Next Article in Journal
Comparison of Mutation Profiles in the Duchenne Muscular Dystrophy Gene among Populations: Implications for Potential Molecular Therapies
Next Article in Special Issue
Targeted siRNA Screens Identify ER-to-Mitochondrial Calcium Exchange in Autophagy and Mitophagy Responses in RPE1 Cells
Previous Article in Journal
Species-Dependent Splice Recognition of a Cryptic Exon Resulting from a Recurrent Intronic CEP290 Mutation that Causes Congenital Blindness
Previous Article in Special Issue
Ligand-Induced Dynamics of Neurotrophin Receptors Investigated by Single-Molecule Imaging Approaches
Article Menu
Issue 3 (March) cover image

Export Article

Open AccessArticle
Int. J. Mol. Sci. 2015, 16(3), 5299-5333; doi:10.3390/ijms16035299

Trans-Membrane Area Asymmetry Controls the Shape of Cellular Organelles

1
The FIRC Institute of Molecular Oncology, Milan 20139, Italy
2
Consorzio Mario Negri Sud, S. Maria Imbaro, Chieti 66030, Italy
3
Department of Mathematics, University of Florida, Gainesville, FL 32611-8105, USA
4
Department of Biochemical Physiology, Institute of Biomembranes, 3584 CH Utrecht, The Netherlands
5
Department of Physiology and Pharmacology, Tel Aviv University, Tel Aviv 69978, Israel
6
Consiglio Nazionale delle Ricerche (CNR), Istituto di Biochimica delle Proteine, Naples 80131, Italy
7
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
View Full-Text   |   Download PDF [3708 KB, uploaded 9 March 2015]   |  

Abstract

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
This is an open access article distributed under the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. (CC BY 4.0).

Supplementary material

Scifeed alert for new publications

Never miss any articles matching your research from any publisher
  • Get alerts for new papers matching your research
  • Find out the new papers from selected authors
  • Updated daily for 49'000+ journals and 6000+ publishers
  • Define your Scifeed now

SciFeed Share & Cite This Article

MDPI and ACS Style

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.

Show more citation formats Show less citations formats

Related Articles

Article Metrics

Article Access Statistics

1

Comments

[Return to top]
Int. J. Mol. Sci. EISSN 1422-0067 Published by MDPI AG, Basel, Switzerland RSS E-Mail Table of Contents Alert
Back to Top