model, aided by molecular dynamics (MD) simulations, was developed to jointly refine different contrast small-angle neutron and X-ray scattering data, which yielded a lipid area of 62.7 Å(2) at 25 °C. MD simulations with POPS lipid area constrained at different values were also performed using all-atom and aliphatic united-atom models...
June 7, 2014: Soft Matter
Peter Heftberger, Benjamin Kollmitzer, Frederick A Heberle, Jianjun Pan, Michael Rappolt, Heinz Amenitsch, Norbert Kučerka, John Katsaras, Georg Pabst
The highly successful scattering density profile (SDP) model, used to jointly analyze small-angle X-ray and neutron scattering data from unilamellar vesicles, has been adapted for use with data from fully hydrated, liquid crystalline multilamellar vesicles (MLVs). Using a genetic algorithm, this new method is capable of providing high-resolution structural information, as well as determining bilayer elastic bending fluctuations from standalone X-ray data. Structural parameters such as bilayer thickness and area per lipid were determined for a series of saturated and unsaturated lipids, as well as binary mixtures with cholesterol...
February 1, 2014: Journal of Applied Crystallography
Frederick A Heberle, Milka Doktorova, Shih Lin Goh, Robert F Standaert, John Katsaras, Gerald W Feigenson
Nanometer-scale domains in cholesterol-rich model membranes emulate lipid rafts in cell plasma membranes (PMs). The physicochemical mechanisms that maintain a finite, small domain size are, however, not well understood. A special role has been postulated for chain-asymmetric or hybrid lipids having a saturated sn-1 chain and an unsaturated sn-2 chain. Hybrid lipids generate nanodomains in some model membranes and are also abundant in the PM. It was proposed that they align in a preferred orientation at the boundary of ordered and disordered phases, lowering the interfacial energy and thus reducing domain size...
October 9, 2013: Journal of the American Chemical Society
Tatyana M Konyakhina, Jing Wu, James D Mastroianni, Frederick A Heberle, Gerald W Feigenson
We report the first 4-component phase diagram for the lipid bilayer mixture, DSPC/DOPC/POPC/chol (distearoylphosphatidylcholine/dioleoylphosphatidylcholine/1-palmitoyl, 2-oleoylphosphatidylcholine/cholesterol). This phase diagram, which has macroscopic Ld+Lo phase domains, clearly shows that all phase boundaries determined for the 3-component mixture containing DOPC transition smoothly into the boundaries for the 3-component mixture containing POPC, which has nanoscopic phase domains of Ld+Lo. Our studies start from two published ternary phase diagrams, and show how these can be combined into a quaternary phase diagram by study of a few hundred samples of intermediate compositions...
September 2013: Biochimica et Biophysica Acta
David G Ackerman, Frederick A Heberle, Gerald W Feigenson
The properties of lipid bilayer nanometer-scale domains could be crucial for understanding cell membranes. Fluorescent probes are often used to study bilayers, yet their effects on host lipids are not well understood. We used molecular dynamics simulations to investigate perturbations in a fluid DPPC bilayer upon incorporation of three indocarbocyanine probes: DiI-C18:0, DiI-C18:2, or DiI-C12:0. We find a 10-12% decrease in chain order for DPPC in the solvation shell nearest the probe but smaller effects in subsequent shells, indicating that the probes significantly alter only their local environment...
May 2, 2013: Journal of Physical Chemistry. B
Jianjun Pan, Frederick A Heberle, Robin S Petruzielo, John Katsaras
The cell plasma membrane is a complex system, which is thought to be capable of exhibiting non-random lateral organization. Studies of live cells and model membranes have yielded mechanisms responsible for the formation, growth, and maintenance of nanoscopic heterogeneities, although the existence and mechanisms that give rise to these heterogeneities remain controversial. Small-angle neutron scattering (SANS) is a tool ideally suited to interrogate lateral heterogeneity in model membranes, primarily due to its unique spatial resolution (i...
May 2013: Chemistry and Physics of Lipids
Frederick A Heberle, Robin S Petruzielo, Jianjun Pan, Paul Drazba, Norbert Kučerka, Robert F Standaert, Gerald W Feigenson, John Katsaras
The observation of lateral phase separation in lipid bilayers has received considerable attention, especially in connection to lipid raft phenomena in cells. It is widely accepted that rafts play a central role in cellular processes, notably signal transduction. While micrometer-sized domains are observed with some model membrane mixtures, rafts much smaller than 100 nm-beyond the reach of optical microscopy-are now thought to exist, both in vitro and in vivo. We have used small-angle neutron scattering, a probe free technique, to measure the size of nanoscopic membrane domains in unilamellar vesicles with unprecedented accuracy...
May 8, 2013: Journal of the American Chemical Society
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