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Biochim Biophys Acta Mol Cell Biol Lipids. 2017 Sep;1862(9):991-1000. doi: 10.1016/j.bbalip.2017.06.011. Epub 2017 Jun 20.

Nanotubes connecting B lymphocytes: High impact of differentiation-dependent lipid composition on their growth and mechanics.

Author information

1
Department of Immunology, Eötvös Lorand University, Budapest, Hungary.
2
Institute of Biochemistry, Biological Research Centre of the Hungarian Academy of Sciences, Szeged, Hungary.
3
Institute of Biochemistry, Biological Research Centre of the Hungarian Academy of Sciences, Szeged, Hungary. Electronic address: balogh.gabor@brc.mta.hu.
4
Department of Biophysics and Radiation Biology, Semmelweis University, Budapest, Hungary.
5
Department of Biophysics, Medical Faculty, University of Pécs, Pécs, Hungary; Department of Szentágothai Research Center, University of Pécs, Pécs, Hungary.
6
Department of Biological Physics, Eötvös Lorand University, Budapest, Hungary.
7
Department of Biophysics and Radiation Biology, Semmelweis University, Budapest, Hungary; MTA-SE Molecular Biophysics Research Group, Semmelweis University, Budapest, Hungary.
8
Department of Biochemistry and Cell Biology, National Institute of Infectious Diseases, Shunjuku-ku, Tokyo, Japan.
9
Department of Immunology, Eötvös Lorand University, Budapest, Hungary. Electronic address: janos.matko@ttk.elte.hu.

Abstract

Nanotubes (NTs) are thin, long membranous structures forming novel, yet poorly known communication pathways between various cell types. Key mechanisms controlling their growth still remained poorly understood. Since NT-forming capacity of immature and mature B cells was found largely different, we investigated how lipid composition and molecular order of the membrane affect NT-formation. Screening B cell lines with various differentiation stages revealed that NT-growth linearly correlates with membrane ganglioside levels, while it shows maximum as a function of cholesterol level. NT-growth of B lymphocytes is promoted by raftophilic phosphatidylcholine and sphingomyelin species, various glycosphingolipids, and docosahexaenoic acid-containing inner leaflet lipids, through supporting membrane curvature, as demonstrated by comparative lipidomic analysis of mature versus immature B cell membranes. Targeted modification of membrane cholesterol and sphingolipid levels altered NT-forming capacity confirming these findings, and also highlighted that the actual lipid raft number may control NT-growth via defining the number of membrane-F-actin coupling sites. Atomic force microscopic mechano-manipulation experiments further proved that mechanical properties (elasticity or bending stiffness) of B cell NTs also depend on the actual membrane lipid composition. Data presented here highlight importance of the lipid side in controlling intercellular, nanotubular, regulatory communications in the immune system.

KEYWORDS:

B cell membrane nanotubes; Cholesterol; Lipid order/fluidity; Lipidomics; Membrane mechanics; Sphingolipids

PMID:
28645851
DOI:
10.1016/j.bbalip.2017.06.011
[Indexed for MEDLINE]

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