Cytoplasmic domain of human myelin protein zero likely folded as β-structure in compact myelin

Biophysical Journal

Volumn 92, Issue 5, 2007, Pages 1585-1597

  Luo, XiaoYang ^a   Sharma, Deepak ^a   Inouye, Hideyo ^a   Lee, Daniel ^a   Avila, Robin L ^a   Salmona, Mario ^b   Kirschner, Daniel A ^a  

^a BOSTON COLLEGE   (United States)

^b MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN PROTEIN; MYELIN PROTEIN ZERO; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CENTRAL NERVOUS SYSTEM; CIRCULAR DICHROISM; CRYSTALLOGRAPHY; CYTOPLASM; FLUORESCENCE SPECTROSCOPY; LIPID BILAYER; MYELIN SHEATH; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE;

EID: 33847786718     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.094722     Document Type: Article

References (74)

1. Greenfield, S., S. Brostoff, E. H. Eylar, and P. Morell. 1973. Protein composition of myelin of the peripheral nervous system. J. Neurochem. 20:1207-1216.
2. Lemke, G., E. Lamar, and J. Patterson. 1988. Isolation and analysis of the gene encoding peripheral myelin protein zero. Neuron. 1:73-83.
3. Uyemura, K., M. Suzuki, Y. Sakamoto, and S. Tanaka. 1987. Structure of P0 protein: homology to immunoglobulin superfamily. Biomed. Res. 8:353-357.
4. Uyemura, K., Y. Takeda, H. Asou, and K. Hayasaka. 1994. Neural cell adhesion proteins and neurological diseases. J. Biochem. (Tokyo). 116:1187-1192.
5. Kirschner, D. A., and A. L. Ganser. 1980. Compact myelin exists in the absence of basic protein in the shiverer mutant mouse. Nature. 283:207-210.
6. Warner, L. E., M. J. Hilz, S. H. Appel, J. M. Killian, E. H. Kolodry, G. Karpati, S. Carpenter, G. V. Watters, C. Wheeler, D. Witt, A. Bodell, E. Nelis, C. Van Broeckhoven, and J. R. Lupski. 1996. Clinical phenotypes of different MPZ (P0) mutations may include Charcot-Marie-Tooth type 1B, Dejerine-Sottas, and congenital hypomyelination. Neuron. 17:451-460.
7. Ninham, B. W., and V. A. Parsegian. 1971. Electrostatic potential between surfaces bearing ionizable groups in ionic equilibrium with physiologic saline solution. J. Theor. Biol. 31:405-428.
8. Verwey, E. J. W., and J. T. G. Overbeek. 1948. Theory of the Stability of Lyophobic Colloids. Elsevier, New York.
9. Inouye, H., J. Karthigasan, and D. A. Kirschner. 1989. Membrane structure in isolated and intact myelins. Biophys. J. 56:129-137.
10. Shapiro, L., J. P. Doyle, P. Hensley, D. R. Colman, and W. A. Hendrickson. 1996. Crystal structure of the extracellular domain from P0, the major structural protein of peripheral nerve myelin. Neuron. 17:435-449.
11. Inouye, H., and D. A. Kirschner. 1988. Membrane interactions in nerve myelin. I. Determination of surface charge from effects of pH and ionic strength on period. Biophys. J. 53:235-245.
12. Inouye, H., H. Tsuruta, J. Sedzik, K. Uyemura, and D. A. Kirschner. 1999. Tetrameric assembly of full-sequence protein zero myelin glycoprotein by synchrotron x-ray scattering. Biophys. J. 76:423-437.
13. De Gioia, L., C. Selvaggini, E. Ghibaudi, L. Diomede, O. Bugiani, G. Forloni, F. Tagliavini, and M. Salmona. 1994. Conformational polymorphism of the amyloidogenic and neurotoxic peptide homologous to residues 106-126 of the prion protein. J. Biol. Chem. 269:7859-7862.
14. Kodama, M., T. Miyata, and Y. Takaichi. 1993. Calorimetric investigations of phase transitions of sonicated vesicles of dimyristoylphosphatidylcholine. Biochim. Biophys. Acta. 1169:90-97.
15. Sreerama, N., and R. W. Woody. 2004. On the analysis of membrane protein circular dichroism spectra. Protein Sci. 13:100-112.
16. Lakowicz, J. R. 2006. Principles of Fluorescence Spectroscopy. Springer, New York.
17. Raghuraman, H., and A. Chattopadhyay. 2004. Interaction of melittin with membrane cholesterol: a fluorescence approach. Biophys. J. 87:2419-2432.
18. Kruger, R. G., P. Dostal, and D. G. McCafferty. 2004. Development of a high-performance liquid chromatography assay and revision of kinetic parameters for the Staphylococcus aureus sortase transpeptidase SrtA. Anal. Biochem. 326:42-48.
19. Chou, P. Y., and G. D. Fasman. 1974. Prediction of protein conformation. Biochemistry. 13:222-245.
20. Cuff, J. A., M. E. Clamp, A. S. Siddiqui, M. Finlay, and G. J. Barton. 1998. JPred: a consensus secondary structure prediction server. Bioinformatics. 14:892-893.
21. Rost, B., G. Yachdav, and J. Liu. 2004. The PredictProtein server. Nucleic Acids Res. 32:321-326.
22. Berova, N., K. Nakanishi, and R. Woody. 2000. Circular Dichroism: Principles and Applications. Wiley-VCH, New York.
23. Inouye, H., and D. A. Kirschner. 1988. Membrane interactions in nerve myelin. II. Determination of surface charge from biochemical data. Biophys. J. 53:247-260.
24. Ding, Y., and K. R. Brunden. 1994. The cytoplasmic domain of myelin glycoprotein P0 interacts with negatively charged phospholipid bilayers. J. Biol. Chem. 269:10764-10770.
25. Terzi, E., G. Holzemann, and J. Seelig. 1997. Interaction of Alzheimer β-amyloid peptide (1-40) with lipid membranes. Biochemistry. 36:14845-14852.
26. Kakio, A., S. Nishimoto, K. Yanagisawa, Y. Kozutsumi, and K. Matsuzaki. 2002. Interactions of amyloid beta-protein with various gangliosides in raft-like membranes: importance of GM1 ganglioside-bound form as an endogenous seed for Alzheimer amyloid. Biochemistry. 41:7385-7390.
27. Roccatano, D., G. Colombo, M. Fioroni, and A. E. Mark. 2002. Mechanism by which 2,2,2-trifluoroethanol/water mixtures stabilize secondary-structure formation in peptides: a molecular dynamics study. Proc. Natl. Acad. Sci. USA. 99:12179-12184.
28. Terzi, E., G. Holzemann, and J. Seelig. 1994. Reversible random coil-β-sheet transition of the Alzheimer beta-amyloid fragment (25-35). Biochemistry. 33:1345-1350.
29. Choo-Smith, L. P., W. Garzon-Rodriguez, C. G. Glabe, and W. K. Surewicz. 1997. Acceleration of amyloid fibril formation by specific binding of Aβ-(1-40) peptide to ganglioside-containing membrane vesicles. J. Biol. Chem. 272:22987-22990.
30. Kakio, A., S. I. Nishimoto, K. Yanagisawa, Y. Kozutsumi, and K. Matsuzaki. 2001. Cholesterol-dependent formation of GM1 ganglioside-bound amyloid beta-protein, an endogenous seed for Alzheimer amyloid. J. Biol. Chem. 276:24985-24990.
31. Kurganov, B., M. Doh, and N. Arispe. 2004. Aggregation of liposomes induced by the toxic peptides Alzheimer's Aβs, human amylin and prion (106-126): facilitation by membrane-bound GM1 ganglioside. Peptides. 25:217-232.
32. McLaurin, J., D. Yang, C. M. Yip, and P. E. Fraser. 2000. Review: modulating factors in amyloid-beta fibril formation. J. Struct. Biol. 130:259-270.
33. Terzi, E., G. Holzemann, and J. Seelig. 1994. Alzheimer β-amyloid peptide 25-35: electrostatic interactions with phospholipid membranes. Biochemistry. 33:7434-7441.
34. Terzi, E., G. Holzemann, and J. Seelig. 1995. Self-association of beta-amyloid peptide (1-40) in solution and binding to lipid membranes. J. Mol. Biol. 252:633-642.
35. Yanagisawa, K., A. Odaka, N. Suzuki, and Y. Ihara. 1995. GM1 ganglioside-bound amyloid beta-protein (Aβ): a possible form of preamyloid in Alzheimer's disease. Nat. Med. 1:1062-1066.
36. Jayasinghe, S. A., and R. Langen. 2005. Lipid membranes modulate the structure of islet amyloid polypeptide. Biochemistry. 44:12113-12119.
37. Wang, S. S., T. A. Good, and D. L. Rymer. 2005. The influence of phospholipid membranes on bovine calcitonin secondary structure and amyloid formation. Protein Sci. 14:1419-1428.
38. Huang, H. W. 2000. Action of antimicrobial peptides: two-state model. Biochemistry. 39:8347-8352.
39. Mason, R. P., R. F. Jacob, M. F. Walter, P. E. Mason, N. A. Avdulov, S. V. Chochina, U. Igbavboa, and W. G. Wood. 1999. Distribution and fluidizing action of soluble and aggregated amyloid beta-peptide in rat synaptic plasma membranes. J. Biol. Chem. 274:18801-18807.
40. Arispe, N., H. B. Pollard, and E. Rojas. 1993. Giant multilevel cation channels formed by Alzheimer disease amyloid beta-protein [Ab P-(1-40)] in bilayer membranes. Proc. Natl. Acad. Sci. USA. 90:10573-10577.
41. Xu, W., D. Manichella, H. Jiang, J. M. Vallat, J. Lilien, P. Baron, G. Scarlato, J. Kamholz, and M. E. Shy. 2000. Absence of P0 leads to the dysregulation of myelin gene expression and myelin morphogenesis. J. Neurosci. Res. 60:714-724.
42. Bizzozero, O. A., K. Fridal, and A. Pastuszyn. 1994. Identification of the palmitoylation site in rat myelin P0 glycoprotein. J. Neurochem. 62:1163-1171.
43. de Foresta, B., L. Tortech, M. Vincent, and J. Gallay. 2002. Location and dynamics of tryptophan in transmembrane α-helix peptides: a fluorescence and circular dichroism study. Eur. Biophys. J. 31:185-197.
44. Ladokhin, A. S., and S. H. White. 2001. Alphas and taus of tryptophan fluorescence in membranes. Biophys. J. 81:1825-1827.
45. Jensen, M. O., O. G. Mouritsen, and G. H. Peters. 2004. Simulations of a membrane-anchored peptide: structure, dynamics, and influence on bilayer properties. Biophys. J. 86:3556-3575.
46. Johnston, J. M., G. A. Cook, J. M. Tomich, and M. S. Sansom. 2006. Conformation and environment of channel-forming peptides: a simulation study. Biophys. J. 90:1855-1864.
47. Morell, P., and H. Jurevics. 1996. Origin of cholesterol in myelin. Neurochem. Res. 21:463-470.
48. Haines, T. H. 2001. Do sterols reduce proton and sodium leaks through lipid bilayers? Prog. Lipid Res. 40:299-324.
49. Brown, D. A., and E. London. 2000. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275:17221-17224.
50. Erne, B., S. Sansano, M. Frank, and N. Schaeren-Wiemers. 2002. Rafts in adult peripheral nerve myelin contain major structural myelin proteins and myelin and lymphocyte protein (MAL) and CD59 as specific markers. J. Neurochem. 82:550-562.
51. Ji, S. R., Y. Wu, and S. F. Sui. 2002. Cholesterol is an important factor affecting the membrane insertion of β-amyloid peptide (Aβ 1-40), which may potentially inhibit the fibril formation. J. Biol. Chem. 277:6273-6279.
52. Micelli, S., D. Meleleo, V. Picciarelli, and E. Gallucci. 2004. Effect of sterols on β-amyloid peptide (AβP 1-40) channel formation and their properties in planar lipid membranes. Biophys. J. 86:2231-2237.
53. Privat, A., C. Jacque, J.-M. Bourre, P. Dupouey, and N. A. Baumann. 1979. Absence of the major dense line in myelin of the mutant mouse "shiverer". Neurosci. Lett. 12:107-112.
54. MacNaughtan, W., K. A. Snook, E. Caspi, and N. P. Franks. 1985. An x-ray diffraction analysis of oriented lipid multilayers containing basic proteins. Biochim. Biophys. Acta. 818:132-148.
55. Mateu, L., V. Luzzati, Y. London, R. M. Gould, and F. G. Vosseberg. 1973. X-ray diffraction and electron microscope study of the interactions of myelin components. The structure of a lamellar phase with a 150 to 180 Å repeat distance containing basic proteins and acidic lipids. J. Mol. Biol. 75:697-709.
56. Murthy, N. S., D. D. Wood, and M. A. Moscarello. 1984. X-ray scattering studies of a model complex of lipid and basic protein of myelin. Biochim. Biophys. Acta. 769:493-498.
57. Epand, R. M., M. A. Moscarello, B. Zierenberg, and W. J. Vail. 1974. The folded conformation of the encephalitogenic protein of the human brain. Biochemistry. 13:1264-1267.
58. Haas, H., C. L. Oliveira, I. L. Torriani, E. Polverini, A. Fasano, G. Carlone, P. Cavatorta, and P. Riccio. 2004. Small angle x-ray scattering from lipid-bound myelin basic protein in solution. Biophys. J. 86:455-460.
59. Krigbaum, W. R., and T. S. Hsu. 1975. Molecular conformation of bovine A1 basic protein, a coiling macromolecule in aqueous solution. Biochemistry. 14:2542-2546.
60. Beniac, D. R., M. D. Luckevich, G. J. Czarnota, T. A. Tompkins, R. A. Ridsdale, F. P. Ottensmeyer, M. A. Moscarello, and G. Harauz. 1997. Three-dimensional structure of myelin basic protein. I. Reconstruction via angular reconstitution of randomly oriented single particles. J. Biol. Chem. 272:4261-4268.
61. Ridsdale, R. A., D. R. Beniac, T. A. Tompkins, M. A. Moscarello, and G. Harauz. 1997. Three-dimensional structure of myelin basic protein. II. Molecular modeling and considerations of predicted structures in multiple sclerosis. J. Biol. Chem. 272:4269-4275.
62. Martenson, R. E. 1986. Possible hydrophobic region in myelin basic protein consisting of an orthogonally packed beta-sheet. J. Neurochem. 46:1612-1622.
63. Stoner, G. L. 1990. Conservation throughout vertebrate evolution of the predicted beta-strands in myelin basic protein. J. Neurochem. 55:1404-1411.
64. Harauz, G., N. Ishiyama, C. M. Hill, I. R. Bates, D. S. Libich, and C. Fares. 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.
65. Sedzik, J., and D. A. Kirschner. 1992. Is myelin basic protein crystallizable? Neurochem. Res. 17:157-166.
66. Bates, I. R., P. Matharu, N. Ishiyama, D. Rochon, D. D. Wood, E. Polverini, M. A. Moscarello, N. J. Viner, and G. Harauz. 2000. Characterization of a recombinant murine 18.5-kDa myelin basic protein. Protein Expr. Purif. 20:285-299.
67. Polverini, E., A. Fasano, F. Zito, P. Riccio, and P. Cavatorta. 1999. Conformation of bovine myelin basic protein purified with bound lipids. Eur. Biophys. J. 28:351-355.
68. Sreerama, N., S. Y. Venyaminov, and R. W. Woody. 2000. Estimation of protein secondary structure from circular dichroism spectra: inclusion of denatured proteins with native proteins in the analysis. Anal. Biochem. 287:243-251.
69. Sreerama, N., and R. W. Woody. 2000. Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287:252-260.
70. Sreerama, N., and R. W. Woody. 2004. Computation and analysis of protein circular dichroism spectra. Methods Enzymol. 383:318-351.
71. Kelley, L. A., R. M. MacCallum, and M. J. Sternberg. 2000. Enhanced genome annotation using structural profiles in the program 3D-PSSM. J. Mol. Biol. 299:499-520.
72. Oosawa, F., and S. Asakura. 1975. Thermodynamics of the Polymerization of Protein. Academic Press, New York.
73. Inouye, H., and D. A. Kirschner. 2000. A β-fibrillogenesis: kinetic parameters for fibril formation from Congo red binding. J. Struct. Biol. 130:123-129.
74. DeLano, W. L. 2002. The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA.