The different forms of PNS myelin P0 protein within and outside lipid rafts

Journal of Neurochemistry

Volumn 107, Issue 1, 2008, Pages 291-301

  Fasano, Anna ^a   Amoresano, Angela ^b   Rossano, Rocco ^c   Carlone, Giulia ^a,c   Carpentieri, Andrea ^b   Liuzzi, Grazia Maria ^a   Pucci, Piero ^b   Riccio, Paolo ^c,d  

^a UNIVERSITY OF BARI   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c UNIVERSITY OF BASILICATA   (Italy)

^d NATIONAL INSTITUTE OF BIOSTRUCTURES AND BIOSYSTEMS   (Italy)

Author keywords

Glycans; Lipid rafts; Mass spectrometry; Myelin; P0; Peripheral nervous system

Indexed keywords

MYELIN PROTEIN; OLIGOSACCHARIDE;

AMINO ACID SEQUENCE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; HIGH PERFORMANCE THIN LAYER CHROMATOGRAPHY; LIPID ANALYSIS; LIPID COMPOSITION; LIPID RAFT; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEIN STRUCTURE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; FEMALE; GLYCOSYLATION; MEMBRANE MICRODOMAINS; MYELIN P0 PROTEIN; MYELIN SHEATH; NERVE FIBERS, MYELINATED; PERIPHERAL NERVES; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 51849095442     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05598.x     Document Type: Article

References (55)

1. Arvanitis D. N., Min W., Gong Y., Heng Y. M. Boggs J. M. (2005) Two types of detergent-insoluble, glycosphingolipid/cholesterol-rich membrane domains from isolated myelin. J. Neurochem. 94, 1696 1710.
2. Avila R. L., Inouye H., Baek R. C., Yin X., Trapp B. D., Feltri M. L., Wrabetz L. Kirschner D. A. (2005) Structure and stability of internodal myelin in mouse models of hereditary neuropathy. J. Neuropathol. Exp. Neurol. 64, 976 990.
3. Brown D. A. London E. (1998) Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14, 111 136.
4. D'Urso D., Brophy P. J., Staugaitis S. M., Gillespie C. S., Frey A. B., Stempak J. G. Colman D. R. (1990) Protein zero of peripheral nerve myelin: biosynthesis, membrane insertion, and evidence for homotypic interaction. Neuron 4, 449 460.
5. DeBruin L. S. Harauz G. (2007) White matter rafting-membrane microdomains in myelin. Neurochem. Res. 32, 213 228. Epub 2006 Sep 21. Review.
6. DeBruin L. S., Haines J. D., Wellhauser L. A., Radeva G., Schonmann V., Bienzle D. Harauz G. (2005) Developmental partitioning of myelin basic protein into membrane microdomains. J. Neurosci. Res. 80, 211 225.
7. DeBruin L. S., Haines J. D., Bienzle D. Harauz G. (2006) Partitioning of myelin basic protein into membrane microdomains in a spontaneously demyelinating mouse model for multiple sclerosis. Biochem. Cell Biol., 84, 993 1005.
8. Deibler G. E., Martenson R. E. Kies M. W. (1972) Large-scale preparation of myelin basic protein from central nervous tissue of several mammalian species. Prep. Biochem. 2, 139 165.
9. Filbin M. T. Tennekoon G. I. (1992) Myelin P0-protein, more than just a structural protein? Bioessays 14, 541 547.
10. Filbin M. T. Tennekoon G. I. (1993) Homophilic adhesion of the myelin P0 protein requires glycosylation of both molecules in the homophilic pair. J. Cell Biol. 122, 451 459.
11. Filbin M. T., Walsh F. S., Trapp B. D., Pizzey J. A. Tennekoon G. I. (1990) The role of myelin P0 protein as a homophilic adhesion molecule. Nature 344, 871 872.
12. Folch J., Ascoli I., Lees M., Meath Ja. Lebaron N. (1951) Preparation of lipid extracts from brain tissue. J. Biol. Chem. 191, 833 841.
13. Gallego R. G., Blanco J. L., Thijssen-van Zuylen C. W., Gotfredsen C. H., Voshol H., Duus J. O., Schachner M. Vliegenthart J. F. (2001) Epitope diversity of N-glycans from bovine peripheral myelin glycoprotein P0 revealed by mass spectrometry and nano probe magic angle spinning 1H NMR spectroscopy. J. Biol. Chem. 276, 30834 30844.
14. Ganser A. L., Kerner A., Brown B., Davisson M. T. Kirschner D. A. (1988) A survey of neurological mutant mice I. Lipid composition of myelinated issue in known myelin mutants Dev. Neurosci. 10, 99 122.
15. Gielen E., Baron W., Vandeven M., Steels P., Hoekstra D. Ameloot M. (2006) Rafts in oligodendrocytes: evidence and structure-function relationship. Glia 54, 499 512.
16. Görg A., Obermaier C., Boguth G., Harder A., Scheibe B., Wildgruber R. Weiss W. (2000) The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 21, 1037 1053.
17. Greenfield S., Brostoff S., Eylar E. H. Morell P. (1973) Protein composition of myelin of the peripheral nervous system. J. Neurochem. 20, 1207 1216.
18. Haas H., Oliveira C. L. P., Torriani I. L., Polverini E., Fasano A., Carlone G., Cavatorta P. Riccio P. (2004) Small angle X-ray scattering from lipid-bound myelin basic protein in solution. Biophys. J. 86, 455 460.
19. Harris T. J. Siu C. H. (2002) Reciprocal raft-receptor interactions and the assembly of adhesion complexes. Bioessays 24, 996 1003.
20. Hasse B., Bosse F. Muller H. W. (2002) Proteins of peripheral myelin are associated with glycosphingolipid/cholesterol-enriched membranes. J. Neurosci. Res. 69, 227 232.
21. Inouye H. Kirschner D. A. (1991) Folding and function of the myelin proteins from primary sequence data. J. Neurosci. Res. 28, 1 17.
22. Inouye H., Tsuruta H., Sedzik J., Uyemura K. Kirschner D. A. (1999) Tetrameric assembly of full-sequence protein zero myelin glycoprotein by synchrotron x-ray scattering. Biophys. J. 76, 423 437.
23. Kim T. Pfeiffer S. E. (1999) Myelin glycosphingolipid/cholesterol- enriched microdomains selectively sequester the non-compact myelin proteins CNP and MOG. J. Neurocytol. 28, 281 293.
24. Kirschner D. A. Blaurock A. E. (1992) Organization, phylogenetic variations and dynamic transitions of myelin structure, in Myelin: Biology and Chemistry (Martenson R. E., ed pp. 3 78. CRC Press, Boca Raton, FL.
25. Kirschner D. A., Wrabetz L. Feltri M. L. (2004) The P0 gene, in Myelin Biology and Disorders (Lazzarini R. A., ed pp. 523 545. Elsevier Academic, San Diego.
26. Laurà M., Milani M., Morbin M., Moggio M., Ripolone M., Jann S., Scaioli V., Taroni F. Pareyson D. (2007) Rapid progression of late onset axonal Charcot-Marie-Tooth disease associated with a novel MPZ mutation in the extracellular domain. J. Neurol. Neurosurg. Psychiatry 78, 1263 1266.
27. Lemke G. Axel R. (1985) Isolation and sequence of a cDNA encoding the major structural protein of peripheral myelin. Cell 198540, 501 508.
28. Lemke G., Lamar E. Patterson J. (1988) Isolation and analysis of the gene encoding peripheral myelin protein zero. Neuron 1, 73 83.
29. McFarland H. F. Martin R. (2007) Multiple sclerosis: a complicated picture of autoimmunity. Nat. Immunol. 8, 913 919.
30. Rabilloud T., Valette C. Lawrence J. J. (1994) Sample application by in-gel rehydration improves the resolution of two-dimensional electrophoresis with immobilized pH gradients in the first dimension. Electrophoresis 15, 1552 1558.
31. Riccio P. Quagliariello E. (1993) Lipid-bound, native-like, myelin basic protein: a well-known protein in a new guise, or an unlikely story? J. Neurochem. 61, 787 788.
32. Riccio P., Rosenbusch J. Quagliariello E. (1984) A new procedure to isolate brain myelin basic protein in a lipid-bound form. FEBS Lett. 177, 236 240.
33. Riccio P., Bobba A., Romito E., Minetola M. Quagliariello E. (1994) A new detergent to purify CNS myelin basic protein isoforms in lipid-bound form. Neuroreport 5, 689 692.
34. Riccio P., Zito F., Fasano A., Liuzzi G. M., Lolli F., Polverini E. Cavatorta P. (1998) Purification of bovine P2 myelin protein with bound lipids. Neuroreport 9, 2769 2773.
35. Sanchez J. C., Rouge V., Pisteur M., Ravier F., Tonella L., Moosmayer M., Wilkins M. R. Hochstrasser D. (1997) Improved and simplified in-gel sample application using reswelling of dry immobilized pH gradients. Electrophoresis 18, 324 327.
36. Saravanan K., Schaeren-Wiemers N., Klein D., Sandhoff R., Schwarz A., Yaghootfam A., Gieselmann V. Franken S. (2004) Specific downregulation and mistargeting of the lipid raft-associated protein MAL in a glycolipid storage disorder. Neurobiol. Dis. 16, 396 406.
37. Schaeren-Wiemers N., Bonnet A., Erb M., Erne B., Bartsch U., Kern F., Mantei N., Sherman D. Suter U. (2004) The raft-associated protein MAL is required for maintenance of proper axon-glia interactions in the central nervous system. J. Cell Biol. 166, 731 742.
38. Sedzik J., Uyemura K. Tsukiharaa T. (2002) Towards crystallization of hydrophobic myelin glycoproteins: P0 and PASII/PMP22. Protein Expr. Purif. 26, 368 377.
39. Sedzik J., Carlone G., Fasano A., Liuzzi G. M. Riccio P. (2003) Crystals of P2 myelin protein in lipid-bound form. J. Struct. Biol. 142, 292 300.
40. Shapiro L., Doyle J. P., Hensley P., Colman D. R. Hendrickson W. A. (1996) Crystal structure of the extracellular domain from P0, the major structural protein of peripheral nerve myelin. Neuron 17, 435 449.
41. Shevchenko A., Wilm M., Vorm O. Mann M. (1996) Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68, 850 858.
42. Simons K. Ikonen E. (1997) Functional rafts in cell membranes. Nature 387, 569 572.
43. Simons K. Toomre D. (2000) Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31 39.
44. Simons M., Krämer E. M., Thiele C., Stoffel W. Trotter J. (2000) Assembly of myelin by association of proteolipid protein with cholesterol- and galactosylceramide-rich membrane domains. J. Cell Biol. 151, 143 154.
45. Smith R. (1992) The basic protein of CNS myelin: its structure and ligand binding. J. Neurochem. 59, 1589 1608.
46. Steinman L. (2007) Antigen-specific therapy of multiple sclerosis: the long-sought magic bullet. Neurotherapeutics 4, 661 665.
47. Taylor C. M., Coetzee T. Pfeiffer S. E. (2002) Detergent-insoluble glycosphingolipid/cholesterol microdomains of the myelin membrane. J. Neurochem. 81, 993 1004.
48. Thompson A. J., Cronin M. S. Kirschner D. A. (2002) Myelin protein zero exists as dimers and tetramers in native membranes of Xenopus laevis peripheral nerve. J. Neurosci. Res. 67, 766 771.
49. Tsui-Pierchala B. A., Encinas M., Milbrandt J. Johnson Jr. E. M. (2002) Lipid rafts in neuronal signaling and function. Trends Neurosci. 25, 412 417.
50. Voshol H., van Zuylen C. W., Orberger G., Vliegenthart J. F. Schachner M. (1996) Structure of the HNK-1 carbohydrate epitope on bovine peripheral myelin glycoprotein P0. J. Biol. Chem. 271, 22957 22960.
51. Warner L. E., Hilz M. J., Appel S. H. et al. (1996) Clinical phenotypes of different MPZ (P0) mutations may include Charcot-Marie-Tooth type 1B, Dejerine-Sottas, and congenital hypomyelination. Neuron 17, 451 460.
52. Wessel D. Flügge U. I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141 143.
53. Wrabetz L., D'Antonio M., Pennuto M. et al. (2006) Different intracellular pathomechanisms produce diverse myelin protein zero neuropathies in transgenic mice. J. Neurosci. 26, 2358 2368.
54. Xie B., Luob X., Zhaoa C., Priest C. M., Chana S.-Y., O'Connor P. B., Kirschner D. A. Costello C. E. (2007) Molecular characterization of myelin protein zero in Xenopus laevis peripheral nerve: equilibrium between non-covalently associated dimer and monomer. Int. J. Mass Spectrom. 268, 304 315.
55. Yazaki T., Miura M., Asou H., Kitamura K., Toya S. Uyemura K. (1992) Glycopeptide of P0 protein inhibits homophilic cell adhesion. Competition assay with transformants and peptides. FEBS Lett. 307, 361 366.