Self-segregation of myelin membrane lipids in model membranes

Biophysical Journal

Volumn 101, Issue 11, 2011, Pages 2713-2720

  Yurlova, Larisa ^a   Kahya, Nicoletta ^b   Aggarwal, Shweta ^a   Kaiser, Hermann Josef ^c   Chiantia, Salvatore ^d   Bakhti, Mostafa ^a   Pewzner Jung, Yael ^e   Ben David, Oshrit ^e   Futerman, Anthony H ^e   Brügger, Britta ^f   Simons, Mikael ^a,g  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^d STONY BROOK UNIVERSITY   (United States)

^e WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^f UNIVERSITY OF HEIDELBERG   (Germany)

^g UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; MEMBRANE LIPID; SPHINGOLIPID; TISSUE EXTRACT;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; C57BL MOUSE; CHEMISTRY; DIFFUSION; MEMBRANE; METABOLISM; MOUSE; MOUSE MUTANT; MYELIN SHEATH;

ANIMALS; DIFFUSION; FATTY ACIDS; MEMBRANE LIPIDS; MEMBRANES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NEUROLOGIC MUTANTS; MODELS, BIOLOGICAL; MYELIN SHEATH; SPHINGOLIPIDS; TISSUE EXTRACTS;

EID: 82955169515     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.10.026     Document Type: Article

References (58)

1. D.L. Sherman, and P.J. Brophy Mechanisms of axon ensheathment and myelin growth Nat. Rev. Neurosci. 6 2005 683 690
2. M. Simons, and J. Trotter Wrapping it up: the cell biology of myelination Curr. Opin. Neurobiol. 17 2007 533 540
3. B. Zalc, D. Goujet, and D. Colman The origin of the myelination program in vertebrates Curr. Biol. 18 2008 R511 R512
4. N. Baumann, and D. Pham-Dinh Biology of oligodendrocyte and myelin in the mammalian central nervous system Physiol. Rev. 81 2001 871 927
5. R. Chrast, and G. Saher M.H. Verheijen Lipid metabolism in myelinating glial cells: lessons from human inherited disorders and mouse models J. Lipid Res. 52 2011 419 434
6. N. Jackman, A. Ishii, and R. Bansal Oligodendrocyte development and myelin biogenesis: parsing out the roles of glycosphingolipids Physiology (Bethesda) 24 2009 290 297
7. S.E. Pfeiffer, A.E. Warrington, and R. Bansal The oligodendrocyte and its many cellular processes Trends Cell Biol. 3 1993 191 197
8. B. Emery Regulation of oligodendrocyte differentiation and myelination Science 330 2010 779 782
9. W. Baron, and D. Hoekstra On the biogenesis of myelin membranes: sorting, trafficking and cell polarity FEBS Lett. 584 2010 1760 1770
10. S.L. Keller, and W.H. Pitscher III H.M. McConnell Red blood cell lipids form immiscible liquids Phys. Rev. Lett. 81 1998 5019 5022
11. C.M. Rosetti, R.G. Oliveira, and B. Maggio The Folch-Lees proteolipid induces phase coexistence and transverse reorganization of lateral domains in myelin monolayers Biochim. Biophys. Acta 1668 2005 75 86
12. C.M. Rosetti, B. Maggio, and N. Wilke Micron-scale phase segregation in lipid monolayers induced by myelin basic protein in the presence of a cholesterol analog Biochim. Biophys. Acta 1798 2010 498 505
13. Y. Hu, and J. Israelachvili Lateral reorganization of myelin lipid domains by myelin basic protein studied at the air-water interface Colloids Surf. B Biointerfaces 62 2008 22 30
14. Y. Pewzner-Jung, and H. Park A.H. Futerman A critical role for ceramide synthase 2 in liver homeostasis. I. Alterations in lipid metabolic pathways J. Biol. Chem. 285 2010 10902 10910
15. Y. Pewzner-Jung, and O. Brenner A.H. Futerman A critical role for ceramide synthase 2 in liver homeostasis. II. Insights into molecular changes leading to hepatopathy J. Biol. Chem. 285 2010 10911 10923
16. G.F. Chernoff Shiverer: an autosomal recessive mutant mouse with myelin deficiency J. Hered. 72 1981 128
17. M. Jung, and A.J. Crang J. Trotter In vitro and in vivo characterization of glial cells immortalized with a temperature sensitive SV40 T antigen-containing retrovirus J. Neurosci. Res. 37 1994 182 196
18. K. Trajkovic, and A.S. Dhaunchak M. Simons Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites J. Cell Biol. 172 2006 937 948
19. J.N. Larocca, and W.T. Norton Isolation of myelin Curr. Protoc. Cell Biol. 2007 DOI:10.1002/0471143030.cb0325s33
20. E.G. Bligh, and W.J. Dyer A rapid method of total lipid extraction and purification Can. J. Biochem. Physiol. 37 1959 911 917
21. B. Brügger, and B. Glass H.G. Kräusslich The HIV lipidome: a raft with an unusual composition Proc. Natl. Acad. Sci. USA 103 2006 2641 2646
22. B. Brügger, and R. Sandhoff F.T. Wieland Evidence for segregation of sphingomyelin and cholesterol during formation of COPI-coated vesicles J. Cell Biol. 151 2000 507 518
23. G. Liebisch, and M. Binder G. Schmitz High throughput quantification of cholesterol and cholesteryl ester by electrospray ionization tandem mass spectrometry (ESI-MS/MS) Biochim. Biophys. Acta 1761 2006 121 128
24. J. Folch, M. Lees, and G.H. Sloane Stanley A simple method for the isolation and purification of total lipids from animal tissues J. Biol. Chem. 226 1957 497 509
25. N. Kahya, D. Scherfeld, and P. Schwille Differential lipid packing abilities and dynamics in giant unilamellar vesicles composed of short-chain saturated glycerol-phospholipids, sphingomyelin and cholesterol Chem. Phys. Lipids 135 2005 169 180
26. A.J. García-Sáez, and P. Schwille Stability of lipid domains FEBS Lett. 584 2010 1653 1658
27. J. Ries, and S.R. Yu P. Schwille Modular scanning FCS quantifies receptor-ligand interactions in living multicellular organisms Nat. Methods 6 2009 643 645
28. N. Kahya, and D. Scherfeld P. Schwille Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy J. Biol. Chem. 278 2003 28109 28115
29. H.J. Kaiser, and D. Lingwood K. Simons Order of lipid phases in model and plasma membranes Proc. Natl. Acad. Sci. USA 106 2009 16645 16650
30. A.K. Kenworthy Fluorescence recovery after photobleaching studies of lipid rafts Methods Mol. Biol. 398 2007 179 192
31. N.P. Franks, and V. Melchior D.L. Caspar Structure of myelin lipid bilayers. Changes during maturation J. Mol. Biol. 155 1982 133 153
32. R.G. Oliveira, R.O. Calderón, and B. Maggio Surface behavior of myelin monolayers Biochim. Biophys. Acta 1370 1998 127 137
33. T. Parasassi, and G. De Stasio E. Gratton Phase fluctuation in phospholipid membranes revealed by Laurdan fluorescence Biophys. J. 57 1990 1179 1186
34. K. Gaus, and E. Gratton W. Jessup Visualizing lipid structure and raft domains in living cells with two-photon microscopy Proc. Natl. Acad. Sci. USA 100 2003 15554 15559
35. D.M. Owen, and A. Magenau K. Gaus Imaging membrane lipid order in whole, living vertebrate organisms Biophys. J. 99 2010 L7 L9
36. T.D. Bird, D.F. Farrell, and S.M. Sumi Brain lipid composition of the Shiverer mouse: (genetic defect in myelin development) J. Neurochem. 31 1978 387 391
37. S. Imgrund, and D. Hartmann K. Willecke Adult ceramide synthase 2 (CERS2)-deficient mice exhibit myelin sheath defects, cerebellar degeneration, and hepatocarcinomas J. Biol. Chem. 284 2009 33549 33560
38. G. Saher, and B. Brügger K.A. Nave High cholesterol level is essential for myelin membrane growth Nat. Neurosci. 8 2005 468 475
39. C. Klose, and C.S. Ejsing K. Simons Yeast lipids can phase-separate into micrometer-scale membrane domains J. Biol. Chem. 285 2010 30224 30232
40. A.J. García-Sáez, S. Chiantia, and P. Schwille Effect of line tension on the lateral organization of lipid membranes J. Biol. Chem. 282 2007 33537 33544
41. S.N. Pinto, and L.C. Silva M. Prieto Membrane domain formation, interdigitation, and morphological alterations induced by the very long chain asymmetric C24:1 ceramide Biophys. J. 95 2008 2867 2879
42. S. Chiantia, and P. Schwille E. London Asymmetric GUVs prepared by MβCD-mediated lipid exchange: an FCS study Biophys. J. 100 2011 L1 L3
43. R.G. Oliveira, and B. Maggio Epifluorescence microscopy of surface domain microheterogeneity in myelin monolayers at the air-water interface Neurochem. Res. 25 2000 77 86
44. R.G. Oliveira, and B. Maggio Compositional domain immiscibility in whole myelin monolayers at the air-water interface and Langmuir-Blodgett films Biochim. Biophys. Acta 1561 2002 238 250
45. C.M. Rosetti, B. Maggio, and R.G. Oliveira The self-organization of lipids and proteins of myelin at the membrane interface. Molecular factors underlying the microheterogeneity of domain segregation Biochim. Biophys. Acta 1778 2008 1665 1675
46. Y. Min, and T.F. Alig J.A. Zasadzinski Critical and off-critical miscibility transitions in model extracellular and cytoplasmic myelin lipid monolayers Biophys. J. 100 2011 1490 1498
47. H.M. McConnell, and M. Vrljic Liquid-liquid immiscibility in membranes Annu. Rev. Biophys. Biomol. Struct. 32 2003 469 492
48. L.A. Bagatolli, and J.H. Ipsen O.G. Mouritsen An outlook on organization of lipids in membranes: searching for a realistic connection with the organization of biological membranes Prog. Lipid Res. 49 2010 378 389
49. T. Baumgart, and A.T. Hammond W.W. Webb Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles Proc. Natl. Acad. Sci. USA 104 2007 3165 3170
50. D. Lingwood, and J. Ries K. Simons Plasma membranes are poised for activation of raft phase coalescence at physiological temperature Proc. Natl. Acad. Sci. USA 105 2008 10005 10010
51. T.A. Ryan, and J. Myers W.W. Webb Molecular crowding on the cell surface Science 239 1988 61 64
52. S. Aggarwal, L. Yurlova, and M. Simons Central nervous system myelin: structure, synthesis and assembly Trends Cell Biol. 21 2011 585 593
53. G. Harauz, V. Ladizhansky, and J.M. Boggs Structural polymorphism and multifunctionality of myelin basic protein Biochemistry 48 2009 8094 8104
54. H. Mueller, H.J. Butt, and E. Bamberg Force measurements on myelin basic protein adsorbed to mica and lipid bilayer surfaces done with the atomic force microscope Biophys. J. 76 1999 1072 1079
55. C.M. Rosetti, and B. Maggio Protein-induced surface structuring in myelin membrane monolayers Biophys. J. 93 2007 4254 4267
56. P. Rispoli, and R. Carzino R. Rolandi A thermodynamic and structural study of myelin basic protein in lipid membrane models Biophys. J. 93 2007 1999 2010
57. D. Fitzner, and A. Schneider M. Simons Myelin basic protein-dependent plasma membrane reorganization in the formation of myelin EMBO J. 25 2006 5037 5048
58. S. Aggarwal, and L. Yurlova M. Simons A size barrier limits protein diffusion at the cell surface to generate lipid-rich myelin-membrane sheets Dev. Cell 21 2011 445 456