From Biophysics to Biology

Springer Series in Biophysics 19 Richard M. Epand Jean-Marie Ruysschaert Editors The Biophysics of Cell Membranes Biological Consequences Springer Series in Biophysics Volume 19 Series editor Boris Martinac [email protected] More information about this series at http://www.springer.com/series/835 [email protected] Richard M. Epand • Jean-Marie Ruysschaert Editors The Biophysics of Cell Membranes Biological Consequences 123 [email protected] Editors Richard M. Epand Jean-Marie Ruysschaert Biochemistry and Biomedical Sciences Sciences Faculty McMaster University Université Libre de Bruxelles Hamilton, ON, Canada Bruxelles, Belgium ISSN 0932-2353 ISSN 1868-2561 (electronic) Springer Series in Biophysics ISBN 978-981-10-6243-8 ISBN 978-981-10-6244-5 (eBook) DOI 10.1007/978-981-10-6244-5 Library of Congress Control Number: 2017952612 © Springer Nature Singapore Pte Ltd. 2017 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Printed on acid-free paper This Springer imprint is published by Springer Nature The registered company is Springer Nature Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore [email protected] Preface Chapters in this volume discuss several aspects of the physical properties of biological membranes and how these properties influence their functioning. The reviews emphasize the mechanisms that result in these changes in membrane properties and function. One of the rapidly developing areas in membrane biophysics in recent years has been the role of transbilayer lipid asymmetry. It is known that the lipid composition of the bilayer of a biological membrane is very different for the two monolayers that compose this bilayer. Most studies of model membranes have employed membranes with identical composition for the two monolayers. There are technical difficulties in making model membranes with transbilayer asymmetry. Chapter 1 describes the methods that are being developed to facilitate the preparation of asymmetric model membranes and how the presence of this transbilayer lipid asymmetry affects the physical properties of the membrane. The maintenance of transbilayer lipid asymmetry is intimately connected with the rates of lipid flip-flop, i.e. the movement of lipid from one face of the bilayer to the opposite side. In model membranes devoid of protein, flip-flop rates of polar lipids are generally very slow. However, in biological membranes these rates can be accelerated by specific proteins, in some cases using an active transport mechanism, as well as through non-specific disordering of membrane packing compared with a pure lipid membrane. Chapter 2 discusses how the flipping rate is dependent on both the chemical structure of the lipid as well as on the physical state of the membrane. Results of studies of flip-flop rates obtained both from experiments as well as computer simulations are presented. The two principle components of biological membranes are proteins and lipids. The function of membrane proteins is modulated by lipids, both by binding to specific lipid binding sites on the protein as well as by modulating the general biophysical properties of the membrane. Some of these properties, including the formation of supercritical fluids as well as long range interactions involving curvature stress, curvature elasticity and hydrophobicity play key roles in the coupling of lipids and proteins. The mechanisms of this modulation of membrane protein function through coupling with the physical properties of the membrane v [email protected] vi Preface are reviewed in Chap. 3. Chapter 4 describes how mechano-sensitive channels can be gated by stretching of the bilayer(forces-from-lipids principle)and/or by the forces conveyed to the channel from the cytoskeleton/extracellular matrix(force- from filament). The final two Chapters deal with larger scale systems. Chapter 5 discusses mechanisms of changes in cell shape. The factors involved can include the cytoskeleton, membrane-bending proteins and membrane biophysical properties including a role for lipid domains in cell membranes. The final Chapter considers the liposome as a minimal cellular model that can be used to simulate diverse processes from the origin-of-life to a reconstituted biochemical pathway. The possibility of applying such systems for future biotechnological applications is also considered. This volume thus summarizes, from diverse points of view, the nature of membrane biophysical properties and how these properties impinge on the various functions of a biological membrane. Hamilton, ON, USA Richard M. Epand Bruxelles, Belgium Jean-Marie Ruysschaert [email protected] Contents 1 Preparation and Physical Properties of Asymmetric Model Membrane Vesicles .......................................................... 1 Johnna R. St. Clair, Qing Wang, Guangtao Li, and Erwin London 2 Spontaneous Lipid Flip-Flop in Membranes: A Still Unsettled Picture from Experiments and Simulations............................... 29 Maria Maddalena Sperotto and Alberta Ferrarini 3 Membrane Lipid-Protein Interactions .................................... 61 Michael F. Brown, Udeep Chawla, and Suchithranga M.D.C. Perera 4 Principles of Mechanosensing at the Membrane Interface.............. 85 Navid Bavi, Yury A. Nikolaev, Omid Bavi, Pietro Ridone, Adam D. Martinac, Yoshitaka Nakayama, Charles D. Cox, and Boris Martinac 5 Lipid Domains and Membrane (Re)Shaping: From Biophysics to Biology ..................................................................... 121 Catherine Léonard, David Alsteens, Andra C. Dumitru, Marie-Paule Mingeot-Leclercq, and Donatienne Tyteca 6 Minimal Cellular Models for Origins-of-Life Studies and Biotechnology................................................................. 177 Pasquale Stano vii [email protected] Chapter 1 Preparation and Physical Properties of Asymmetric Model Membrane Vesicles Johnna R. St. Clair, Qing Wang, Guangtao Li, and Erwin London Abstract Model biomembrane vesicles composed of lipids have been widely used to investigate the principles of membrane assembly and organization. A limitation of these vesicles has been that they do not mimic the transbilayer lipid asymmetry seen in many natural membranes, most notably the asymmetry in the plasma membrane of eukaryotic cells. Recently, a number of approaches have been developed to prepare asymmetric membranes and study their properties. This review describes methods to prepare asymmetric model membranes, and the physical properties of asymmetric lipid vesicles. Emphasis is placed on the vesicles prepared by cyclodextrin-catalyzed exchange, which has proven to be a versatile and powerful tool, including for studies manipulating lipid asymmetry in living cells. Keywords Membrane domains • Liquid ordered state • Sphingolipids • Phospholipids • Cyclodextrins 1.1 Lipid Asymmetry: Definition and Origin When studying biological membrane organization and function, one important aspect to consider is lipid asymmetry. Lipid asymmetry refers to the difference in lipid composition in the outer (exoplasmic, exofacial) leaflet vs. the inner (cytoplas- mic, cytofacial) leaflet of a membrane. Many cell membranes possess lipid asymmetry. In mammalian cells, the outer leaflet of the plasma membrane is enriched in sphingomyelin (SM), glycosphingolipids (GSL) and phosphatidylcholine (PC), while the inner leaflet is composed mainly of phosphatidylethanolamine (PE), and anionic lipids such as phosphatidylserine (PS) and phosphatidylinositol (PI) (Fig. 1.1)[1]. Cholesterol is present in both leaflets, but its distribution is still in dispute [2, 3]. J.R. St. Clair • Q. Wang • G. Li • E. London () Department of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, NY, 11794-5215, USA e-mail: [email protected] © Springer Nature Singapore Pte Ltd. 2017 1 R.M. Epand, J.-M. Ruysschaert (eds.), The Biophysics of Cell Membranes, Springer Series in Biophysics 19, DOI 10.1007/978-981-10-6244-5_1 [email protected] 2 J.R.St. Clair et al. Fig. 1.1 Representation of lipid asymmetry in natural biomembranes. In mammalian cells the outer, or exofacial, leaflet is enriched in saturated acyl-chain sphingomyelin and in phosphatidylcholine, while the inner, or cytofacial, leaflet is composed primarily

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