The classic basic protein of myelin - Conserved structural motifs and the dynamic molecular barcode involved in membrane adhesion and protein-protein interactions

Current Protein and Peptide Science

Volumn 10, Issue 3, 2009, Pages 196-215

  Harauz, George ^a   Libich, David S ^a,b  

^a UNIVERSITY OF GUELPH   (Canada)

^b MASSEY UNIVERSITY   (New Zealand)

Author keywords

Amphipathic helix; Golli (genes of oligodendrocyte lineage); Intrinsically disordered protein; Lipid rafts; Membrane adhesion; Multiple sclerosis; Myelin basic protein; Polyproline type II helix

Indexed keywords

ACTIN; CALCIUM; CALMODULIN; CYTOSKELETON PROTEIN; EPITOPE; MARCKS PROTEIN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYELIN; MYELIN BASIC PROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PHOSPHOLIPID; PROLINE; PROTEIN KINASE C; PROTEIN SH3; STATHMIN; TAU PROTEIN; THREONINE; TUBULIN;

ALPHA HELIX; CARBOXY TERMINAL SEQUENCE; CENTRAL NERVOUS SYSTEM; CIRCULAR DICHROISM; ELECTRON SPIN RESONANCE; ENTROPY; FLUORESCENCE SPECTROSCOPY; GENETIC CONSERVATION; HUMAN; MULTIPLE SCLEROSIS; MYELIN SHEATH; MYELINATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHOLIPID MEMBRANE; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; RNA SPLICING; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; STRUCTURE ACTIVITY RELATION; TRANSCRIPTION INITIATION; ADHESION; AMINO ACID SEQUENCE; ANIMAL; CELL MEMBRANE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN BINDING;

ADHESIVENESS; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; CONSERVED SEQUENCE; HUMANS; MOLECULAR SEQUENCE DATA; MYELIN BASIC PROTEINS; PROTEIN BINDING;

EID: 69249131573     PISSN: 13892037     EISSN: None     Source Type: Journal    
DOI: 10.2174/138920309788452218     Document Type: Review

References (200)

1. Lazzarini, R.A. Myelin Biology and Disorders, Elsevier Academic Press, San Diego, 2004.
2. Campagnoni, AT.; Campagnoni, C. In Myelin Biology and Disorders, Lazzarini, R.A.; Griffin, J.W.; Lassman, H.; Nave, K.-A.; Miller, R.H.; Trapp, B.D.; Eds. Elsevier Academic Press, San Diego, 2004; pp. 387-400.
3. Givogri, M.I.; Bongarzone, E.R.; Campagnoni, A.T. New insights on the biology of myelin basic protein gene: the neural-immune connection. J. Neurosci. Res., 2000, 59, 153-159.
4. Hill, C.M.D.; Libich, D.S.; Harauz, G. Assembly of tubulin by classic myelin basic protein isoforms and regulation by post-translational modification. Biochemistry, 2005, 44, 16672-16683.
5. Feng, J.M.; Fernandes, A.O.; Campagnoni, C.W.; Hu, Y.H.; Campagnoni, A.T. The golli-myelin basic protein negatively regulates signal transduction in -T lymphocytes. J. Neuroimmunol., 2004, 152, 57-66.
6. Fernandes, A.O.; Campagnoni, C.W.; Kampf, K.; Feng, J.M.; Handley, V.W.; Schonmann, V.; Bongarzone, E.R.; Reyes, S.; Campagnoni, A.T. Identification of a protein that interacts with the golli-myelin basic protein and with nuclear LIM interactor in the nervous system. J. Neurosci. Res., 2004, 75, 461-471.
7. Jacobs, E.C.; Pribyl, T.M.; Kampf, K.; Campagnoni, C.; Colwell, C.S.; Reyes, S.D.; Martin, M.; Handley, V.; Hiltner, T.D.; Readhead, C.; Jacobs, R.E.; Messing, A.; Fisher, R.S.; Campagnoni, A.T. Region-specific myelin pathology in mice lacking the golli products of the myelin basic protein gene. J. Neurosci., 2005, 25, 7004-7013.
8. Feng, J.M.; Hu, Y.K.; Xie, L.H.; Colwell, C.S.; Shao, X.M.; Sun, X.P.; Chen, B.; Tang, H.; Campagnoni, A.T. Golli protein negatively regulates store depletion-induced calcium influx in T cells. Immunity, 2006, 24, 717-727.
9. Campagnoni, C.; Campagnoni, A.T.; Bassilian, S.; Ryan, C.; Whitelegge, J.; Faull, K. A myristoylated fragment of the Golli-MBP protein in mouse brain. J. Neurochem., 2008, 104 (Supplement 1), 43-44.
10. Paez, P.M.; Fulton, D.J.; Spreur, V.; Handley, V.; Campagnoni, C.W.; Campagnoni, A.T. Regulation of Ca2+ entry into oligodendrocytes by Golli products of the Mbp gene. J. Neurochem., 2008, 104 (Supplement 1), 43.
11. Harauz, G.; Ishiyama, N.; Hill, C.M.D.; Bates, I.R.; Libich, D.S.; Farès, C. Myelin basic protein - diverse conformational states of an intrinsically unstructured protein and its roles in myelin assembly and multiple sclerosis. Micron, 2004, 35, 503-542.
12. Boggs, J.M. Myelin basic protein: a multifunctional protein. Cell. Mol. Life Sci., 2006, 63, 1945-1961.
13. Pedraza, L., Fidler, L.; Staugaitis, S.M.; Colman, D.R. The active transport of myelin basic protein into the nucleus suggests a regulatory role in myelination. Neuron, 1997, 18, 579-589.
14. Inouye, H.; Kirschner, D.A. Folding and function of the myelin proteins from primary sequence data. J. Neurosci. Res., 1991, 28, 1-17.
15. Thompson, J.D.; Higgins, D.G.; Gibson, T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 1994, 22, 4673-4680.
16. Altschul, S.F.; Madden, T.L.; Schaffer, A.A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 1997, 25, 3389-3402.
17. Mitchell, C., Sokal, R. A quantitative approach to a problem in classification. Evolution, 1957, 11, 130-162.
18. Sneath, P.; Sokal, R. (1973) Numerical Taxonomy (Freeman, San Francisco).
19. Kim, J.K.; Mastronardi, F.G.; Wood, D.D.; Lubman, D.M.; Zand, R.; Moscarello, M.A. Multiple sclerosis: an important role for post-translational modifications of myelin basic protein in pathogenesis. Mol. Cell. Proteomics, 2003, 2, 453-462.
20. Moscarello, M.A.; Wood, D.D.; Ackerley, C.; Boulias, C. Myelin in multiple sclerosis is developmentally immature. J. Clin. Invest., 1994, 94, 146-154.
21. Wood, D.D.; Bilbao, J.M.; O'Connors, P.; Moscarello, M.A. Acute multiple sclerosis (Marburg type) is associated with developmentally immature myelin basic protein. Ann. Neurol., 1996, 40, 18-24.
22. Whitaker, J.N.; Mitchell, G.W. A possible role for altered myelin basic protein in multiple sclerosis. Ann. Neurol., 1996, 40, 3-4.
23. Yang, X.J. Multisite protein modification and intramole-cular signaling. Oncogene, 2005, 24, 1653-1662.
24. Minagar, A. (2008) The neurobiology of multiple sclerosis (Elsevier Academic Press, San Diego).
25. Kouzarides, T. Chromatin modifications and their function. Cell, 2007, 128, 693-705.
26. Verhey, K.J.; Gaertig, J. The tubulin code. Cell Cycle, 2007, 6, 2152-2160.
27. Vossenaar, E.R.; Zendman, A.J.; Van Venrooij, W.J.; Pruijn, G.J. PAD, a growing family of citrullinating enzymes: genes, features and involvement in disease. Bioessays, 2003, 25, 1106-1118.
28. Harauz, G.; Musse, A.A. A tale of two citrullines - structural and functional aspects of myelin basic protein deimination in health and disease. Neurochem. Res., 2007, 32, 137-158.
29. Moscarello, M.A.; Mastronardi, F.G.; Wood, D.D. The role of citrullinated proteins suggests a novel mechanism in the pathogenesis of multiple sclerosis. Neurochem. Res., 2007, 32, 251-256.
30. Kim, S.; Chanderkar, L.P.; Ghosh, S.K.; Park, J.O.; Paik, W.K. Enzymatic methylation of arginine residue in myelin basic protein. Adv. Exp. Med. Biol., 1988, 231, 327-340.
31. Raijmakers, R.; Zendman, A.J.; Egberts, W.V.; Vossenaar, E.R.; Raats, J.; Soede-Huijbregts, C.; Rutjes, F.P.; van Veelen, P.A.; Drijfhout, J.W.; Pruijn, G.J. Methylation of arginine residues interferes with citrullination by peptidylarginine deiminases in vitro. J. Mol. Biol., 2007, 367, 1118-1129.
32. Eichberg, J.; Iyer, S. Phosphorylation of myelin protein: recent advances. Neurochem. Res., 1996, 21, 527-535.
33. Kim, H.; Jo, S.; Song, H.J.; Park, Z.Y.; Park, C.S. Myelin basic protein as a binding partner and calmodulin adaptor for the BK(Ca) channel. Proteomics, 2007, 7, 2591-2602.
34. Polverini, E.; Rangaraj, G.; Libich, D.S.; Boggs, J.M.; Harauz, G. Binding of the proline-rich segment of myelin basic protein to SH3-domains - Spectroscopic, microarray, and modelling studies of ligand conformation and effects of post-translational modifications. Biochemistry, 2008, 47, 267-282.
35. Stapulionis, R.; Oliveira, C.L.P.; Gjelstrup, M.C.; Pedersen, J.S.; Hokland, M.A.; Hoffmann, S.V.; Poulsen, K.; Jacobsen, C.; Vorup-Jensen, T. Structural insight into the function of myelin basic protein as a ligand for integrin □ □ □ □. J. Immunol., 2008, 180, 3946-3956.
36. Majava, V.; Petoukhov, M.V.; Hayashi, N.; Pirila, P.; Svergun, D.I.; Kursula, P. Interaction between the C-terminal region of human myelin basic protein and calmodulin: analysis of complex formation and solution structure. BMC Struct. Biol., 2008, 8, 10.
37. Libich, D.S.; Harauz, G. Backbone dynamics of the 18.5 kDa isoform of myelin basic protein reveals transient □-helices and a calmodulin-binding site. Biophys. J., 2008, 94, 4847-4866.
38. Krämer, E.M.; Schardt, A.; Nave, K.A. Membrane traffic in myelinating oligodendrocytes. Microsc. Res. Tech., 2001, 52, 656-671.
39. Sherman, D.L.; Brophy, P.J. Mechanisms of axon ensheathment and myelin growth. Nat. Rev. Neurosci., 2005, 6, 683-690.
40. Fitzner, D.; Schneider, A.; Kippert, A.; Mobius, W.; Willig, K.I.; Hell, S.W.; Bunt, G.; Gaus, K.; Simons, M. Myelin basic protein-dependent plasma membrane reorganization in the formation of myelin. EMBO J., 2006, 25, 5037-5048.
41. Simons, M.; Trotter, J. Wrapping it up: the cell biology of myelination. Curr. Opin. Neurobiol., 2007, 17, 533-540.
42. Song, J.; Goetz, B.D.; Baas, P.W.; Duncan, I.D. Cytoskeletal reorganization during the formation of oligodendrocyte processes and branches. Mol. Cell Neurosci., 2001, 17, 624-636.
43. Richter-Landsberg, C. Organization and functional roles of the cytoskeleton in oligodendrocytes. Microsc. Res. Tech., 2001, 52, 628-636.
44. Richter-Landsberg, C. The cytoskeleton in oligoden-drocytes: microtubule dynamics in health and disease. J. Mol. Neurosci., 2008, 35, 55-63.
45. Boggs, J.M.; Rangamj, G. Interaction of lipid-bound myelin basic protein with actin filaments and calmodulin. Biochemistry, 2000, 39, 7799-7806.
46. Boggs, J.M.; Rangaraj, G.; Hill, C.M.; Bates, I.R.; Heng, Y.M.; Harauz, G. Effect of arginine loss in myelin basic protein, as occurs in its deiminated charge isoform, on mediation of actin polymerization and actin binding to a lipid membrane in vitro. Biochemistry, 2005, 44, 3524-3534.
47. Hill, C.M.D.; Harauz, G. Charge effects modulate actin assembly by classic myelin basic protein isoforms. Biochem. Biophys. Res. Commun., 2005, 329, 362-369.
48. Boggs, J.M.; Rangaraj, G.; Gao, W.; Heng, Y.M. Effect of phosphorylation of myelin basic protein by MAPK on its interactions with actin and actin binding to a lipid membrane in vitro. Biochemistry, 2006, 45, 391-401.
49. Galiano, M.R.; Andrieux, A.; Deloulme, J.C.; Bose, C.; Schweitzer, A.; Job, D.; Hallak, M.E. Myelin basic protein functions as a microtubule stabilizing protein in differentiated oligoden-drocytes. J. Neurosci. Res., 2006, 84, 534-541.
50. Perkins, G.A.; Sosinsky, G.E.; Ghassemzadeh, S.; Perez, A.; Jones, Y.; Ellisman, M.H. Electron tomographic analysis of cytoskeletal cross-bridges in the paranodal region of the node of Ranvier in peripheral nerves. J. Struct. Biol., 2008, 161, 469-480.
51. Martenson, R.E. (1980) in Biochemistry of Brain, ed. Kumar, S. (Pergamon Press, Oxford), pp. 49-79.
52. Benmerah, A.; Scott, M.; Poupon, V.; Marullo, S. Nuclear functions for plasma membrane-associated proteins? Traffic, 2003, 4, 503-511.
53. Sedzik, J.; Kirschner, D.A. Is myelin basic protein crystallizable? Neurochem. Res., 1992, 17, 157-166.
54. Hill, C.M.D.; Bates, I.R.; White, G.F.; Hallett, F.R.; Harauz, G. Effects of the osmolyte- trimethylamine-N-oxide on conformation, self-association, and two-dimensional crystallization of myelin basic protein. J. Struct. Biol., 2002, 139, 13-26.
55. Receveur-Bréchot, V.; Bourhis, J.M.; Uversky, V.N.; Canard, B.; Longhi, S. Assessing protein disorder and induced folding. Proteins, 2006, 62, 24-45.
56. Radivojac, P.; Iakoucheva, L.M.; Oldfield, C.J.; Obradovic, Z.; Uversky, V.N.; Dunker, A.K. Intrinsic disorder and functional proteomics. Biophys. J., 2007, 92, 1439-1456.
57. Xie, H.; Vucetic, S.; Iakoucheva, L.M.; Oldfield, C.J.; Dunker, A.K.; Uversky, V.N.; Obradovic, Z. Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions. J. Proteome Res., 2007, 6, 1882-1898.
58. Vucetic, S.; Xie, H.; Iakoucheva, L.M.; Oldfield, C.J.; Dunker, A.K.; Obradovic, Z., Uversky, V.N. Functional anthology of intrinsic disorder. 2. Cellular components, domains, technical terms, developmental processes, and coding sequence diversities correlated with long disordered regions. J. Proleome Res., 2007, 6, 1899-1916.
59. Xie, H.; Vucetic, S.; Iakoucheva, L.M.; Oldfield, C.J.; Dunker, A.K.; Obradovic, Z.; Uversky, V.N.) Functional anthology of intrinsic disorder. 3. Ligands, post-translational modifications, and diseases associated with intrinsically disoTdered proteins. J. Proteome Res., 2007, 6, 1917-1932.
60. Tompa, P.; Szasz, C.; Buday, L. Structural disorder throws new light on moonlighting. Trends Biochem. Sci., 2005, 30, 484-489.
61. Tompa, P. The interplay between structure and function in intrinsically unstructured proteins. FEBS Lett., 2005, 579, 3346-3354.
62. Fuxreiter, M.; Tompa, P.; Simon, I. Local structural disorder imparts plasticity on linear motifs. Bioinformatics, 2007, 23, 950-956.
63. Mohan, A.; Oldfield, C.J.; Radivojac, P.; Vacic, V.; Cortese, M.S Dunker, A.K.; Uversky, V.N. Analysis of molecular recognition features (MoRFs). J. Mol. Biol., 2006, 362, 1043-1059.
64. Vacic, V.; Oldfield, C.J.; Mohan, A.; Radivojac, P.; Cortese, M.S.; Uversky, V.N.; Dunker, A.K.) Characterization of molecular recognition features, MoRFs, and their binding partners. J. Proteome Res., 2007, 6, 2351-2366.
65. Demarest S.J.; Martinez-Yamout, M.; Chung, J.; Chen, H.; Xu, W.; Dyson, H.J.; Evans, R.M.; Wright, P.E. Mutual synergistic folding in recruitment of CBP/p300 by p 160 nuclear receptor coactivators. Nature, 2002, 415, 549-553.
66. Dosztanyi, Z.; Chen, J.; Dunker, A,K.; Simon, I.; Tompa, P. Disorder and sequence repeats in hub proteins and their implications for network evolution. J. Proteome Res., 2006, 5, 2985-2995.
67. Patil, A.; Nakamura, H. Disordered domains and high surface charge confer hubs with the ability to interact with multiple proteins in interaction networks. FEBS Lett., 2006, 580, 2041-2045.
68. Hershey, P.E.; McWhirter, S.M.; Gross, J.D.; Wagner, G.; Alber, T.; Sachs, A.B. The Cap-binding protein eIF4E promotes folding of a functional domain of yeast translation initiation factor eIF4G1. J Biol. Chem., 1999, 274, 21297-21304.
69. Chi, S.W.; Lee, S.H.; Kim, D.H.; Ahn, M.J.; Kim, J.S.; Woo, J.Y.; Torizawa, T.; Kainosho, M.; Han, K.H. Structural details on mdm2-p53 interaction. J. Biol. Chem., 2005, 280, 38795-38802.
70. Solt, I.; Magyar, C.; Simon, I.; Tompa, P.; FuXreiter, M. Phosphorylation-induced transient intrinsic structure in the kinase-inducible domain of CREB facilitates its recognition by the KIX domain of CBP. Proteins, 2006, 64, 749-757.
71. Takeuchi, K.; Wagner, G. NMR studies of protein interactions. Curr. Opin. Struct. Biol., 2006, 16, 109-117.
72. Iakoucheva, L.M.; Radivojac, P.; Brown, C.J.; O'Connor, T.R.; Sikes, J.G.; Obradovic, Z.; Dunker, A.K. The importance of intrinsic disorder for protein phosphorytation. Nucleic Acids Res., 2004, 32, 1037-1049.
73. Finerty, P.J., Jr.; Mittermaier, A.K.; Muhandiram, R.; Kay, L.E.; Forman-Kay, J.D. NMR dynamics-derived insights into the binding properties of a peptide interacting with an SH2 domain. Biochemistry, 2005, 44, 694-703.
74. Borg, M.; Mittag, T.; Pawson, T,; Tyers, M.; Forman-Kay, J.D.; Chan, H.S. Polyelectrostatic interactions of disordered ligands suggest a physical basis for ultrasensitivity. Proc. Natl. Acad. Sci. U. S. A., 2007, 104, 9650-9655.
75. Bamm, V.V.; Ahmed, M.A.; Ladizhansky, V.; Harauz, G. Purification and spectroscopic characterization of the recombinant BG21 isoform of murine golli myelin basic protein. J. Neurosci. Res., 2007, 85, 272-284.
76. Ahmed, M.A.; Bamm, V.V.; Hmuz, G.; Ladizhansky, V. The BG21 isoform of Golli myelin basic protein is intrinsically disordered with a highly flexible amino-terminal domain. Biochemistry, 2007, 46, 9700-9712.
77. Moscarello, M.A.; Gagnon, J.; Wood, D.D.; Anthony, J.; Epand, R. Conformational flexibility of a myelin protein, Biochemistry, 1973, 12, 3402-3406.
78. Dyer, C.A.; Philibotte, T.M.; Wolf, M.K.; Billings-Gagliardi, S. Myelin basic protein mediates extraceltular signals that regulate microtubule stability in oligodendrocyte membrane sheets. J. Neurosci. Res., 1994, 39, 97-107.
79. Dyer, C.A. (1997) in Cell biology and pathology of myelin: evolving biological concepts and therapeutic approaches., eds. Juurlink, B. H. J., Devon, R. M., Doucette, J. R., Nazarali, A. J., Schreyer, D. J., and Verge, V. M. K. (New York, Plenum Press), pp. 69-74.
80. Campagnoni, A.T.; Skoff, R.P. The pathobiology of myelin mutants reveal novel biological functions of the MBP and PLP genes. Brain Parhol., 2001, 11, 74-91.
81. DeBruin, L.S.; Haines, J.D.; Wellhauser, L.A.; Radeva, G.; Schonmann, V.; Bienzle, D.; Harauz, G. Developmental partition-ing of myelin basic protein into membrane microdomains. J. Neurosci. Res., 2005, 80, 211-225.
82. Harauz, G.; Musse, A.A.; Gao, W.; Boggs, J.M. MBP as a "PIP2-modulin: New biological functions for an old CNS protein. J. Neurochem., 2008, 104 (Supplement 1), 19.
83. Harauz, G.; Ishiyama, N.; Bates, I.R. Analogous structural motifs in myelin basic protein and in MARCKS. Mol. Cell. Biochem., 2000, 209, 155-163.
84. Ishiyama, N.; Bates, I.R.; Hill, C.M.D.; Wood, D.D.; Matharu, P.; Viner, N.J.; Moscarello, M.A.; Harauz, G. The effects of deimination of myelin basic protein on structures formed by its interaction with phosphoinositide-containing lipid monolayers. J Struct. Biol., 2001, 136, 30-45.
85. Boggs, J.M.; Moscarello, M.A. Effect of basic protein from human central nervous system myelin on lipid bilayer structure. J Membr. Biol., 1978, 39, 75-96.
86. Sedzik, J.; Blaurock, A.E.; Höchli, M. Lipid/myelin basic protein multilayers: a model for the cytoplasmic space in central nervous system myehn. J. Mol. Biol., 1984, 174, 385-409.
87. Zhong, L.; Bamm, V.V.; Ahmed, MA.; Harauz, G.; Ladizhansky, V. Solid-state NMR spectroscopy of 18.5 kDa myelin basic protein reconstituted with lipid vesicles: spectroscopic characterisation and spectral assignments of solvent-exposed protein fragments. Biochim. Biophys. Acta (Biomembranes), 2007, 1768, 3193-3205.
88. Bates, I.R.; Boggs, J.M.; Feix, J.B.; Harauz, G. Membrane-anchoring and charge effects in the interaction of myelin basic protein with lipid bilayers studied by site-directed spin labeling. J. Biol. Chem., 2003, 278, 29041-29047.
89. Bates, I.R.; Feix, J.B.; Boggs, J.M.; Harauz, G. An immunodominant epitope of myelin basic protein is an amphipathic alpha-helix. J. Biol. Chem., 2004, 279, 5757-5764.
90. Musse, A.A.; Boggs, J.M.; Harauz, G. Deimination of membrane-bound myelin basic protein in multiple sclerosis exposes an immunodominant epitope. Proc. Natl. Acad. Sci. U. S. A., 2006, 103, 4422-4427.
91. Feix, J. B.; Klug, C. S. (1998) in Spin Labeling: The Next Millenium, ed. Berliner, X. (Plenum, New York), pp. 251-281.
92. Fanucci, G.E.; Cafiso, D.S. Recent advances and applications of site-directed spin labeling. Curr. Opin. Struct. Biol., 2006, 16, 644-653.
93. Biswas, R.; Kuhne, H.; Brudvig, G.W.; Gopalan, V. Use of EPR spectroscopy to study macromolecular structure and function. Sci. Prog., 2001, 84, 45-67.
94. Li, X.; Romero, P.; Rani, M.; Dunker, A.K.; Obradovic, Z. Predicting protein disorder for N-, C-, and internal regions. Genome Inform. Ser. Workshop Genome Inform., 1999, 10, 30-40.
95. Romero, P.; Obradovic, Z.; Li, X.; Garner, E.C.; Brown, C.J.; Dunker, A.K. Sequence complexity of disordered protein. Proteins, 2001, 42, 38-48.
96. Gaboriaud, C.; Bissery, V.; Benchetrit, T.; Momon, J.P. Hydrophobic cluster analysis: an efficient new way to compare and analyse amino acid sequences. FEBS Lett., 1987, 224, 149-155.
97. Collins, M.O.; Yu, L.; Campuzano, I.; Grant, S.G.; Choudhary, J.S. Phosphoproteomic analysis of the mouse brain cytosol reveals a predominance of protein phosphorylation in regions of intrinsic sequence disorder. Mol. Cell Proteornics, 2008, 7, 1331-1348.
98. Sospedra, M.; Martin, R. Immunology of multiple sclerosis. Annu. Rev. Inummol., 2005, 23, 683-747.
99. Farès, C.; Libich, D.S.; Harauz, G. Solution NMR structure of an immunodominant epitope of myelin basic protein. Conformational dependence on environment of an intrinsically unstructured protein, FEBS J., 2006, 273, 601-614.
100. Tselios, T; Probert, L.; Kolhas, G.; Matsoukas, E.; Roumehoti, P.; Alexopoulos, K.; Moore, G.J.; Matsoukas, J. Design and synthesis of small semi-mimetic peptides with immunomodulatory activity based on myelin basic protein (MBP). Amino Acids, 1998, 14, 333-341.
101. Tselios, T.; Probert, L.; Daliani, L; Matsoukas, E.; Troganis, A.; Gerothanassis, I.P.; Mavromoustakos, T.; Moore, G.J.; Matsoukas, J.M. Design and synthesis of a potent cyclic analogue of the myelin basic protein epitope MBP72-85: importance of the Ala81 carboxyl group and of a cyclic conformation for induction of experimental allergic encephalomyelitis. J. Med. Chem., 1999, 42, 1170-1177.
102. Warren, K.G.; Catz, I. Kinetic profiles of cerebrospinal fluid anti-MBP in response to intravenous MBP synthetic peptide DENP(85)VVHFFKNIVTP(96)RT in multiple sclerosis patients. Mult. Scler., 2000, 6, 300-311.
103. Tselios, T.; Daliani, I.; Deraos, S.; Thymianou, S.; Matsoukas, E.; Troganis, A.; Gerothanassis, L; Mouzaki, A.; Mavromoustakos, T.; Probert, L.; Matsoukas J. Treatment of experimental allergic encephalomyelitis (EAE) by a.rationally designed cyclic analogue of myelin basic protein (MBP) epitope 72-85. Bioorg. Med. Chem. Lett., 2000, 10, 2713-2717.
104. Tselios, T.; Daliani, I.; Probert, L.; Deraos, S.; Matsoukas, E.; Roy, S.; Pires, J.; Moore, G.; Matsoukas, J. Treatment of experimental allergic encephalomyelitis (EAE) induced by guinea pig myelin basic protein epitope 72-85 with a human MBP(87-99) analogue and effects of cyclic peptides. Bioorg. Med. Chem., 2000, 8, 1903-1909.
105. Tselios, T.; Apostolopoulos, V.; Daliani, I.; Deraos, S.; Grdadolnik, S.; Mavromoustakos, T.; Melachrinou, M.; Thymianou, S.; Probert, L.; Mouzaki, A.; Matsoukas J. Antagonistic effects of human cyclic MBP(87-99) altered peptide ligands in experimental allergic encephalomyelitis and human T-cell proliferation. J. Med. Chem., 2002, 45, 275-283.
106. Mouzaki, A.; Tselios, T.; Papathanassopoulos, P.; Matsoukas, I.; Chatzantoni, K. Immunotherapy for multiple sclerosis: basic insights for new clinical strategies. Curr. Neurovasc. Res., 2004, 1, 325-340.
107. Tzakos, A.G.; Fuchs, P.; Van Nuland, N.A.; Troganis, A.; Tselios, T.; Deraos, S.; Matsoukas, J.; Gerothanassis, I.P.; Bonvin, A.M. NMR and molecular dynamics studies of an autoimmune myelin basic protein peptide and its antagonist: structural implications for the MHC II (I-Au)-peptide complex from docking calculations. Eur. J. Biochem., 2004, 271, 3399-3413.
108. Matsoukas, J.; Apostolopoulos, V.; Kalbacher, H.; Papini, A.M.; Tselios, T.; Chatzantoni, K.; Biagioli, T.; Lolli, F.; Deraos, S.; Papathanassopoulos, P.; Troganis, A.; Mantzourani, E.; Mavromoustakos, T.; Mouzaki, A. Design and synthesis of a novel potent myelin basic protein epitope 87-99 cyclic analogue: enhanced stability and biological properties of mimics render them a potentially new class of immunomodulators. J. Med. Chem., 2005, 48, 1470-1480.
109. Warren, K.G.; Catz, I.; Ferenczi, L.Z.; Krantz, M.J. Intravenous synthetic peptide MBP8298 delayed disease progression in an HLA Class II-defined cohort of patients with progressive multiple sclerosis: results of a 24-month double-blind placebo-controlled clinical trial and 5 years of follow-up treatment. Eur. J. Neurol., 2006, 13, 887-895.
110. Darlington, C. MBP-8299, a synthetic peptide analog of myelin basic protein for the treatment of multiple sclerosis. Curr. Opin. Mol. Ther., 2007, 9, 398-402.
111. Macosko, J.C.; Kim, C.H.; Shin, Y.K. The membrane topology of the fusion peptide region of influenza hemagglutinin determined by spin-labeling EPR. J. Mol. Biol., 1997, 267, 1139-1148.
112. Cajal, Y.; Boggs, J.M.; Jain, M.K. Salt-triggered intermembrane exchange of phospholipids and hemifusion by myelin basic protein. Biochemistry, 1997, 36, 2566-2576.
113. Fernandez-Vidal, M.; Jayasinghe, S.; Ladokhin, A.S.; White, S.H. Folding amphipathic helices into membranes: amphiphilicity trumps hydrophobicity. J. Mol. Blol., 2007, 370, 459-470.
114. Strandberg, E.; Killian, J.A. Snorkeling of lysine side chains in transmembrane helices: how easy can it get? FEBS Lett., 2003, 544, 69-73.
115. Wishart, D.S.; Bigam, C.G.; Holm, A.; Hodges, R.S.; Sykes, B.D. 1H, 13C and 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR, 1995, 5, 67-81.
116. Wishart, D.S.; Bigam, C.G.; Yao, J.; Abildgaard, F.; Dyson, H.J.; Oldfield, E.; Markley, J.L.; Sykes, B.D. 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR, 1995, 6, 135-140.
117. Wishart, D.S.; Nip, A.M. Protein chemical shift analysis: a practical guide. Biochem. Cell Biol., 1998, 76, 153-163.
118. Bates, I.R.; Harauz, G. Molecular dynamics exposes □-helices in myelin basic protein. J. Mol. Mod., 2003, 9, 290-297.
119. Erickson, A.K.; Payne, D.M.; Martino, P.A.; Rossomando, A.J.; Shabanowitz, J.; Weber, M.J.; Hunt, D.F.; Sturgill, T.W. Identification by mass spectrometry of threonine 97 in bovine myelin basic protein as a specific phosphorylation site for mitogen-activated protein kinase. J. Biol. Chem., 1990, 265, 19728-19735.
120. Hirschberg, D.; Radmark, O.; Jornvall, H.; Bergman, T. Thr94 in bovine myelin basic protein is a second phosphorylation site for 42-kDa mitogen-activated protein kinase (ERK2). J. Protein Chem., 2003, 22, 177-181.
121. Persaud, R.; Fraser, P.; Wood, D.D.; Moscarello, M.A. The glycosylation of human myelin basic protein at threonines 95 and 98 occurs sequentially. Biochim. Biophys. Acta, 1988, 966, 357-361.
122. Li, S.S. Specificity and versatility of SH3 and other proline-recognition domains: structural basis and implications for cellular signal transduction. Biochem. J., 2005, 390, 641-653.
123. Rath, A.; Davidson, A.R.; Deber, C.M. The structure of "unstructured" regions in peptides and proteins: role of the polyproline II helix in protein folding and recognition. Biopolymers, 2005, 80, 179-185.
124. Chellgren, B.W.; Creamer, T.P. Short sequences of non-proline residues can adopt the polyproline II helical conformation. Biochemistry, 2004, 43, 5864-5869.
125. Bochicchio, B.; Tamburro, A.M.) Polyproline II structure in proteins: identification by chiroptical spectroscopies, stability, and functions. Chirality, 2002, 14, 782-792.
126. Tiffany, M.L.; Krimm, S. Circular dichroism of poly-L-proline in an unordered conformation. Biopolymers, 1968, 6, 1767-1770.
127. Rucker, A.L.; Creamer, T.P. Polyproline II helical structure in protein unfolded states: lysine peptides revisited. Protein Sci., 2002, 11, 980-985.
128. Ruzza, P.; Calderan, A.; Guiotto, A.; Osler, A.; Borin, G. Tat cell-penetrating peptide has the characteristics of a poly(proline) II helix in aqueous solution and in SDS micelles. J. Pept. Sci., 2004, 10, 423-426.
129. Deibler, G.E.; Stone, A.L.; Kies, M.W. Role of phosphorylation in conformational adaptability of bovine myelin basic protein. Proteins, 1990, 7, 32-40.
130. Yang, S.T.; Jeon, J.H.; Kim, Y.; Shin, S.Y.; Hahm, K.S.; Kim, J.I. Possible role of a PXXP central hinge in the antibacterial activity and membrane interaction of PMAP-23, a member of cathelicidin family. Biochemistry, 2006, 45, 1775-1784.
131. Yang, S.T.; Lee, J.Y.; Kim, H.J.; Eu, Y.J.; Shin, S.Y.; Hahm, K.S.; Kim, J.I. Contribution of a central proline in model amphipathic alpha-helical peptides to self-association, interaction with phospholipids, and antimicrobial mode of action. FEBS J., 2006, 273, 4040-4054.
132. Nygaard, E.; Mendz, G.L.; Moore, W.J.; Martenson, R.E. NMR of a peptic peptide spanning the triprolyl sequence in myelin basic protein. Biochemistry, 1984, 23, 4003-4010.
133. Fraser, P.E.; Deber, C.M. Structure and function of the proline-rich region of myelin basic protein. Biochemistry, 1985, 24, 4593-4598.
134. Dyson, H.J.; Wright, P.E. Unfolded proteins and protein folding studied by NMR. Chem. Rev., 2004, 104, 3607-3622.
135. Wishart, D.S.; Sykes, B.D. Chemical shifts as a tool for structure determination. Methods Enzymol., 1994, 239, 363-392.
136. Schwarzinger, S.; Kroon, G.J.; Foss, T.R.; Chung, J.; Wright, P.E.; Dyson, H.J. Sequence-dependent correction of random coil NMR chemical shifts. J. Am. Chem. Soc., 2001, 123, 2970-2978.
137. Lam, S.L.; Hsu, V.L. NMR identification of left-handed polyproline type II helices. Biopolymers, 2003, 69, 270-281.
138. Karplus, S.; Karplus, M. Nuclear magnetic resonance determination of the angle psi in peptides. Proc. Natl. Acad. Sci. U.S.A., 1972, 69, 3204-3206.
139. Rule, G. S.; Hitchens, T. K. in Fundamentals of protein NMR spectroscopy, Springer, Dordrecht, The Netherlands, 2006.
140. Vuister, G.W.; Delaglio, F.; Bax, A. The use of 1JC alpha H alpha coupling constants as a probe for protein backbone conformation. J. Biomol. NMR, 1993, 3, 6740.
141. Vuister, G.W.; Bax, A. Measurement of two-bond JCOH alpha coupling constants in proteins uniformly enriched with 13C. J. Biomol. NMR, 1992, 2, 401-405.
142. Libich, D.S.; Robertson, V.J.; Monette, M.M.; Harauz, G. Backbone resonance assignments of the 18.5 kDa isoform of murine myelin basic protein (MBP) J. Biomol. NMR, 2004, 29, 545-546.
143. Libich, D.S.; Monette, M.M.; Robertson, V.J.; Harauz, G. NMR assignment of an intrinsically disordered protein under physiological conditions: the 18.5 kDa isoform of myelin basic protein. Biomolecular NMR Assignments, 2007, 1, 61-63.
144. Pawson, T.; Scott, J.D. Protein phosphorylation in signaling - 50 years and counting. Trends Biochem Sci., 2005, 30, 286-290.
145. Jones, L.S.; Yazzie, B.; Middaugh, C.R. Polyanions and the proteome. Mol. Cell. Proteomics, 2004, 3, 746-769.
146. Woods, A.S. The mighty arginine, the stable quaternary amines, the powerful aromatics, and the aggressive phosphate: their role in the noncovalent minuet. J. Proteome Res., 2004, 3, 478-484.
147. Jackson, S.N.; Wang, H.Y.; Yergey, A.; Woods, A.S. Phosphate stabilization of intermolecular interactions. J. Proteome Res., 2006, 5, 122-126.
148. Salazar, C.; Höfer, T. Versatile regulation of multisite protein phosphorylation by the order of phosphate processing and protein-protein interactions. FEBS J., 2007, 274, 1046-1061.
149. Serber, Z.; Ferrell, J.E. Jr. Tuning bulk electrostatics to regulate protein function. Cell, 2007, 128, 441-444.
150. Muntane, G.; Dalfo, E.; Martinez, A.; Ferrer, I. Phosphorylation of tau and alpha-synuclein in synaptic-enriched fractions of the frontal cortex in Alzheimer's disease, and in Parkinson's disease and related alpha-synucleinopathies. Neuroscience, 2008, 152, 913-923.
151. Marta, C.B.; Taylor, C.M.; Coetzee, T.; Kim, T.; Winkler, S.; Bansal, R.; Pfeiffer, S.E. Antibody cross-linking of myelin oligodendrocyte glycoprotein leads to its rapid repartitioning into detergent-insoluble fractions, and altered protein phosphorylation and cell morphology. J. Neurosci., 2003, 23, 5461-5471.
152. Marta, C.B.; Montano, M.B.; Taylor, C.M.; Taylor, A.L.; Bansal, R.; Pfeiffer, S.E. Signaling cascades activated upon antibody cross-linking of myelin oligodendrocyte glycoprotein: potential iniplications for multiple sclerosis. J. Biol. Chem., 2005, 280, 8985-8993.
153. Stariha, R.L.; Kim, S.U. Protein kinase C and mitogen-activated protein kinase signalling in oligodendrocytes. Microsc. Res. Tech., 2001, 52, 680-688.
154. Ramwani, J.J.; Epand, R.M.; Moscarello, M.A. Secondary structure of charge isomers of myelin basic protein before and after phosphorylation. Biochemistry, 1989, 28, 6538-6543.
155. Ramwani, J.; Moscarello, M.A. Phosphorylation of charge isomers (components) of human myelin basic protein: identification of phosphorylated sites. J. Neurochem., 1990, 55, 1703-1710.
156. Boggs, J.M.; Yip, P.M.; Rangaraj, G.; Jo, E. Effect of posttranslational modifications to myelin basic protein on its ability to aggregate acidic lipid vesicles. Biochemistry, 1997, 36, 5065-5071.
157. Ulmer, J.B.; Braun, P.E. In vivo phosphorylation of myelin basic proteins in developing mouse brain: evidence that phosphorylation is an early event in myelin formation. Dev. Neurosci., 1983, 6, 345-355.
158. Vartanian, T.; Szuchet, S.; Dawson, G.; Campagnoni, A.T. Oligodendrocyte adhesion activates protein kinase C-mediated phosphorylation of myelin basic protein. Science, 1986, 234, 1395-1398.
159. Stariha, R.L.; Kikuchi, S.; Siow, Y.L.; Pelech, S.L.; Kim, M.; Kim, S.U. Role of extracellular signal-regulated protein kinases 1 and 2 in oligodendroglial process extension. J. Neurochem., 1997, 68, 945-953.
160. Campagnoni, A.T. Molecular biology of myelin proteins from the central nervous system. J. Neurochem., 1988, 51, 1-14.
161. Dyer, C.A. The structure and function of myelin: from inert membrane to perfusion pump. Neurochem. Res., 2002, 27, 1279-1292.
162. Atkins, C.M.; Yon, M.; Groome, N.P.; Sweatt, J.D. Regulation of myelin basic protein phosphorylation by mitogen-activated protein kinase during increased action potential firing in the hippocampus. J. Neurochem., 1999, 73, 1090-1097.
163. DeBruin, L.S.; Haines, J.D.; Bienzle, D.; Harauz, G. Partitioning of myelin basic protein into membrane microdomains in a spontaneously demyelinating mouse model for multiple sclerosis. Biochem. Cell Biol., 2006, 84, 993-1005.
164. DeBruin, L.S.; Harauz, G. White matter rafting - membrane microdomains in myelin. Neurochem. Res., 2007, 32, 213-228.
165. Tholey, A.; Lindemann, A.; Kinzel, V.; Reed, J. Direct effects of phosphorylation on the preferred backbone conformation of peptides: a nuclear magnetic resonance study. Biophys. J., 1999, 76, 76-87.
166. Andrew, C.D.; Warwicker, J.; Jones, G.R.; Doig, A.J. Effect of phosphorylation on alpha-helix stability as a function of position. Biochemistry, 2002, 41, 1897-1905.
167. Wulf, G.; Finn, G.; Suizu, F.; Lu, K.P. Phosphorylation-specific prolyl isomerization: is there an underlying theme? Nat. Cell Biol., 2005, 7, 435-441.
168. Liou, Y.C.; Sun, A.; Ryo, A.; Zhou, X.Z.; Yu, Z.X.; Huang, H.K.; Uchida, T.; Bronson, R.; Bing, G.; Li, X.; Hunter, T.; Lu, K.P. Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature, 2003, 424, 556-561.
169. Lu, K.P.; Liou, Y.C.; Vincent, I. Proline-directed phosphorylation and isomerization in mitotic regulation and in Alzheimer's Disease. Bioessays, 2003, 25, 174-181.
170. Libich, D.S.; Harauz, G. Interactions of the 18.5 kDa isoform of myelin basic protein with Ca2+-calmodulin: in vitro studies using fluorescence microscopy and spectroscopy. Biochem. Cell Biol., 2002, 80, 395-406.
171. Libich, D.S.; Harauz, G. Interactions of the 18.5 kDa isoform of myelin basic protein with Ca2+-calmodulin - in vitro studies using gel shift assays. Mol. Cell. Biochem., 2002, 241, 45-52.
172. Libich, D.S.; Hill, C.M.; Haines, J.D.; Harauz, G. Myelin basic protein has multiple calmodulin-binding sites. Biochem. Biophys. Res. Commun., 2003, 308, 313-319.
173. Libich, D.S.; Hill, C.M.; Bates, I.R.; Hallett, F.R.; Armstrong, S.; Siemiarczuk, A.; Harauz, G. Interaction of the 18.5-kD isoform of myelin basic protein with Ca2+ -calmodulin: effects of deimination assessed by intrinsic Trp fluorescence spectroscopy, dynamic light scattering, and circular dichroism. Protein Sci., 2003, 12, 1507-1521.
174. Berggard, T.; Arrigoni, G.; Olsson, O.; Fex, M.; Linse, S.; James, P. 140 mouse brain proteins identified by Ca2+-calmodulin affinity chromatography and tandem mass spectrometry. J. Proteome Res., 2006, 5, 669-687.
175. Zhang, Z.; Ottens, A.K.; Golden, E.C.; Hayes, R.L.; Wang, K.K.W. Using calmodulin-affinity capture to study the rat brain calmodulin proteome and its vulnerability to calpain and caspase proteolysis. Calcium Binding Proteins, 2006, 1, 125-129.
176. Polverini, E.; Boggs, J.M.; Bates, I.R.; Harauz, G.; Cavatorta, P. Electron paramagnetic resonance spectroscopy and molecular modelling of the interaction of myelin basic protein (MBP) with calmodulin (CaM)-diversity and conformational adaptability of MBP CaM-targets. J. Struct. Biol., 2004, 148, 353-369.
177. Fuxreiter, M.; Simon, I.; Friedrich, P.; Tompa, P. Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. J. Mol. Biol., 2004, 338, 1015-1026.
178. Mészáros, B.; Tompa, P.; Simon, I.; Dosztányi, Z. Molecular principles of the interactions of disordered proteins. J. Mol. Biol., 2007, 372, 549-561.
179. Porumb, T.; Crivici, A.; Blackshear, P.J.; Ikura, M. Calcium binding and conformational properties of calmodulin complexed with peptides derived from myristoylated alanine-rich C kinase substrate (MARCKS) and MARCKS-related protein (MRP). Eur. Biophys. J., 1997, 25, 239-247.
180. Hoeflich, K.P.; Ikura, M. Calmodulin in action: diversity in target recognition and activation mechanisms. Cell, 2002, 108, 739-742.
181. Permyakov, S.E.; Millett, I.S.; Doniach, S.; Permyakov, E.A.; Uversky, V.N. Natively unfolded C-terminal domain of caldesmon remains substantially unstructured after the effective binding to calmodulin. Proteins, 2003, 53, 855-862.
182. Radivojac, P.; Vucetic, S.; O'Connor, T.R.; Uversky, V.N.; Obradovic, Z.; Dunker, A.K. Calmodulin signaling: analysis and prediction of a disorder-dependent molecular recognition. Proteins, 2006, 63, 398-410.
183. Baker, J.M.; Hudson, R.P.; Kanelis, V.; Choy, W.Y.; Thibodeau, P.H.; Thomas, P.J.; Forman-Kay, J.D. CFTR regulatory region interacts with NBD1 predominantly via multiple transient helices. Nat. Struct. Mol. Biol., 2007, 14, 738-745.
184. Hill, C.M.D.; Haines, J.D.; Antler, C.E.; Bates, I.R.; Libich, D.S.; Harauz, G. Terminal deletion mutants of myelin basic protein: new insights into self-association and phospholipid interactions. Micron, 2003, 34, 25-37.
185. Hu, Y.; Doudevski, I.; Wood, D.; Moscarello, M.; Husted, C.; Genain, C.; Zasadzinski, J.A., Israelachvili, J. Synergistic interactions of lipids and myelin basic protein. Proc. Natl. Acad. Sci. U.S.A., 2004, 101, 13466-13471.
186. Rispoli, P.; Carzino, R.; Svaldo-Lanero, T.; Relini, A.; Cavalleri, O.; Fasano, A.; Liuzzi, G.M.; Carlone, G.; Riccio, P.; Ghozzi, A.; Rolandi, R. A thermodynamic and structural study of myelin basic protein in lipid membrane models. Biophys. J., 2007, 93, 1999-2010.
187. Rosetti, C.M.; Maggio, B. Protein-induced surface structuring in myelin membrane monolayers. Biophys. J., 2007, 93, 4254-4267.
188. Hu, Y.; Israelachvili, J. Lateral reorganization of myelin lipid domains by myelin basic protein studied at the air-water interface. Colloids Surf. B Biointerfaces, 2007, 62, 22-30.
189. Franklin, R.J. Why does remyelination fail in multiple sclerosis? Nat. Rev. Neurosci., 2002, 3, 705-714.
190. Hegedus, T.; Serohijos, A.W.; Dokholyan, N.V.; He, L.; Riordan, J.R. Computational studies reveal phosphory-lation-dependent changes in the unstructured R domain of CFTR. J. Mol. Biol., 2008, 378, 1052-1063.
191. Karthigasan, J.; Inouye, H.; Kirschner, D.A. Implications of the sequence similarities between tau and myelin basic protein. Med. Hypotheses, 1995, 45, 235-240.
192. Greer, J.M.; Lees, M.B. Myelin proteolipid protein - the first 50 years. Int. J. Biochem. Cell Biol., 2002, 34, 211-215.
193. Duncan, I.D. The PLP mutants from mouse to man. J. Neurol. Sci., 2005, 228, 204-205.
194. Agnati, L.F.; Zunarelli, E.; Genedani, S.; Fuxe, K. On the existence of a global molecular network enmeshing the whole central nervous system: physiological and pathological impli-cations. Curr. Protein Pept. Sci., 2006, 7, 3-15.
195. Uversky, V.N. Neuropathology, biochemistry, and biophy-sics of alpha-synuclein aggregation. J. Neurochem., 2007, 103, 17-37.
196. Cheng, Y.; LeGall, T.; Oldfield, C.J.; Dunker, A.K.; Uversky, V.N. Abundance of intrinsic disorder in protein associated with cardiovascular disease. Biochemistry, 2006, 45, 10448-10460.
197. Musse, A.A.; Harauz, G. Molecular "negativity" may underlie multiple sclerosis: role of the myelin basic protein family in the pathogenesis of MS. Int. Rev. Neurobiol., 2007, 79, 149-172.
198. Dohm, C.P.; Kermer, P.; Bahr, M. Aggregopathy in neurodegenerative diseases: Mechanisms and therapeutic impli-cation. Neurodegener. Dis., 2008, 5, 321-338.
199. Soto, C.; Estrada, L.D. Protein misfolding and neurodegeneration. Arch. Neurol., 2008, 65, 184-189.
200. Doyle, H.A.; Mamula, M.J. Posttranslational protein modifications: new flavors in the menu of autoantigens. Curr. Opin. Rheumatol., 2002, 14, 244-249.