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The Still Valid Fluid Mosaic Model for Molecular Organization of Biomembranes: Accumulating Data Confirm It

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The Still Valid Fluid Mosaic Model for Molecular Organization of Biomembranes: Accumulating Data Confirm It DISCOVERIES 2013, Oct-Dec; 1(1): e7 DOI: 10.15190/d.2013.7 The still actual fluid mosaic model for membrane organization Focused REVIEW The still valid fluid mosaic model for molecular organization of biomembranes: accumulating data confirm it Mircea Leabu1,* 1University of Medicine and Pharmacy “Carol Davila”, Department of Cellular and Molecular Medicine; “Victor Babes” National Institute of Pathology; University of Bucharest, Research Center for Applied Ethics *Correspondence to: Mircea Leabu, PhD, “Victor Babes” National Institute of Pathology, 99101, Splaiul Independentei, 050096, Bucharest, Romania; E-mail: [email protected] Citation: Leabu M. The still valid fluid mosaic model for molecular organization of biomembranes: accumulating data confirm it. Discoveries 2013, Oct-Dec; 1(1): e7. DOI: 10.15190/d.2013.7 ABSTRACT Keywords: membrane organization, membrane fluidity, membrane microdomains, Singer-Nicolson More than forty years passed since Singer and model, science history Nicolson launched the fluid mosaic model related to molecular organization and dynamics of cell Introduction membranes, applicable to endomembranes as well. For 20 years I and perhaps many other professors During this period of time, that will reach half a have been teaching students in medicine about the century soon, accumulating data all confirm, but not molecular organization of the cell membrane, infirm the brilliant idea of such a model. presenting with a high enthusiasm the fluid mosaic Sometimes, the results developed the model in a model launched by Seymour Jonathan Singer and very impacting manner, as was the case with the Garth L. Nicolson in 19721, and considering it as an introduction of the membrane microdomain concept inspired, still actual scientific and even pedagogic (mainly lipid rafts organization). From a didactical idea. A recent article by Akihiro Kusumi et al.2 point of view, membrane microdomain organization proposed that the current advances on plasma suggests the mosaic’s “bricks” are even more membrane structure are critical and distinguish the complex than mere proteins or protein aggregates cellular membrane structure from the model (the initial ones determining the parents of the proposed by Singer and Nicolson in 1972. Although model to design it). Current times, with high the manuscript is an important contribution in the resolution equipments and techniques allowing live field of membrane organization and functioning, cell investigation, have opened new approaches some aspects and conclusions need to be further resulting in enhancement of our understanding discussed and analyzed. Moreover, this paper about biomembranes organization, dynamics and follows a style specific to the contributions in soft functioning. This paper will analyze some of the sciences, namely a phrase assessment and most recent data about membrane molecular comparisons with the affirmations of Singer and organization and dynamics of biomembrane Nicolson published in their paper in Science, over components, as well as interpretation of these data forty years ago, and, for a stronger argumentation, to see if they could modify the concept related to in two other papers published by the parents of the the fluid mosaic model. In a text assessment model one year before, and by Singer alone two specific to papers in soft sciences, I will show the years after3,4. What’s the story? anticipatory and wise presentation of the fluid The bewilderment that determined this paper started mosaic model by Singer and Nicolson, which has even by reading the abstract of the mentioned made it as a still valid one. paper, where the authors admonished the readers that “The recent rapid accumulation of knowledge www.discoveriesjournals.org/discoveries 1 The still actual fluid mosaic model for membrane organization on the dynamics and structure of the plasma (floating on one or the other surface of, or membrane has prompted major modifications of the immersed into the bilayer), with an oligo/poly- textbook fluid-mosaic model.” Further on, as saccharide “cream” on the external side, carried by conclusions, in the abstract the authors have glycoconjugates (either glycolipids or mentioned: “We propose that the cooperative action glycoproteins/proteoglycans). The cohesiveness of of the hierarchical three-tiered mesoscale (2–300 these diverse molecular components – delimiting a nm) domains – actin-membrane-skeleton induced cell by an ultrastructure without free ends – is compartments (40–300 nm), raft domains (2–20 maintained by noncovalent interactions, allowing a nm), and dynamic protein complex domains (3–10 permanent movement of biocompounds in the nm) – is critical for membrane function and membrane plane. This permanent moving of distinguishes the plasma membrane from a classical molecular components induces a two-dimensional Singer-Nicolson-type model.” After reading the fluidic behavior to the ultrastructure. Indeed, this paper entirely, no reason was found to consider the simplified description of the fluid mosaic model mentioned contributions very different from the could result in misunderstandings, but the eventual fluid mosaic model as introduced and argued, in a confusions are acceptable for beginners like very precautious and clever manner, by Singer and students and not for scientists, a fact pointed out as Nicolson. Furthermore, it was necessary to proceed a common occurrence by the authors of the review at rereading the original papers, to refresh my under discussion: “Many colleagues in other areas memory and find reasons that my understanding of of biomedical science still consider the plasma the fluid mosaic model does not result from my membrane as a simple sea of lipids or, worse, as a generosity, but on account of the argumentation that solid plate, and they describe it as such in major the parents of the model stated. The results of my textbooks, reviews, and research papers. research on the texts will be presented here. Meanwhile, physicists and physical chemists still naively think that the molecular dynamics and The textbook fluid mosaic model is an interactions in the plasma membrane can be oversimplified one understood by directly applying the knowledge The oversimplified presentation of the Singer and gained by using liposomes and artificially Nicolson model inside textbooks (Figure 1) constructed simple membranes.” (See ref. 2, p. 217) stipulates that the basic element in membranes’ There is the teacher’s duty to avoid organization is a lipid bilayer, organized by misunderstanding of the model by the students, on amphiphilic membrane lipids, decorated with the one hand, and the responsibility of every mosaics built by large protein macromolecules scientist to carefully read papers and appropriately Figure 1. Fluid-Mosaic Model Image with an oversimplified presen- tation of the fluid mosaic model in textbooks. Although the heterogeneity and asymmetry in organization is obvious, no dynamics is shown in the image, no protein-protein association, no preferential interaction between lipids and proteins, and no specific organization of peripheral proteins on the cytoplasmic side, all modeling and/or restricting the movement of molecular components. Teachers have to take the responsibility to avoid misunderstanding of the model by the students. www.discoveriesjournals.org/discoveries 2 The still actual fluid mosaic model for membrane organization perceive the matter, on the other hand. No systems are not a primary concern of this article.” misunderstanding could find its source in Singer’s My question is: where is the “universality and and Nicolson’s papers, published at the time, as I apparent uniqueness […] comparable with those of will try to prove below. the double-helical structure of DNA”? The fluid mosaic model is a general one, but not Fluidity in the mosaic model is not grounded in a necessarily universal Brownian movement of molecular components The review’s authors mention on page 217: The idea of a Brownian movement isn’t present “consider that virtually all biological membranes on anywhere in the three mentioned papers1,3,4 of Earth share the common (although peculiar) basic Singer (two of them with Nicolson as co-author). structure of a two-dimensional liquid, consisting of Moreover, Singer and Nicolson have mentioned in the mosaic-like mixture of lipids and proteins that their paper in 1971 that “some of the lipid may not undergo thermal diffusion in the two-dimensional be in the bulk bilayer phase, but may be more space (Singer & Nicolson 1972), and that such strongly interacting with proteins in the membrane” universality and apparent uniqueness are (see ref. 3, p. 429). That means parents of the fluid comparable with those of the double-helical mosaic model rather anticipated the sequestration of structure of DNA.” Here, the authors over some lipids around transmembrane domains of the interpreted Singer’s and Nicolson’s texts. The only proteins, assuring them a right functional reference to nucleic acids in their 1972 paper is conformation, and accompanying them during their related to explanations on scientific sources of the translational movement. The idea that the motility model they propose: “The fluid mosaic model has of membrane components follows other rules but evolved by a series of stages from earlier versions not exactly a Brownian movement, because of […]. Thermodynamic considerations about putative interactions in-between, is largely membranes and membrane components initiated, expressed in the paper in Science:
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