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Int. J. Mol. Sci. 2015, 16(3), 5299-5333;

Trans-Membrane Area Asymmetry Controls the Shape of Cellular Organelles

The FIRC Institute of Molecular Oncology, Milan 20139, Italy
Consorzio Mario Negri Sud, S. Maria Imbaro, Chieti 66030, Italy
Department of Mathematics, University of Florida, Gainesville, FL 32611-8105, USA
Department of Biochemical Physiology, Institute of Biomembranes, 3584 CH Utrecht, The Netherlands
Department of Physiology and Pharmacology, Tel Aviv University, Tel Aviv 69978, Israel
Consiglio Nazionale delle Ricerche (CNR), Istituto di Biochimica delle Proteine, Naples 80131, Italy
Institute of Biophysics, University of Ljubljana, 1000 Ljubljana, Slovenia
Authors to whom correspondence should be addressed.
Academic Editor: Jeremy Simpson
Received: 5 December 2014 / Revised: 4 February 2015 / Accepted: 13 February 2015 / Published: 9 March 2015
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Membrane organelles often have complicated shapes and differ in their volume, surface area and membrane curvature. The ratio between the surface area of the cytosolic and luminal leaflets (trans-membrane area asymmetry (TAA)) determines the membrane curvature within different sites of the organelle. Thus, the shape of the organelle could be critically dependent on TAA. Here, using mathematical modeling and stereological measurements of TAA during fast transformation of organelle shapes, we present evidence that suggests that when organelle volume and surface area are constant, TAA can regulate transformation of the shape of the Golgi apparatus, endosomal multivesicular bodies, and microvilli of brush borders of kidney epithelial cells. Extraction of membrane curvature by small spheres, such as COPI-dependent vesicles within the Golgi (extraction of positive curvature), or by intraluminal vesicles within endosomes (extraction of negative curvature) controls the shape of these organelles. For instance, Golgi tubulation is critically dependent on the fusion of COPI vesicles with Golgi cisternae, and vice versa, for the extraction of membrane curvature into 50–60 nm vesicles, to induce transformation of Golgi tubules into cisternae. Also, formation of intraluminal ultra-small vesicles after fusion of endosomes allows equilibration of their TAA, volume and surface area. Finally, when microvilli of the brush border are broken into vesicles and microvilli fragments, TAA of these membranes remains the same as TAA of the microvilli. Thus, TAA has a significant role in transformation of organelle shape when other factors remain constant. View Full-Text
Keywords: intra-Golgi transport; Golgi apparatus; lipid membrane; trans-membrane area asymmetry; organelle shape; kiss-and-run model intra-Golgi transport; Golgi apparatus; lipid membrane; trans-membrane area asymmetry; organelle shape; kiss-and-run model

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Beznoussenko, G.V.; Pilyugin, S.S.; Geerts, W.J.C.; Kozlov, M.M.; Burger, K.N.J.; Luini, A.; Derganc, J.; Mironov, A.A. Trans-Membrane Area Asymmetry Controls the Shape of Cellular Organelles. Int. J. Mol. Sci. 2015, 16, 5299-5333.

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