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

Eszter A. Tóth, Ádám Oszvald, Mária Péter, G. Balogh, Anikó Osteikoetxea-Molnár, Tamás Bozó, Edina Szabó-Meleg, M. Nyitrai, I. Derényi, M. Kellermayer, Toshiyuki Yamaji, Kentaro Hanada, L. Vígh, J. Matkó

Research output: Contribution to journalArticle

4 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)991-1000
Number of pages10
JournalBiochimica et Biophysica Acta - Molecular and Cell Biology of Lipids
Volume1862
Issue number9
DOIs
Publication statusPublished - Sep 1 2017

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Nanotubes
Mechanics
B-Lymphocytes
Lipids
Growth
Membranes
B-Lymphoid Precursor Cells
Cholesterol
Glycosphingolipids
Sphingolipids
Sphingomyelins
Docosahexaenoic Acids
Gangliosides
Elasticity
Membrane Lipids
Phosphatidylcholines
Actins
Immune System
Cell Membrane
Cell Line

Keywords

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

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

Cite this

Nanotubes connecting B lymphocytes : High impact of differentiation-dependent lipid composition on their growth and mechanics. / Tóth, Eszter A.; Oszvald, Ádám; Péter, Mária; Balogh, G.; Osteikoetxea-Molnár, Anikó; Bozó, Tamás; Szabó-Meleg, Edina; Nyitrai, M.; Derényi, I.; Kellermayer, M.; Yamaji, Toshiyuki; Hanada, Kentaro; Vígh, L.; Matkó, J.

In: Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids, Vol. 1862, No. 9, 01.09.2017, p. 991-1000.

Research output: Contribution to journalArticle

Tóth, Eszter A. ; Oszvald, Ádám ; Péter, Mária ; Balogh, G. ; Osteikoetxea-Molnár, Anikó ; Bozó, Tamás ; Szabó-Meleg, Edina ; Nyitrai, M. ; Derényi, I. ; Kellermayer, M. ; Yamaji, Toshiyuki ; Hanada, Kentaro ; Vígh, L. ; Matkó, J. / Nanotubes connecting B lymphocytes : High impact of differentiation-dependent lipid composition on their growth and mechanics. In: Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids. 2017 ; Vol. 1862, No. 9. pp. 991-1000.
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