Myelin basic protein-dependent plasma membrane reorganization in the formation of myelin.
During vertebrate development, oligodendrocytes wrap their plasma membrane around axons to produce myelin, a specialized membrane highly enriched in galactosylceramide (GalC) and cholesterol. Here, we studied the formation of myelin membrane sheets in a neuron-glia co-culture system. We applied different microscopy techniques to visualize lipid packing and dynamics in the oligodendroglial plasma membrane. We used the fluorescent dye Laurdan to examine the lipid order with two-photon microscopy and observed that neurons induce a dramatic lipid condensation of the oligodendroglial membrane. On a nanoscale resolution, using stimulated emission depletion and fluorescence resonance energy transfer microscopy, we demonstrated a neuronal-dependent clustering of GalC in oligodendrocytes. Most importantly these changes in lipid organization of the oligodendroglial plasma membrane were not observed in shiverer mice that do not express the myelin basic protein. Our data demonstrate that neurons induce the condensation of the myelin-forming bilayer in oligodendrocytes and that MBP is involved in this process of plasma membrane rearrangement. We propose that this mechanism is essential for myelin to perform its insulating function during nerve conduction.
Fitzner
Dirk
D
Centre for Biochemistry and Molecular Cell Biology, University of Göttingen, Göttingen, Germany.
Schneider
Anja
A
Kippert
Angelika
A
Möbius
Wiebke
W
Willig
Katrin I
KI
Hell
Stefan W
SW
Bunt
Gertrude
G
Gaus
Katharina
K
Simons
Mikael
M
D000818:Animals; D001369:Axons / Q000378:metabolism*; D002462:Cell Membrane / Q000378:metabolism*; D002478:Cells, Cultured; D018920:Coculture Techniques; D047108:Embryonic Development / Q000502:physiology; D031541:Fluorescence Resonance Energy Transfer / Q000379:methods; D008563:Membrane Lipids / Q000378:metabolism*; D051379:Mice; D008817:Mice, Mutant Strains; D036641:Microscopy, Fluorescence, Multiphoton / Q000379:methods; D004676:Myelin Basic Protein / Q000378:metabolism*; D009186:Myelin Sheath / Q000378:metabolism*; D009836:Oligodendroglia / Q000166:cytology / Q000378:metabolism*; D015398:Signal Transduction / Q000502:physiology
D008563:Membrane Lipids; D004676:Myelin Basic Protein