Myelin Membrane Assembly Is Driven by a Phase Transition of Myelin Basic Proteins Into a Cohesive Protein Meshwork

PLoS Biology

Volumn 11, Issue 6, 2013, Pages

  Aggarwal, Shweta ^a,b   Snaidero, Nicolas ^a,b   Pähler, Gesa ^b   Frey, Steffen ^c   Sánchez, Paula ^b,d   Zweckstetter, Markus ^c,e   Janshoff, Andreas ^b   Schneider, Anja ^a,e   Weil, Marie Theres ^a,b   Schaap, Iwan A T ^b,d   Görlich, Dirk ^c   Simons, Mikael ^a,b  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^d Cluster of Excellence Nanoscale Microscopy and Molecular Physiology of the Brain   (Germany)

^e GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; MYELIN; MYELIN BASIC PROTEIN; PHENYLALANINE;

ANIMAL CELL; ARTICLE; BIOGENESIS; CONTROLLED STUDY; HYDROPHOBICITY; MOUSE; NONHUMAN; PHASE TRANSITION; PHYSICAL CHEMISTRY; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM;

AMINO ACID SEQUENCE; AMYLOID; ANIMALS; HEK293 CELLS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MEMBRANES; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MYELIN BASIC PROTEIN; MYELIN SHEATH; PHASE TRANSITION; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84879345495     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001577     Document Type: Article

References (53)

1. Hyman AA, Simons K, (2012) Beyond oil and water-phase transitions in cells. Science 337: 1047-1049.
2. Weber Stephanie C, Brangwynne Clifford P, (2012) Getting RNA and protein in phase. Cell 149: 1188-1191.
3. Brangwynne CP, Eckmann CR, Courson DS, Rybarska A, Hoege C, et al. (2009) Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324: 1729-1732.
4. Kato M, Han Tina W, Xie S, Shi K, Du X, et al. (2012) Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149: 753-767.
5. Emery B, (2010) Regulation of oligodendrocyte differentiation and myelination. Science 330: 779-782.
6. Aggarwal S, Yurlova L, Simons M, (2011) Central nervous system myelin: structure, synthesis and assembly. Trends Cell Biol 21: 585-593.
7. Sherman DL, Brophy PJ, (2005) Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6: 683-690.
8. Barres BA, (2008) The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60: 430-440.
9. Wu LM, Williams A, Delaney A, Sherman DL, Brophy PJ, (2012) Increasing internodal distance in myelinated nerves accelerates nerve conduction to a flat maximum. Curr Biol 22: 1957-1961.
10. Lee S, Leach MK, Redmond SA, Chong SYC, Mellon SH, et al. (2012) A culture system to study oligodendrocyte myelination processes using engineered nanofibers. Nat Methods 9: 917-922.
11. Poliak S, Peles E, (2003) The local differentiation of myelinated axons at nodes of Ranvier. Nat Rev Neurosci 4: 968-980.
12. Salzer JL, Brophy PJ, Peles E, (2008) Molecular domains of myelinated axons in the peripheral nervous system. Glia 56: 1532-1540.
13. Boggs J, (2006) Myelin basic protein: a multifunctional protein. Cellular and Molecular Life Sciences 63: 1945-1961.
14. Harauz G, Ishiyama N, Hill CMD, Bates IR, Libich DS, et al. (2004) Myelin basic protein-diverse conformational states of an intrinsically unstructured protein and its roles in myelin assembly and multiple sclerosis. Micron 35: 503-542.
15. Harauz G, Ladizhansky V, Boggs JM, (2009) Structural polymorphism and multifunctionality of myelin basic protein. Biochemistry 48: 8094-8104.
16. Roach A, Boylan K, Horvath S, Prusiner SB, Hood LE, (1983) Characterization of cloned cDNA representing rat myelin basic protein: absence of expression in brain of shiverer mutant mice. Cell 34: 799-806.
17. Aggarwal S, Yurlova L, Snaidero N, Reetz C, Frey S, et al. (2011) A size barrier limits protein diffusion at the cell surface to generate lipid-rich myelin-membrane sheets. Dev Cell 21: 445-456.
18. Alexander RT, Jaumouille V, Yeung T, Furuya W, Peltekova I, et al. (2011) Membrane surface charge dictates the structure and function of the epithelial Na+/H+ exchanger. EMBO J 30: 679-691.
19. Yeung T, Gilbert GE, Shi J, Silvius J, Kapus A, et al. (2008) Membrane phosphatidylserine regulates surface charge and protein localization. Science 319: 210-213.
20. Frey S, Richter RP, Görlich D, (2006) FG-rich repeats of nuclear pore proteins form a three-dimensional meshwork with hydrogel-like properties. Science 314: 815-817.
21. Mueller H, Butt H-J, Bamberg E, (1999) Force measurements on myelin basic protein adsorbed to mica and lipid bilayer surfaces done with the atomic force microscope. Biophys J 76: 1072-1079.
22. Chen H, McCarty DM, Bruce AT, Suzuki K, (1999) Oligodendrocyte-specific gene expression in mouse brain: use of a myelin-forming cell type-specific promoter in an adeno-associated virus. J Neurosci Res 55: 504-513.
23. Inoue T, Heo WD, Grimley JS, Wandless TJ, Meyer T, (2005) An inducible translocation strategy to rapidly activate and inhibit small GTPase signaling pathways. Nat Meth 2: 415-418.
24. Li P, Banjade S, Cheng H-C, Kim S, Chen B, et al. (2012) Phase transitions in the assembly of multivalent signalling proteins. Nature 483: 336-340.
25. Belli M, Ramazzotti M, Chiti F, (2011) Prediction of amyloid aggregation in vivo. EMBO Rep 12: 657-663.
26. Fowler DM, Koulov AV, Balch WE, Kelly JW, (2007) Functional amyloid from bacteria to humans. Trends in Biochemical Sciences 32: 217-224.
27. Stankoff B, Freeman L, Aigrot M-S, Chardain A, Dollé F, et al. (2011) Imaging central nervous system myelin by positron emission tomography in multiple sclerosis using [methyl-11C]-2-(4′-methylaminophenyl)- 6-hydroxybenzothiazole. Ann Neurol 69: 673-680.
28. Hyman AA, Brangwynne CP, (2011) Beyond stereospecificity: liquids and mesoscale organization of cytoplasm. Dev Cell 21: 14-16.
29. Updike DL, Hachey SJ, Kreher J, Strome S, (2011) P granules extend the nuclear pore complex environment in the C. elegans germ line. J Cell Biol 192: 939-948.
30. Uversky VN, Oldfield CJ, Dunker AK, (2008) Intrinsically disordered proteins in human diseases: introducing the D2 concept. Annu Rev Biophys 37: 215-246.
31. Chiti F, Dobson CM, (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75: 333-366.
32. Ader C, Frey S, Maas W, Schmidt HB, Görlich D, et al. (2010) Amyloid-like interactions within nucleoporin FG hydrogels. Proc Natl Acad Sci U S A 107: 6281-6285.
33. Adler-Abramovich L, Vaks L, Carny O, Trudler D, Magno A, et al. (2012) Phenylalanine assembly into toxic fibrils suggests amyloid etiology in phenylketonuria. Nat Chem Biol 8: 701-706.
34. Maji SK, Perrin MH, Sawaya MR, Jessberger S, Vadodaria K, et al. (2009) Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325: 328-332.
35. White R, Gonsior C, Krämer-Albers E-M, Stöhr N, Hüttelmaier S, et al. (2008) Activation of oligodendroglial Fyn kinase enhances translation of mRNAs transported in hnRNP A2-dependent RNA granules. J Cell Biol 181: 579-586.
36. Laursen LS, Chan CW, ffrench-Constant C, (2011) Translation of myelin basic protein mRNA in oligodendrocytes is regulated by integrin activation and hnRNP-K. J Cell Biol 192: 797-811.
37. Wake H, Lee PR, Fields RD, (2011) Control of local protein synthesis and initial events in myelination by action potentials. Science 333: 1647-1651.
38. Hülsmann Bastian B, Labokha Aksana A, Görlich D, (2012) The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model. Cell 150: 738-751.
39. Crystal AS, Giasson BI, Crowe A, Kung MP, Zhuang ZP, Trojanowski JQ, Lee VM, (2003) A comparison of amyloid fibrillogenesis using the novel fluorescent compound K114. J Neurochem 86: 1359-1368.
40. Trajkovic K, Dhaunchak AS, Goncalves JT, Wenzel D, Schneider A, et al. (2006) Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites. J Cell Biol 172: 937-948.
41. Kügler S, Hahnewald R, Garrido M, Reiss J, (2007) Long-term rescue of a lethal inherited disease by adeno-associated virus-mediated gene transfer in a mouse model of molybdenum-cofactor deficiency. Am J Hum Genet 80: 291-297.
42. Kenworthy AK, (2007) Fluorescence recovery after photobleaching studies of lipid rafts. Methods Mol Biol 398: 179-192.
43. Serrels A, Timpson P, Canel M, Schwarz JP, Carragher NO, et al. (2009) Real-time study of e-cadherin and membrane dynamics in living animals: implications for disease modeling and drug development. Cancer Res 69: 2714-2719.
44. Fogel AI, Stagi M, Perez de Arce K, Biederer T, (2011) Lateral assembly of the immunoglobulin protein SynCAM 1 controls its adhesive function and instructs synapse formation. EMBO J 30: 4728-4738.
45. Nawaz S, Kippert A, Saab AS, Werner HB, Lang T, et al. (2009) Phosphatidylinositol 4,5-bisphosphate-dependent interaction of myelin basic protein with the plasma membrane in oligodendroglial cells and its rapid perturbation by elevated calcium. J Neurosci 29: 4794-4807.
46. Werner HB, Kuhlmann K, Shen S, Uecker M, Schardt A, et al. (2007) Proteolipid protein is required for transport of sirtuin 2 into CNS myelin. J Neurosci 27: 7717-7730.
47. Eisele NB, Frey S, Piehler J, Gorlich D, Richter RP, (2010) Ultrathin nucleoporin phenylalanine-glycine repeat films and their interaction with nuclear transport receptors. EMBO Rep 11: 366-372.
48. Kahya N, Scherfeld D, Schwille P, (2005) Differential lipid packing abilities and dynamics in giant unilamellar vesicles composed of short-chain saturated glycerol-phospholipids, sphingomyelin and cholesterol. Chem Phys Lipids 135: 169-180.
49. Garcia-Saez AJ, Schwille P, (2010) Stability of lipid domains. FEBS Lett 584: 1653-1658.
50. Andrushchenko VV, Vogel HJ, Prenner EJ, (2007) Optimization of the hydrochloric acid concentration used for trifluoroacetate removal from synthetic peptides. J Peptide Sci 13: 37-43.
51. Reimhult E, Höök F, Kasemo B, (2002) Temperature dependence of formation of a supported phospholipid bilayer from vesicles on SiO_{2}. Phys Rev E 66: 051905.
52. Friedrichson T, Kurzchalia TV, (1998) Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature 394: 802-805.
53. Olzscha H, Schermann SM, Woerner AC, Pinkert S, Hecht MH, et al. (2011) Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 144: 67-78.