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Fluid Mosaic Model of the Structure of Cell Membranes Author(S): S The Fluid Mosaic Model of the Structure of Cell Membranes Author(s): S. J. Singer and Garth L. Nicolson Source: Science, New Series, Vol. 175, No. 4023 (Feb. 18, 1972), pp. 720-731 Published by: American Association for the Advancement of Science Stable URL: http://www.jstor.org/stable/1733071 Accessed: 12/09/2008 12:57 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=aaas. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We work with the scholarly community to preserve their work and the materials they rely upon, and to build a common research platform that promotes the discovery and use of these resources. For more information about JSTOR, please contact [email protected]. American Association for the Advancement of Science is collaborating with JSTOR to digitize, preserve and extend access to Science. http://www.jstor.org experimental evidence in terms of the model; and (v) to show that the fluid mosaic model suggests new ways of The Fluid Mosaic Model of the thinkingabout membranefunctions and membrane phenomena. Structure of Cell Membranes Thermodynamics and Cell membranes are viewed as two-dimensional solutions Membrane Structure of oriented globular proteins and lipids. The fluid mosaic model has evolved by a series of stages from earlier ver- sions (1-4). Thermodynamicconsidera- tions about membranesand membrane S. J. L. Singer and Garth Nicolson components initiated, and are still cen- tral to, these developments.These con- siderations derived from two decades of intensive studies of protein and nu- Biological membranesplay a crucial considerable detail several models of cleic acid structures;the thermodynamic role in almost all cellular phenomena, the gross structural organization of principles involved, however, are per- yet our understandingof the molecular membranes,in terms of the thermody- fectly general and apply to any macro- organizationof membranesis still rudi- namics of macromolecularsystems and molecular system in an aqueous en- mentary.Experience has taughtus, how- in the light of the then available ex- vironment. These principles and their ever, that in order to achieve a satisfac- perimentalevidence. From this analysis, application to membrane systems have tory understandingof how any biologi- it was concluded that a mosaic struc- been examined in detail elsewhere (1) cal system functions, the detailed ture of alternating globular proteins and are only summarizedhere. For our molecular composition and structureof and phospholipid bilayer was the only present purposes, two kinds of non- that system must be known. While we membranemodel among those analyzed covalent interactions are most impor- are still a long way from such knowl- that was simultaneouslyconsistent with tant, hydrophobic (5) and hydrophilic edge about membranesin general,prog- thermodynamicrestrictions and with all (1). By hydrophobic interactions is ress at both the theoretical and experi- the experimental data available. Since meant a set of thermodynamicfactors mental levels in recentyears has brought that article was written, much new evi- that are responsible for the sequester- us to a stage where at least the gross dence has been published that strongly ing of hydrophobicor nonpolar groups aspects of the organizationof the pro- supportsand extends this mosaic model. away from water, as, for example, the teins and lipids of membranes can be In particular,the mosaic appears to be immiscibility of hydrocarbons and discerned.There are some investigators, a fluid or dynamic one and, for many water. To be specific, it requires the however, who, impressedwith the great purposes, is best thought of as a two- expenditure of 2.6 kilocalories of free diversityof membranecompositions and dimensional oriented viscous solution. energy to transfer a mole of methane functions, do not think there are any In this article, we therefore present and from a nonpolar medium to water at useful generalizationsto be made even discuss a fluid mosaic model of mem- 25?C (5). Free energy contributionsof about the gross structure of cell mem- brane structure, and propose that it is this magnitude,summed over the many branes. We do not share that view. We applicable to most biological mem- nonpolar amino acid residues of soluble suggest that an analogy exists between branes, such as plasmalemmal and in- proteins, are no doubt of primary im- the problems of the structure of mem- tracellular membranes, including the portance in determiningthe conforma- branes and the structure of proteins. membranes of different cell organelles, tions that protein molecules adopt in The latter are tremendously diverse in such as mitochondriaand chloroplasts. aqueous solution (6), in which the non- composition, function, and detailed These membranes are henceforth re- polar residues are predominantly se- structure. Each kind of protein mole- ferred to as functional membranes. questered in the interior of the mole- cule is structurallyunique. Nevertheless, There may be some other membrane- cules away from contact with water. generalizations about protein structure like systems, such as myelin, or the By hydrophilic interactions is meant a have been very useful in understanding lipoproteinmembranes of small animal set of thermodynamicfactors that are the propertiesand functions of protein viruses, which we suggest may be rigid, responsible for the preference of ionic molecules. Similarly, valid generaliza- rather than fluid, mosaic structures,but and polar groups for an aqueous rather tions may exist about the ways in which such membrane systems are not a pri- than a nonpolar environment. For ex- the proteins and lipids are organized in mary concern of this article. ample, the free energy requiredto trans- an intact membrane.The ultimate test Our objectivesare (i) to review briefly fer a mole of zwitterionic glycine from of such generalizations, or models, is some of the thermodynamicsof macro- water to acetone is about 6.0 kcal at whether they are useful to explain old molecular, and particularlymembrane, 25?C, showing that ion pairs strongly experiments and suggest new ones. systems in an aqueous environment; prefer to be in water than in a non- Singer (1) has recently examined in (ii) to discuss some of the properties polar medium (1). These and related of the proteins and lipids of functional free energy terms no doubt provide the Dr. Singer is a professor of biology at the Uni- versity of California at San Diego, La Jolla. Dr. membranes; (iii) to describe the fluid reasons why essentially all the ionic Nicolson is a research associate at the Armand mosaic model in to residues of molecules are ob- Hammer Cancer Center of the Salk Institute for detail; (iv) analyze protein Biological Studies, La Jolla, California. some of the recent and more direct served to be in contact with water, 720 SCIENCE, VOL. 175 usually on the outer surface of the mol- Fig. 1. A phospho- spectrin (8) of erythrocytemembranes, sche- ecule, according to x-ray crystallo- lipid bilayer: which can be removed by chelating matic cross-sectional under mild are ex- graphic studies. Similar thermodynamic view. The filled cir- agents conditions, argumentsapply to saccharide residues cles represent the amples of membrane proteins that sat- (1). It requires the expenditure of sub- ionic and polarhead isfy the criteria for peripheralproteins. stantial free energy to transfer a simple groups of the phos- On the other hand, the major portion saccharide from water to a Ita? pholipid molecules, (> 70 of the of most nonpolar which make contact percent) proteins and membranes have different characteris- solvent, such residueswill therefore withwater; the wavy be in a lower free energy state in con- lines represent the tics, which may be assigned to integral tact with water than in a less polar fatty acid chains. proteins: (i) they require much more environment. drastic treatments, with reagents such There are other noncovalent inter- as detergents, bile acids, protein dena- actions, such as hydrogen bonding and (to the maximum extent feasible) from turants,or organicsolvents, to dissociate electrostatic interactions, which also contact with water, while the ionic and them from membranes;(ii) in many in- contributeto determinemacromolecular polar groups of the proteins-along stances, they remain associated with structure.However, with respectto gross with those of the lipids and the oligosac- lipids when isolated; (iii) if completely structure, with which we are now charides-should be in contact with the freed of lipids, they are usually highly concerned, these are very likely of sec- aqueous solvent. These requirements insolubleor aggregatedin neutral aque- ondary magnitude compared to hydro- place restrictions on models of mem- ous buffers(9). phobic and hydrophilic
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