Different cellular and molecular mechanisms for early and late-onset myelin protein zero mutations

Human Molecular Genetics

Volumn 17, Issue 13, 2008, Pages 1877-1889

  Grandis, Marina ^a   Vigo, Tiziana ^a,c   Passalacqua, Mario ^b   Jain, Manisha ^d   Scazzola, Sara ^c   La padula, Veronica ^a   Brucal, Michelle ^d   Benvenuto, Federica ^a   Nobbio, Lucilla ^a   Cadoni, Angela ^b   Mancardi, Gian Luigi ^a   Kamholz, John ^d   Shy, Michael E ^d   Schenone, Angelo ^a,c  

^a Department of Neurosciences Ophthalmology and Genetics ^*  (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c CNR   (Italy)

^d WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN PROTEIN; MYELIN PROTEIN ZERO;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL FUNCTION; CELL MEMBRANE; CELL MIGRATION; CELL VIABILITY; CONTROLLED STUDY; CYTOPLASM; GENE DELETION; GENE MUTATION; HELA CELL; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; SCHWANN CELL; TRANSIENT TRANSFECTION; WILD TYPE;

AGE OF ONSET; ANIMALS; APOPTOSIS; CELL AGGREGATION; CELL SURVIVAL; CHARCOT-MARIE-TOOTH DISEASE; GENES, REPORTER; GLYCOSYLATION; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; MICE; MUTATION, MISSENSE; MYELIN P0 PROTEIN; PROTEIN FOLDING; PROTEIN TRANSPORT;

MURINAE;

EID: 45749132610     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn083     Document Type: Article

References (37)

1. Lemke, G. and Axel, R. (1985) Isolation and sequence of a cDNA encoding the major structural protein of peripheral myelin. Cell, 40, 501-508.
2. Filbin, M.T., Walsh, F.S., Trapp, B.D., Pizzey, J.A. and Tennekoon, G.I. (1990) Role of myelin PO protein as a homophilic adhesion molecule. Nature, 344, 871-872.
3. Spiryda, L.B. (1998) Myelin protein zero and membrane adhesion. J. Neurosci. Res., 54, 137-146.
4. Eichberg, J. (2002) Myelin PO: New knowledge and new roles. Neurochem. Res., 27, 1331-1340.
5. Shapiro, L., Doyle, J.P., Hensley, P., Colman, D.R. and Hendrickson, W.A. (1996) Crystal structure of the extracellular domain from PO, the major structural protein of peripheral nerve myelin. Neuron, 17 435-449.
6. Wong, M.H. and Filbin, M.T. (1994) The cytoplasmic domain of the myelin PO protein influences the adhesive interactions of its extracellular domain. J. Cell Biol., 126, 1089-1097.
7. Xu, W., Shy, M.E., Kamholz, J., Elferink, L., Xu, G., Lilien, J. and Balsamo, J. (2001) Mutations in the cytoplasmic domain of PO reveal a role for PKC-mediated phosphorylation in adhesion and myelination. J. Cell Biol., 155, 439-446.
8. Gaboreanu, A.M., Hrstka, R., Xu, W., Shy, M., Kamholz, J., Lilien, J. and Balsamo, J. (2007) Myelin protein zero/PO phosphorylation and function require an adaptor protein linking it to RACK1 and PKC(alpha). J. Cell Biol., 177, 707-716.
9. Shy, M.E., Jani, A., Krajewski, K, Grandis, M., Lewis, R.A., Li, J., Shy, R.R., Balsamo, J., Lilien, J., Garbern, J.Y. and Kamholz, J. (2004) Phenotypic clustering in MPZ mutations. Brain, 127, 371-384.
10. Bai, I., Ianokova, E., Pu, Q., Ghandour, K., Levinson, R., Martin, J.J., Ceuterick-de Groote, C., Mazanec, R., Seeman, P., Shy, M.E. and Li, J. (2006) Effect of an R69C mutation in the myelin protein zero gene on myelination and ion channel subtypes. Arch. Neurol., 63, 1787-1794.
11. Li, J., Bai, Y., Ianakova, E., Grandis, M., Uchwat, F., Trostinskaia, A., Krajewski, K.M., Garbern, J., Kupsky, W.J. and Shy, M.E. (2006) Major myelin protein gene (PO) mutation causes a novel form of axonal degeneration. J. Comp. Neurol., 10, 252-265.
12. Shames, I., Fraser, A., Colby, J., Orfali, W. and Snipes, G.J. (2003) Phenotypic differences between peripheral myelin protein-22 (PMP22) and myelin protein zero (PO) mutations associated with Charcot-Marie-Tooth-related diseases. J. Neuropathol. Exp. Neurol. 62, 751-764.
13. Inoue, K., Khajavi, M., Ohyama, T., Hirabayashi, S., Wilson, J., Reggin J.D., Mancias, P., Butler, I.J., Wilkinson, M.F., Wegner, M. et al. (2004; Molecular mechanism for distinct neurological phenotypes conveyed by allelic truncating mutations. Nat. Genet., 36, 361-369.
14. Parodi, A.J. (2000) Protein glucosylation and its role in protein folding. Annu. Rev. Biochem., 69, 69-93.
15. Gallagher, M.J., Shen, W., Song, L. and Macdonald, R.L. (2005) Endoplasmic reticulum retention and associated degradation of a GABAA receptor epilepsy mutation that inserts an aspartate in the M3 transmembrane segment of the alphal subunit. J. Biol. Chem., 280, 37995-38004.
16. Niemann, S., Sereda, M.W., Suter, U., Griffiths, I.R. and Nave, K.A. (2000) Uncoupling of myelin assembly and schwann cell differentiation by transgenic overexpression of peripheral myelin protein 22. Neuroscience, 20, 4120-4128.
17. Zhang, K. and Kaufman, R.J. (2006) The unfolded protein response: A stress signaling pathway critical for health and disease. Neurology 66, S102-S109.
18. Rutkowski, D.T. and Kaufman, R.J. (2004) A trip to the ER: Coping with stress. Trends Cell. Biol., 14, 20-28.
19. Calfon, M., Zeng, H., Urano, F., Till, J.H., Hubbard, S.R., Harding, H.P., Clark, S.G. and Ron, D. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature, 415, 92-96.
20. Doyle, J.P., Stempak, J.G., Cowin, P., Colman, D.R. and D'Urso, D. (1995) Protein zero, a nervous system adhesion molecule, triggers epithelial reversion in host carcinoma cells. J. Cell Biol., 131, 465-482.
21. Toews, A.D., Fischer, H.R., Goodrum, J.F., Windes, S. and Morell, P. (1987) Metabolism of phosphate and sulfate groups modifying the PO protein of peripheral nervous system myelin. J. Neurochem., 48 883-887.
22. Quarles, R.H. (1997) Glycoproteins of myelin sheaths. J. Mol. Neurosci, 8, 1-12.
23. Filbin, M.T. and Tennekoon, G.I. (1993) Homophilic adhesion of the myelin PO protein requires glycosylation of both molecules in the homophilic pair. J. Cell Biol., 122, 451-459.
24. Filbin, M.T. and Tennekoon, G.I. (1991) The role of complex carbohydrates in adhesion of the myelin protein, PO. Neuron, 7 845-855.
25. De Jonghe, P., Timmerman, V., Ceuterick, C., Nelis, E., De Vriendt, E., Lofgren, A., Vercruyssen, A., Verellen, C., Van Maldergem, L., Martin, J.J. et al. (1999) The Thr124Met mutation in the peripheral myelin protein zero (MPZ) gene is associated with a clinically distinct Charcot-Marie-Tooth phenotype. Brain, 122, 81-90.
26. Blanquet-Grossard, F., Pham-Dinh, D., Dautigny, A., Latour, P., Bonnebouche, C., Diraison, P., Chapon, F., Chazot, G. and Vandenberghe, A. (1996) Charcot-Marie-Tooth type 1B neuropathy: A mutation at the single glycosylation site in the major peripheral myelin glycoprotein Po. Hum. Mutat., 8, 185-186.
27. Sommer, L. and Suter, U. (1998) The glycoprotein PO in peripheral gliogenesis. Cell. Tissue Res., 292, 11-16.
28. Martini, R., Zielasek, J., Toyka, K.V., Giese, K.P. and Schachner, M. (1995) Protein zero (PO)-deficient mice show myelin degeneration in peripheral nerves characteristic of inherited human neuropathies. Nat. Genet., 11, 281-286.
29. Shy, M.E., Arroyo, E., Sladky, J., Menichella, D., Jiang, H., Xu, W., Kamholz, J. and Scherer, S.S. (1997) Heterozygous PO knockout mice develop a peripheral neuropathy that resembles chronic inflammatory demyelinating polyneuropathy (CIDP). J. Neuropathol. Exp. Neurol., 56, 811-821.
30. Giese, K.P., Martini, R., Lemke, G., Soriano, P. and Schachner, M. (1992) Mouse PO gene disruption leads to hypomyelination, abnormal expression of recognition molecules, and degeneration of myelin and axons. Cell, 71, 565-576.
31. Wrabetz, L., D'Antonio, M., Pennuto, M., Dati, G., Tinelli, E., Fratta, P., Previtali, S., Imperiale, D., Zielasek, J., Toyka, K. et al. (2006) Different intracellular pathomechanisms produce diverse Myelin Protein Zero neuropathies in transgenic mice. J. Neurosci., 26 2358-2368.
32. Dickson, K.M., Bergeron, J.J., Shames, I., Colby, J., Nguyen, D.T., Chevet, E., Thomas, D.Y. and Snipes, G.J. (2002) Association of calnexin with mutant peripheral myelin protein-22 ex vivo: A basis for 'gain-of-function' ER diseases. Proc. Natl Acad. Sci. USA, 99 9852-9857.
33. Fortun, J., Li, J., Go, J., Fenstermaker, A., Fletcher, B.S. and Notterpek, L. (2005) Impaired proteasome activity and accumulation of ubiquitinated substrates in a hereditary neuropathy model. J. Neurochem., 92, 1531-1541.
34. Avila, R.L., Inouye, K., D'Antonio, M.L., Feltri, M.L., Wrabetz, L. and Kirschner, D.A. (2007) Roles of Adhesion interfaces and novel disulfide in myelin instability and packing defects in MPZS63C transgenic mice. J. Peripher. Nerv. Syst., 12S, 6.
35. Manent, J., Oguievetskaia, K., Bayer, J., Ratner, N. and Giovannini, M. (2003) Magnetic cell sorting for enriching Schwann cells from adult mouse peripheral nerves. J. Neurosci. Methods, 123, 167-173.
36. Zacharias, D.A., Violin, J.D., Newton, A.C. and Tsien, R.Y. (2002) Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science, 296, 913-916.
37. Qian, Y., Galli, A., Ramamoorthy, S., Risso, S., DeFelice, L.J. and Blakely, R.D. (1997) Protein kinase C activation regulates human serotonin transporters in HEK-293 cells via altered cell surface expression. J. Neurosci., 17, 45-57.