Trans-membrane area asymmetry controls the shape of cellular organelles

Beznoussenko, Galina V. (author), Pilyugin, Sergei S. (author), Geerts, Willie J. C. (author), Kozlov, Michael M. (author), Burger, Koert N. J. (author), Luini, Alberto (author), Derganc, Jure (author), Mironov, Alexander A. (author)

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.

• Language: English
• Keywords: lipid membrane, asymmetry, Golgi apparatus, intra-Golgi transport, trans-membrane area asymmetry, organelle shape, kiss-and-run model
• Work type: Article
• Typology: 1.01 - Original Scientific Article
• Organization: MF - Faculty of Medicine
• Publication status: Published
• Publication version: Version of Record
• Year: 2015
• Number of pages: Str. 5299-5333
• Numbering: Vol. 16, iss. 3
• PID: 20.500.12556/RUL-130503
• UDC: 577
• ISSN on article: 1422-0067
• DOI: 10.3390/ijms16035299
• COBISS.SI-ID: 32179417
• Publication date in RUL: 15.09.2021

Record is a part of a journal

• Title: International journal of molecular sciences
• Shortened title: Int. j. mol. sci.
• Publisher: MDPI
• ISSN: 1422-0067
• COBISS.SI-ID: 2779162

Licences

• License: CC BY 4.0, Creative Commons Attribution 4.0 International
• Link: http://creativecommons.org/licenses/by/4.0/
• Description: This is the standard Creative Commons license that gives others maximum freedom to do what they want with the work as long as they credit the author.
• Licensing start date: 09.03.2015

Secondary language

• Language: Slovenian
• Keywords: lipidna membrana, asimetrija, Golgijev aparat

Projects

• Funder: Other - Other funder or multiple funders
• Funding programme: Consorzio Mario Negri Sud

• Funder: Other - Other funder or multiple funders
• Funding programme: FIRC (Italy)