Thomas Huber

Laboratory of Molecular Biology and Biochemistry
Rockefeller Research Building 510

The Rockefeller University, Box 187
1230 York Avenue
New York, NY 10065

Telephone: 212-327-8284
Fax: 212-327-7904
hubert@rockefeller.edu

Biosketch

Education:

Postdoc, Rockefeller University, 2002
Postdoc, University of Arizona, 2002
Postdoc, University of Munich, 2000
Ph.D. in Medicine (Dr. med.), University of Munich , 1999
M.D. (Ärztliche Prüfung), University of Munich, 1995

Teaching Experience
1996–2000 Seminar within the program of preclinical education for medical students covering the entire field of Medical Biochemistry (72 hrs per year), Institute for Physiological Chemistry, University of Munich

Professional membership
Biophysical Society, Bethesda, MD.

Patent application/pending
Rockefeller University, New York, NY
RU 870
A Novel Method for the Production of Nanoscale Membrane Particles
Technology Summary
Inventors
Dr. Thomas Sakmar, Dr. Thomas Huber, and Sourabh Banerjee
Patent Information & References
· Patent pending
· Banerjee, et al. 2008. J. Mol. Biol. DOI: 10.1016/j.jmb.2008.01.066

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Research:

The goal of my research is to elucidate the biophysical principles of molecular recognition in biomembranes with a special emphasis on transmembrane receptors and their native lipid environment. Despite enormous advances, there are still gaps in scientific understanding of the fundamental processes of molecular biology, such as protein folding, genetic encoding of biomolecular function, and highly selective molecular recognition {Ball, 2006}. In order to address some of these fundamental issues, my strategy is an interdisciplinary approach combining experimental and computational techniques. Keys to this approach are 1) to apply the quantitative measurement process of physical sciences to biochemistry, molecular biology, and pharmacology, and 2) to interpret the molecular mechanism by computer simulations of dynamic models. Currently, my research focuses on the role of the phospholipid membrane in ligand-receptor and protein-protein interactions. The first project addresses the question of how a hydrophobic ligand, 11-cis-retinal, finds its way via the lipid membrane into the buried binding pocket of a seven-transmembrane (7-TM) helix receptor, opsin, a prototypical G-protein-coupled receptor (GPCR). The second project addresses the effect of hydrophobic mismatch on the self-assembly process of receptors in membrane microdomains and resulting changes in receptor function. In the near future, my plan is to miniaturize the experiments employing ultra-sensitive fluorescence microscopy in combination with microfluidics techniques. These nanoscale experiments will enable me, on the one hand, to work with receptors that are difficult to be produced in large quantities and, on the other hand, to switch from ensemble to single molecule measurements. Ideally, the single molecule techniques might reveal completely new mechanistic insight. In a second line of development, I plan to make a stronger connection of the current in vitro approach using reconstituted pure components to in vivo model systems using live cell culture in combination with similar fluorescence microscopy techniques.

Azido labels enable FTIR analysis of rhodopsin activation.

Although recent advances have provided several high-resolution crystal structures of protein-coupled receptors (GPCR), understanding the detailed structural changes upon activation of a GPCR remains paramount. We demonstrate the site-specific incorporation of an infra red (IR)-active unnatural amino acid (UAAM) into the GPCR rhodopsin. We used Fourier transform infra red (FTIR) difference spectroscopy to monitor these amino acids and show specific environmental changes during receptor activation. The conformational changes were consistent with the changes observed in a recent crystal structure, a ligand-free version of rhodopsin. Our long-term goal is to combine an array of experimental and computational biophysical tools to provide a comprehensive model of the activation mechanism of GPCRs. The Sakmar Lab performed the FTIR spectroscopy in collaboration with the Vogel lab at the Albert-Ludwigs-University Freiburg, Germany.

Structural Basis for Ligand Binding and Specificity in Adrenergic Receptors: Implications for GPCR-targeted Drug Discovery.

The crystal structures of beta-2 adrenergic receptors were one of the scientific breakthroughs in 2007. It was the first G protein-coupled receptor (GPCR) with a diffusible ligand, (nor-) epinephrine or adrenaline. In this work, we applied some of the molecular dynamics simulation methodology developed earlier for studies of rhodopsin to this new receptor structure. We were comparing simulations of a "beta-blocker" drug bound receptor with simulations containing the activating hormone adrenaline. Together these simulations exceeded 600 nanoseconds, which render this study computationally as one of the largest simulations in the literature up to that point. These extensive simulations were supported by the National Science Foundation (NSF) that provided generous supercomputing time on the Teragrid nationwide network of massive parallel computer clusters. Huber and Sakmar are corresponding authors on this paper. Huber serves as the principal investigator of this NSF grant.

Site-specific incorporation of keto amino acids into functional G protein-coupled receptors using unnatural amino acid mutagenesis.

In all living organisms, genetic material (DNA or RNA) is translated into proteins. The genetic code defines a mapping between nucleotide triplets, called codons, and amino acids. Nature utilizes this code to assemble all proteins from only twenty different amino acids, which are the building blocks of proteins. In this work building on results from the Schultz group at Scripps, we have developed a system for unnatural amino acids mutagenesis of proteins in mammalian cell culture, in particular of the two G protein-coupled receptors (GPCRs), visual rhodopsin and CCR5 chemokine receptor. We were able to introduce the unnatural amino acid at an arbitrary, but specific position in the protein. We demonstrated that the receptors were functional, and that the unnatural amino acid could be modified by specific chemical reactions to introduce informative biophysical probes, for example, fluorescence labels. This work was a collaboration of the Sakmar lab and the RajBhandary lab at the Massachusetts Institute of Technology (MIT), Cambridge, MA.

Functional role of the "ionic lock"—an interhelical hydrogen-bond network in family A heptahelical receptors.

The crystal structure of visual rhodopsin from the Palczewski group in 2000 has provided an unprecedented view into the atomic interactions in this prototypical G protein-coupled receptor (GPCR). One of the intriguing observations was the presence of a so called "ionic lock" that appears to keep the receptor in the off state. Here we investigated a series of site-directed mutants of rhodopsin using Fourier transform infra red (FTIR) difference spectroscopy. We were able to quantify the effect of the ionic lock on the on-off equilibrium of the receptor, consistent with the hypothesis. Interestingly, in the recently elucidated structure of beta-2 adrenergic receptor, the ionic lock is broken, and at the same time the off state of this receptor appears to be destabilized. This work was part of a long standing collaboration of the Siebert lab at the Albert-Ludwigs-University Freiburg, Germany, and the Sakmar lab.

Bilateral olfactory sensory input enhances chemotaxis behavior.

The olfactory system utilizes G protein-coupled receptors (GPCRs) to detect odorants. These receptors are called odorant receptors. Animals are able to use the olfactory system for chemotaxis. Chemotaxis involves direct navigation toward attractive chemicals and away from aversive chemicals. In order to be able to study the processing of olfactory data in the central nervous system (CNS), we chose a simple model organism that can be genetically manipulated; the fruit fly Drosophila melanogaster, and more specifically their larval state. We developed new spectroscopic methods to create stable odorant gradients in which odor concentrations were experimentally measured by Fourier transform infrared spectroscopy (FTIR). Using high-resolution behavioral analysis, we demonstrated that sensory input from both sides of the head increases the overall accuracy of navigation. This study was a collaboration between the Sakmar and Vosshall labs at the Rockefeller University.

Rapid incorporation of functional rhodopsin into nanoscale apolipoprotein bound bilayer (NABB) particles.

It is generally accepted that several G protein-coupled receptors (GPCRs) are dimeric proteins, which require dimerization for proper functionality. However, for the majority of GPCRs the situation is not that clear, and it is matter of intense debate, whether the functional unit of the visual photoreceptor rhodopsin is a monomer or a dimer. In this paper, we addressed this problem and developed novel nanoscale apolipoprotein bound bilayer (NABB) particles to study rhodopsin monomers and dimers with a controlled stoichiometry. The receptor in these NABB particles retains its exceptional stability against thermal denaturation, which renders these particles substantially better than detergent micelles used traditionally for isolated receptors. Moreover, we used single-particle electron microscopy techniques to visualize the relative orientation of the rhodopsin dimers in these NABBs. We concluded that neither the dimer is required nor particularly active compared to the monomer of rhodopsin, which consequently seems to be the functional unit.

G Protein-Coupled Receptors Self-Assemble in Dynamics Simulations of Model Bilayers.

The self-assembly process of membrane proteins in biomembranes has important implications for the structure and function of macromolecular complexes involved, for example, in signal transduction systems. It is possible to follow the self-assembly process by spectroscopic methods, such as fluorescence resonance energy transfer (FRET) experiments, which result in some sort of order parameter that allows quantitative comparison of related systems observed under similar conditions. These "wet" or "test tube" experiments do not provide detailed information on how the different molecules are interacting with each other to result in the observed phenomena. In order to overcome this fundamental problem, we started collaborating with Dr. Xavier Periole in the Marrink lab in Groningen, The Netherlands. They had developed a novel molecular dynamics simulation technique, called coarse-grained molecular dynamics (CGMD) that allows modeling of large assemblies of dozens of membrane proteins in membranes containing thousands of lipids. In this paper, we report the results of a larger set of simulations with different lipids, each several microseconds long. The results are in overall agreement with our experimental studies of these systems. The corresponding authors of this paper are Periole and Huber, who established this transatlantic collaboration, during which they met several times in either Groningen or New York, respectively.

Curvature and Hydrophobic Forces Drive Oligomerization and Modulate Activity of Rhodopsin in Membranes.

Biomembranes are complex structures with different membrane proteins embedded in a lipid matrix, frequently described by a fluid mosaic model. Many membrane proteins have the intrinsic propensity to self-assemble into dimeric pairs or higher-order structures. However, for a large number of membrane proteins, it is difficult to pinpoint their behavior in the sense that they would have a strict tendency to stay monomeric, that is, without assembling into higher-order structures, or to form dimers or larger oligomers. Visual rhodopsin is such a case. While some authors have reported that it forms rows of dimers in the native membranes with the dimers as the functional unit for signaling, others have rejected this position in favor of a strictly monomeric protein. In this study, our aim was to determine the role of the membrane bilayer in the process of self-assembly of rhodopsin. We used fluorescence resonance energy transfer (FRET) experiments to monitor rhodopsin self-assembly in membranes of controlled composition, and we were using UV-Vis spectroscopy to probe the ability of rhodopsin to form the active state in these membranes. Consistent with a hydrophobic mismatch mechanism, we found that lipid bilayers with a thickness different from the hydrophobic lenght of rhodopsin induce self-assembly of the receptors into dimers or higher-order oligomers. The unexpected result was that these receptor clusters appear to block activation of the receptors. This work was performed as a collaborative project between the Brown lab at the University of Arizona, Tucson, and the Sakmar lab at the Rockefeller University, New York. Botelho and Huber share the first authorship.

Membrane model for the GPCR rhodopsin: hydrophobic interface and dynamical structure.

The crystal structure of visual rhodopsin from the Palczewski group in the year 2000 was a hallmark event in structural biology. Rhodopsin is the light receptor in the rod cells of the retina in the back of the eyes. Rhodopsin is a transmembrane protein, which is embedded in membranes that are rich in lipids containing the omega-3 polyunsaturated fatty acid, docosahexaenoic acid (DHA). The specific aim of this study was to characterize the interfaces of rhodopsin that are in contact with the membrane lipids and with water, respectively. It should be noted that the dynamical nature of biological membranes makes the structure of lipids and the protein-lipid interface inaccessible to standard techniques of structural biology, which rely on single, static conformations. Our approach of combining solid-state deuterium NMR experiments with computational molecular dynamics simulations, which we applied successfully to at least one other system (see reference 7), are the state-of-the-art method to investigate these receptors in a native-like biomembrane model. The paper describes a detailed analysis of the system, and we found some remarkable movements of some regions of the receptor once released from the "straight-jacket" of the densely packed crystalline environment. This paper is based on my research originally started in the Beyer lab at the University of Munich and mainly performed during my stay in the Brown lab at the University of Arizona, Tucson, AZ, first as postdoctoral fellow and later as a visiting scientist.

Structure of docosahexaenoic acid-containing phospholipid bilayers as studied by 2H NMR and molecular dynamics simulations.

Polyunsaturated fatty acids are essential nutrients for humans, which imply that they are similar to vitamines that need to be provided with the diet. There are two classes, omega-6 and omega-3, depending on the position of the first unsaturation or double bond in the acyl chain. Docosahexaenoic acid (DHA) is the most important omega-3 fatty acid, especially concentrated in fish oil. Deficiency has been linked to retinal and neural development, learning, neurological dysfunction including Alzheimer's disease, Parkinson's disease, Zellweger's syndrome, and schizophrenia, and diseases including atherosclerosis and cancer. Despite this large number of associated medical conditions, the molecule mechanism of action for DHA is largely unknown. One possible hypothesis is that lipids carrying DHA chains have unique physicochemical properties that modulate the material properties of the membranes they are most highly concentrated in, such as synaptosomal membranes in the brain or the retinal photoreceptor rod cells. In order to obtain insight into the chemical basis that governs these material properties, we developed a new force field to perform computer simulations of model membranes, comparing DHA with more regular monounsaturated fatty acyl chains. In addition to these computer simulations, we were studying the same systems using solid-state deuterium NMR experiments. It should be noted that the results of our study were published back-to-back with a competing study, and both were the first computational studies applying molecular dynamics (MD) simulations of DHA containing bilayer membranes. This paper covers several years of work performed in the Beyer lab at the University of Munich and the Brown lab at the University of Arizona, Tucson, AZ.

A solid-state NMR study of phospholipid-cholesterol interactions: sphingomyelin-cholesterol binary systems.

Cholesterol is an essential building block of animal cells, including those in the human body. However, excessively high levels of cholesterol are associated with coronary heart disease, atherosclerosis, cerebrovascular disease, and an increased risk for heart attack and stroke. Understanding the physiology and pathophysiology of cholesterol is one of the most important research topics today. In this study, our aims are to understand the interactions in the molecular complex of cholesterol and sphingomyelin, which is a characteristic complex that makes up so called "lipid rafts", and to determine the critical saturation limit for cholesterol before microscopic crystals form, which is thought to occur as a consequence of hypercholesterinemia . Lipid rafts are thought to be self-organizing microdomains in the plasma membrane of cells, which enable efficient organization of functional systems, for example, the macromolecular complexes used for signal transduction of hormonal signals. This study employs various solid-state NMR techniques including the novel method to prepare oriented membranes with defined water content (see paper 5). This study was a collaboration of the Klaus Beyer lab at the University of Munich and the James A Hamilton lab at Boston University.

A 2H NMR study of macroscopically aligned bilayer membranes containing interfacial hydroxyl residues.

Energy-conserving biological membranes (biomembranes) are fundamentally important in living organisms. The inner membrane of mitochondria is one of those membranes. Mitochondria (as outlined above for paper 1) are sometimes called the "cellular power plants". This function is intimately connected to the properties of the energy conserving biomembranes, that is, their ability to maintain concentration gradients for protons and other metabolites. In this study, we applied solid-state nuclear magnetic resonance (NMR) spectroscopy to investigate the properties of hydroxyl residues on phospholipids and cholesterol. Especially the hydroxyl residues of the acidic phospholipids phosphatidylglycerol and cardiolipin might be involved in lateral proton conducting "wires" that connect the different units of the energy conversion mechanism of the mitochondria; the Fo/F1-ATPase and the respiratory chain complexes, which together form a proton circuit that converts one form of chemical energy into another. For this study, we developed a novel method to prepare oriented membranes with defined water content. This method was subsequently used in several other studies. We found that these hydroxyl residues were unusually stable, and we attributed this stability to reduced water accessibility to those groups. In summary, these results are consistent with a special environment of these hydroxyl residues that could support their role as proton conducting wires along the surface of mitochondria, and other energy conserving biomembranes, such as those in chloroplasts and bacterial inner membranes.

Mixed micelle formation between gramicidin-S and a nonionic detergent: a nuclear magnetic resonance model study of peptide/detergent aggregation.

Gramicidin-S is an unusual peptide antibiotic that is currently not used in medicine. However, due to the increased resistance seen for classical antibiotics, as for example MRSA (Methicillin-resistant Staphylococcus aureus) and other multi drug resistant bacteria, research on other types of antibiotics (such as gramicidin-S) becomes more important. Here we tried to investigate the mechanism of how the antibiotic binds to nonionic detergent micelles, which can be seen as very simple models of the bacterial cell membranes. Nuclear magnetic resonance (NMR) spectroscopy experiments revealed changes in the acid and base catalysis of the hydrogen to deuterium exchange reaction of the peptide bonds, as well as changes in the proton and carbon-13 spin-lattice relaxation rates. Together these data indicate that upon binding the flexible ring structure of the cyclic peptide becomes more stable and the anchors to the oily core of the micelle with the valine, leucine, and d-phenylalanine side chains.

Contribution of copper binding to the inhibition of lipid oxidation by plasmalogen phospholipids.

Several vitamines, such as A, C, and E, are protecting the cells from the detrimental effects of oxidative damage. Especially susceptible to this damage are many lipids in biological membranes. Here we investigated the role of copper in some detailed mechanism of lipid damage, utilizing nuclear magnetic resonance (NMR) spectroscopy and biochemical assays. The study was performed in collaboration with the laboratory of Engelmann, and we have developed the NMR spectroscopy analytical methods employed.

Investigation of the microscopic structure of a biological membrane; numerical model calculations as a methodological extension of physical experiments.

A biological membrane is an enclosing layer that acts as a barrier within or around a cell. It is composed of a double layer of lipids and proteins. Such membranes typically define enclosed spaces or compartments in which cells may maintain a chemical or biochemical environment that differs from the outside. Biological membranes are of fundamental importance in all forms of life we know of. Despite this paramount importance, it is difficult to render a detailed picture of the structure of such a membrane, since it is liquid and highly dynamic. We have built a simulation system utilizing extensive supercomputer calculations providing an unprecedented microscopic view into a 'virtual reality' of biological membranes. In this way we were able to interpret and understand physical experiments.

Binding of nucleotides by the mitochondrial ADP/ATP carrier as studied by 1H nuclear magnetic resonance spectroscopy.

In cell biology, mitochondria are membrane-enclosed organelle found in most eukaryotic cells, i.e., in cells from fungi, plants, and animals including humans. Mitochondria are sometimes described as "cellular power plants" because they generate most of the cell's supply of adenosine triphosphate (ATP), used as a source of chemical energy. ATP may be viewed as a "charged battery", and ADP is its discharged counterpart. The recycling process that recharges ATP from ADP involves selective transport of ADP and ATP across the membranes of mitochondria. In this study we have shown how a so-called carrier protein provides a selectivity filter, excluding other similar compounds from interfering with the recharging process. The studies involved computational quantum mechanics calculations, and nuclear magnetic resonance (NMR) spectroscopy, a technique related to the medical diagnostic method of magnetic resonance imaging (MRI).

Previous high-performance computing projects.

Large-scale biomembrane simulations with NAMD2 at the Pittsburgh Supercomputing Center (PSC), Carnegie Mellon University, University of Pittsburgh, Pittsburgh, PA, at the National Center for Supercomputing Applications, Champaign, IL, and at other sites participating in the TeraGrid project of the National Science Foundation.
Migration of an IBM/SP-2 project to home-build LINUX clusters using MPICH and LAM with CHARMM and Charm with NAMD2. Development of parallel molecular dynamics code for AMBER: shared memory on SNI/KSR-1 for version 4.0, and TCGMSG message passing on SPARC workstation cluster for version 4.1. Performance optimization of MPI message passing routines in the PME code of AMBER 4.1 on an IBM/SP-2. Local adaptation of GAMESS-US to SP-2.

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Awards:

National Science Foundation's Partnerships for Advanced Computational Infrastructure (NFS PACI) Medium Resource Allocation Committee (MRAC) Renewal grant MCB060033 Huber (PI) 2008-2009
"Ligand binding mechanism in the visual photoreceptor opsin, a G-protein-coupled receptor (GPCR)"
The long-term goal of our research is to provide comprehensive understanding of ligand recognition in seven-transmembrane (7-TM) helical G-protein coupled receptors (GPCRs). The determination of the first high resolution structure of a GPCR, the visual photoreceptor rhodopsin, in the year 2000 was a hallmark that enabled us to study GPCRs by molecular dynamics (MD) simulations. We built models of receptors in a native-like phospholipid bilayer environment. These all-atom models contain typically about 50,000 atoms, and can be routinely simulated on a sub-microsecond timescale using massive parallel processing (MPP) architectures on the TeraGrid, such as the PSC BigBen Cray XT3. Along with biochemical and biophysical experiments to map the thermodynamics of ligand binding in rhodopsin, this research aims at formulating methods to study the mechanism of ligand binding and recognition for GPCRs in general. In contrast to computational 'alchemy' studies to determine the absolute free energy of ligand binding, we utilize in a conceptual framework that focuses on thermally accessible ligand binding pathways and the role of receptor conformational changes in gating the ligand access. In the past year, publication of a series of high resolution crystal structures of additional GPCRs led to dramatic advances in the field. The new structures include β2-adrenergic receptor, squid rhodopsin, and most recently, opsin, the ligand-free form of bovine rhodopsin. Due to the importance of the β2-adrenergic receptor structure, we used the majority of the 300,000 service units (SUs) of from the previous application period to simulate several models of β2-adrenergic receptor with the inverse agonist carazolol and the natural agonist epinephrine (adrenaline) for more than 600 nanoseconds simulation time in total. Here we apply for TeraGrid Wide Roaming Access with 500,000 SUs in order to continue the studies on 11-cis-retinal binding to opsin, which we would like to supplement with comparative studies on ligand binding in β2-adrenergic receptor. The computational resources will be used for conventional MD simulations to study the equilibrium dynamics of several receptor structures, as well as for biased MD simulations to probe the free energy landscape of the ligand binding pathway.
Role: PI

Completed Research Support

National Science Foundation's Partnerships for Advanced Computational Infrastructure (NFS PACI) Medium Resource Allocation Committee (MRAC) Renewal grant MCB060033 Huber (PI) 2007-2008
"Ligand binding mechanism in the visual photoreceptor opsin, a G-protein-coupled receptor (GPCR)"
Role: PI
NFS PACI Medium Resource Allocation Committee (MRAC) grant MCB060033 Huber (PI) 2006-2007
"Ligand binding mechanism in the visual photoreceptor opsin, a G-protein-coupled receptor (GPCR)"
Role: PI
NSF PACI Development grant MCB020015P Huber (PI) 2002-2003
"Dynamics of phospholipids in G protein-coupled receptor containing membranes"
Role: PI
NSF PACI Development grant MCB020017N Huber (PI) 2002-2003
"Molecular dynamics simulations of a Biomembrane model comprising the G protein-coupled receptor rhodopsin in a polyunsaturated lipid bilayer membrane"
Role: PI
NSF PACI Alliance Allocations Board (AAB) grant MCB020034 Huber (PI) 2002-2003
"Rhodopsinthe single quantum detector and its unique environment"
Role: PI

NFS PACI Alliance Allocations Board (AAB) grant MCB030026 Huber (PI) 2003-2005
"Biomembrane models of G protein-coupled receptor signaling"
Role: PI

Published Papers:

PMID: 18313692 [PubMed - indexed for MEDLINE]

1).
Huber, T., M. Klingenberg, and K. Beyer.
Binding of nucleotides by the mitochondrial ADP/ATP carrier as studied by 1H nuclear magnetic resonance spectroscopy.
Biochemistry, 1999, 38:762-769

PMID: 9888816 [PubMed - indexed for MEDLINE]

Recent Presentations:

Invited Talks
Principles of molecular recognition in biomembranes. 2007. Department of Chemistry, City College of CUNY, New York, NY.

Thermodynamic analysis of the ligand binding pathway in the seven-transmembrane (7-TM) receptor rhodopsin. 2007. Biophysical Society Annual Meeting, Baltimore, MD.

Functional consequences of seven-transmembrane receptor association in bilayers. 2007. Biophysical Society Annual Meeting, Baltimore, MD.

Curvature and Hydrophobic Mismatch Drive Non-Ideal Mixing and Activation of Rhodopsin in Membranes. 2006. Biophysical Society Annual Meeting, Salt Lake City, UT.

Closing the visual cycle–exit and entry of retinal in opsin. 2006. Biophysical Society Annual Meeting, Salt Lake City, UT.

Visual Photoreceptor Membranes, New Challenges from a Classical System. 2004. Groningen Biomolecular Sciences and Biotechnology Institute (GBB), University of Groningen, Groningen, The Netherlands.

The hydrophobic interface of the GPCR prototype rhodopsin. 2002. Laboratory of Molecular Biology and Biochemistry, Rockefeller University, New York, NY.

Critical evaluation of influences of membrane lipid properties on rhodopsin function. 2002. Biophysical Society Annual Meeting, San Francisco, CA.

Mixed micelle formation between gramicidin-S and a nonionic detergent. 1997. Annual Meeting of the Sonderforschungsbereich 266, Schloß Ringberg Tagungsstätte der Max-Planck-Gesellschaft, Tegernsee, Germany.

Numerical simulations of a bilayer lipid membrane. 1996. Department of Chemistry, Penn State University, University Park, PA.

2000 Biophysical Society 44th Annual Meeting in New Orleans, LA
2001 Biophysical Society 45th Annual Meeting in Boston, MA
2002 Biophysical Society 46th Annual Meeting in San Francisco, CA
2003 Biophysical Society 47th Annual Meeting in San Antonio, TX
2004 Biophysical Society 48th Annual Meeting in Baltimore, MD
2005 Biophysical Society 49th Annual Meeting in Long Beach, CA
2006 Biophysical Society 50th Annual Meeting in Salt Lake City, UT
2007 Biophysical Society 51st Annual Meeting in Baltimore, MD
2008 Biophysical Society 52nd Annual Meeting in Long Beach, CA
2009 Biophysical Society 53rd Annual Meeting in Boston, MA

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Posters:

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