Peripheral myelin of Xenopus laevis: Role of electrostatic and hydrophobic interactions in membrane compaction

Journal of Structural Biology

Volumn 162, Issue 1, 2008, Pages 170-183

  Luo, XiaoYang ^a   Cerullo, Jana ^a   Dawli, Tamara ^a   Priest, Christina ^a   Haddadin, Zaid ^a   Kim, Angela ^a   Inouye, Hideyo ^a   Suffoletto, Brian P ^a   Avila, Robin L ^a   Lees, Jonathan P B ^a   Sharma, Deepak ^a   Xie, Bo ^b   Costello, Catherine E ^b   Kirschner, Daniel A ^a  

^a BOSTON COLLEGE   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adhesion protein; Detergents; Frog; Hydroxylamine; Mass spectrometry; Membrane membrane interactions; PNS; Protein zero cDNA; X ray diffraction

Indexed keywords

COMPLEMENTARY DNA; DETERGENT; FATTY ACID; HISTONE; MYELIN; UREA;

ANIMAL TISSUE; ARTICLE; CONFORMATIONAL TRANSITION; CYTOPLASM; DNA DENATURATION; DNA SEQUENCE; ELECTRICITY; FEMALE; FROG; HYDROPHOBICITY; IONIC STRENGTH; MEMBRANE COMPONENT; MOUSE; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PH; PRIORITY JOURNAL; PROTEIN STABILITY; PROTON TRANSPORT; SCIATIC NERVE; STRUCTURE ANALYSIS; VERTEBRATE; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; ANURA; BASE SEQUENCE; COMPUTER SIMULATION; DETERGENTS; ELECTROSTATICS; HYDROGEN-ION CONCENTRATION; HYDROPHOBICITY; HYDROXYLAMINE; MOLECULAR SEQUENCE DATA; MYELIN P0 PROTEIN; MYELIN SHEATH; OSMOLAR CONCENTRATION; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; X-RAY DIFFRACTION; XENOPUS LAEVIS;

ANURA; VERTEBRATA; XENOPUS LAEVIS;

EID: 41649088710     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2007.10.012     Document Type: Article

References (63)

1. Akers C.K., and Parsons D.F. X-ray diffraction of myelin membrane. I. Optimal conditions for obtaining unmodified small angle diffraction data from frog sciatic nerve. Biophys. J. 10 (1970) 101-115
2. Avila R.L., Inouye H., Baek R., Yin X., Trapp B.D., Feltri M.L., Wrabetz L., and Kirschner D.A. Structure and stability of internodal myelin in mouse models of hereditary neuropathy. J. Neuropathol. Exp. Neurol. 64 (2005) 976-990
3. Avila R.L., Tevlin B.R., Lees J.P., Inouye H., and Kirschner D.A. Myelin structure and composition in zebrafish. Neurochem. Res. 32 (2007) 197-209
4. Barbu M. Molecular cloning of cDNAs that encode the chicken P0 protein: evidence for early expression in avians. J. Neurosci. Res. 25 (1990) 143-151
5. Bizzozero O.A., Bixler H.A., Davis J.D., Espinosa A., and Messier A.M. Chemical deacylation reduces the adhesive properties of proteolipid protein and leads to decompaction of the myelin sheath. J. Neurochem. 76 (2001) 1129-1141
6. Bizzozero O.A., Fridal K., and Pastuszyn A. Identification of the palmitoylation site in rat myelin P0 glycoprotein. J. Neurochem. 62 (1994) 1163-1171
7. Blaurock, A.E., 1967. Low-Angle X-ray Diffraction Studies of the Myelin Sheath of Nerve, University of Michigan. Ph.D.
8. Blaurock A.E. Structure of the nerve myelin membrane: proof of the low-resolution profile. J. Mol. Biol. 56 (1971) 35-52
9. Blaurock A.E., Yale J.L., and Roots B.I. Ca-controlled, reversible structural transition in myelin. Neurochem. Res. 11 (1986) 1103-1129
10. Boggs J.M., Menikh A., and Rangaraj G. Trans interactions between galactosylceramide and cerebroside sulfate across apposed bilayers. Biophys. J. 78 (2000) 874-885
11. Brösamle C., and Halpern M.E. Characterization of myelination in the developing zebrafish. Glia 39 (2002) 47-57
12. Caspar D.L.D., and Kirschner D.A. Myelin membrane structure at 10 Å resolution. Nat. New Biol. 231 (1971) 46-52
13. Chandross R.J., Bear R.S., and Montgomery R.L. An X-ray diffraction comparison of myelins from the human nervous system. J. Comp. Neurol. 177 (1978) 1-9
14. Cserzo M., Wallin E., Simon I., von Heijne G., and Elofsson A. Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng. 10 (1997) 673-676
15. DeLano, W.L., 2002. The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA.
16. Eichberg J. Myelin P0: new knowledge and new roles. Neurochem. Res. 27 (2002) 1331-1340
17. Eisenberg D., Schwarz E., Komaromy M., and Wall R. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J. Mol. Biol. 179 (1984) 125-142
18. Faham S., Boulting G.L., Massey E.A., Yohannan S., Yang D., and Bowie J.U. Crystallization of bacteriorhodopsin from bicelle formulations at room temperature. Protein Sci. 14 (2005) 836-840
19. Fernandez-Moran H., and Finean J.B. Electron microscope and low-angle X-ray diffraction studies of the nerve myelin sheath. J. Biophys. Biochem. Cytol. 3 (1957) 725-748
20. Filbin M.T., and Tennekoon G.I. The role of complex carbohydrates in adhesion of the myelin protein, P0. Neuron 7 (1991) 845-855
21. Finean J.B., and Burge R.E. The determination of the Fourier transform of the myelin layer from a study of swelling phenomena. J. Mol. Biol. 17 (1963) 672-682
22. Frishman D., and Argos P. Knowledge-based protein secondary structure assignment. Proteins 23 (1995) 566-579
23. Gao Y., Li W., and Filbin M.T. Acylation of myelin P0 protein is required for adhesion. J. Neurosci. Res. 60 (2000) 704-713
24. Glover K.J., Whiles J.A., Wu G., Yu N., Deems R., Struppe J.O., Stark R.E., Komives E.A., and Vold R.R. Structural evaluation of phospholipid bicelles for solution-state studies of membrane-associated biomolecules. Biophys. J. 81 (2001) 2163-2171
25. Guex N., Diemand A., and Peitsch M.C. Protein modelling for all. Trends Biochem. Sci. 24 (1999) 364-367
26. Hayasaka K., Nanao K., Tahara M., Sato W., Takada G., Miura M., and Uyemura K. Isolation and sequence determination of cDNA encoding the major structural protein of human peripheral myelin. Biochem. Biophys. Res. Commun. 180 (1991) 515-518
27. Hoglund G., and Ringertz H. X-ray diffraction studies on peripheral nerve myelin. Acta Physiol. Scand. 51 (1961) 290-295
28. Inouye H., Karthigasan J., and Kirschner D.A. Membrane structure in isolated and intact myelins. Biophys. J. 56 (1989) 129-137
29. Inouye H., and Kirschner D.A. Membrane interactions in nerve myelin. I. Determination of surface charge from effects of pH and ionic strength on period. Biophys. J. 53 (1988) 235-245
30. Inouye H., and Kirschner D.A. Membrane interactions in nerve myelin: II. Determination of surface charge from biochemical data. Biophys. J. 53 (1988) 247-260
31. Inouye H., and Kirschner D.A. Phylogenetic aspects of myelin structure. NATO ASI Series (1990), Springer-Verlag 373--387
32. Inouye H., and Kirschner D.A. Folding and function of the myelin proteins from primary sequence data. J. Neurosci. Res. 28 (1991) 1-17
33. Inouye H., Tsuruta H., Sedzik J., Uyemura K., and Kirschner D.A. Tetrameric assembly of full-sequence protein zero myelin glycoprotein by synchrotron X-ray scattering. Biophys. J. 76 (1999) 423-437
34. Inouye H., Worthington A.R., and Worthington C.R. An X-ray study of fish nerves. Biol. Bull. 159 (1980) 485 (Abstract)
35. Kabsch W., and Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22 (1983) 2577-2637
36. Kirschner D.A., and Ganser A.L. Myelin labeled with mercuric chloride. Asymmetric localization of phosphatidylethanolamine plasmalogen. J. Mol. Biol. 157 (1982) 635-658
37. Kirschner D.A., Inouye H., Ganser A.L., and Mann V. Myelin membrane structure and composition correlated: a phylogenetic study. J. Neurochem. 53 (1989) 1599-1609
38. Kirschner D.A., Wrabetz L., and Feltri M.L. In: Lazzarini R.A., Griffin J.W., Lassmann H., et al. (Eds). The P0 gene. Myelin Biology and Disorders 1 vol. 1 (2004), Elsevier/Academic Press, Amsterdam 523-545
39. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schemiatic plots of protein structures. J. Appl. Cryst. 24 (1991) 946-950
40. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality protein structures. J. Appl. Cryst. 26 (1993) 283-291
41. Lemke G., and Axel R. Isolation and sequence of a cDNA encoding the major structural protein of peripheral myelin. Cell 40 (1985) 501-508
42. Luo X., Sharma D., Inouye H., Lee D., Avila R.L., Salmona M., and Kirschner D.A. Cytoplasmic domain of human myelin protein zero likely folded as {beta}-structure in compact myelin. Biophys. J. 92 (2007) 1585-1597
43. Martini R., Mohajeri M.H., Kasper S., Giese K.P., and Schachner M. Mice doubly deficient in the genes for P0 and myelin basic protein show that both proteins contribute to the formation of the major dense line in peripheral nerve myelin. J. Neurosci. 15 (1995) 4488-4495
44. Mateu L., Luzzati V., Vargas R., Vonasek E., and Borgo M. Order-disorder phenomena in myelinated nerve sheaths. II. The structure of myelin in native and swollen rat sciatic nerves and in the course of myelinogenesis. J. Mol. Biol. 215 (1990) 385-402
45. McIntosh T.J., and Worthington C.R. Direct determination of the lamellar structure of peripheral nerve myelin at low resolution (17 A). Biophys. J. 14 (1974) 363-386
46. McRee D.E. XtalView/Xfit-A versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125 (1999) 156-165
47. Moody M.F. X-ray diffraction pattern of nerve myelin: a method for determining the phases. Science 142 (1963) 1173-1174
48. Nielsen H., Engelbrecht J., Brunak S., and von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10 (1997) 1-6
49. Norton W.T., and Poduslo S.E. Myelination in rat brain: method of myelin isolation. J. Neurochem. 21 (1973) 749-757
50. Previtali S.C., Quattrini A., Fasolini M., Panzeri M.C., Villa A., Filbin M.T., Li W., Chiu S.-Y., Messing A., Wrabetz L., and Feltri M.L. Epitope-tagged P0 glycoprotein causes charcot-marie-tooth-like neuropathy in transgenic mice. J. Cell Biol. 151 (2000) 1035-1046
51. Saavedra R.A., Fors L., Aebersold R.H., Arden B., Horvath S., Sanders J., and Hood L. The myelin proteins of the shark brain are similar to the myelin proteins of the mammalian peripheral nervous system. J. Mol. Evol. 29 (1989) 149-156
52. Sakamoto Y., Kitamura K., Yoshimura K., Nishijima T., and Uyemura K. Complete amino acid sequence of PO protein in bovine peripheral nerve myelin. J. Biol. Chem. 262 (1987) 4208-4214
53. Schmitt F.O., Bear R.S., and Clark G.L. X-ray diffraction studies on nerve. Radiology 25 (1935) 131-151
54. Schweitzer J., Becker T., Becker C.G., and Schachner M. Expression of protein zero is increased in lesioned axon pathways in the central nervous system of adult zebrafish. Glia 41 (2003) 301-317
55. Senes A., Gerstein M., and Engelman D.M. Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with beta-branched residues at neighboring positions. J. Mol. Biol. 296 (2000) 921-936
56. Shapiro L., Doyle J.P., Hensley P., Colman D.R., and Hendrickson W.A. Crystal structure of the extracellular domain from P0, the major structural protein of peripheral nerve myelin. Neuron 17 (1996) 435-449
57. Smith S.O., Eilers M., Song D., Crocker E., Ying W., Groesbeek M., Metz G., Ziliox M., and Aimoto S. Implications of threonine hydrogen bonding in the glycophorin A transmembrane helix dimer. Biophys. J. 82 (2002) 2476-2486
58. Stratmann A., and Jeserich G. Molecular cloning and tissue expression of a cDNA encoding IP1-a P0-like glycoprotein of trout CNS myelin. J. Neurochem. 64 (1995) 2427-2436
59. Wells C.A., Saavedra R.A., Inouye H., and Kirschner D.A. Myelin P0-glycoprotein: predicted structure and interactions of extracellular domain. J. Neurochem. 61 (1993) 1987-1995
60. Worthington C.R., and Blaurock A.E. A structural analysis of nerve myelin. Biophys. J. 9 (1969) 970-990
61. Xie B., Luo X.Y., Zhao C., Priest C.M., Chan S.-Y., O'Connor P.B., Kirschner D.A., and Costello C.E. Molecular characterization of myelin protein zero in Xenopus laevis peripheral nerve: Equilibrium between non-covalnetly associated diimer and monomer. Int. J. Mass. Spctrom. 268 (2007) 304-315
62. Xu W., Shy M., Kamholz J., Elferink L., Xu G., Lilien J., and Balsamo J. Mutations in the cytoplasmic domain of P0 reveal a role for PKC-mediated phosphorylation in adhesion and myelination. J. Cell Biol. 155 (2001) 439-446
63. You K.-H., Hsieh C.-L., Hayes C., Stahl N., Francke U., and Popko B. DNA sequence, genomic organization, and chromosomal localization of the mouse peripheral myelin protein zero gene: identification of polymorphic alleles. Genomics 9 (1991) 751-757