PLP overexpression perturbs myelin protein composition and myelination in a mouse model of Pelizaeus-Merzbacher disease

GLIA

Volumn 55, Issue 4, 2007, Pages 341-351

  Karim, Saadia A ^a   Barrie, Jennifer A ^a   Mcculloch, Mailis C ^a   Montague, Paul ^a   Edgar, Julia M ^a   Kirkham, Douglas ^a   Anderson, Thomas J ^a   Nave, Klaus A ^b   Griffiths, Ian R ^a   Mclaughlin, Mark ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

Autophagic vacuole; Dysmyelination; Myelin basic protein; Oligodendrocyte

Indexed keywords

MYELIN PROTEIN; PROTEOLIPID PROTEIN; PROTEOLIPID PROTEIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE EXPRESSION; GENE LOCUS; GENE OVEREXPRESSION; HEMIZYGOSITY; LYSOSOME; MOUSE; MYELIN SHEATH; MYELINATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PATHOGENESIS; PELIZAEUS MERZBACHER DISEASE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SOMATIC CELL; TRANSGENE;

ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL COUNT; CELLS, CULTURED; GENE DOSAGE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYELIN PROTEINS; MYELIN PROTEOLIPID PROTEIN; MYELIN SHEATH; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; PELIZAEUS-MERZBACHER DISEASE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPINAL CORD;

EID: 33847006611     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20465     Document Type: Article

References (43)

1. Al-Saktawi K, McLaughlin M, Klugmann M, Schneider A, Barrie JA, McCulloch MC, Montague P, Kirkham D, Nave K-A, Griffiths IR. 2003. Genetic background determines phenotypic severity of the Plp rumpshaker mutation. J Neurosci Res 72:12-24.
2. Amaducci L, Pazzagli A, Pessina G. 1962. The relation of proteolipids and phosphatidopeptides to tissue elements in the bovine nervous system. J Neurochem 9:309-318.
3. Anderson TJ. 1997. Effects of increased dosage of the Plp gene: A study in transgenic mice. PhD Thesis, University of Glasgow.
4. Anderson TJ, Klugmann M, Thomson CE, Schneider A, Readhead C, Nave K-A, Griffiths IR. 1999. Distinct phenotypes associated with increasing dosage of the Plp gene: Implications for CMT1A due to Pmp22 gene duplication. Ann NY Acad Sci 883:234-246.
5. Anderson TJ, Schneider A, Barrie JA, Klugmann M, McCulloch MC, Kirkham D, Kynakides E, Nave K-A, Griffiths IR. 1998. Late-onset neurodegeneration in mice with increased dosage of the proteolipid protein gene. J Comp Neurol 394:506-519.
6. Bauer J, Bradl M, Klein M, Leisser M, Deckwerth TL, Wekerle H, Lassmann H. 2002. Endoplasmic reticulum stress in PLP-overexpressing transgenic rats: Gray matter oligodendrocytes are more vulnerable than white matter oligodendrocytes. J Neuropathol Exp Neurol 61:12-22.
7. Bradl M, Bauer J, Inomate T, Zielasek J, Nave KA, Toyka K, Lassmann H, Wekerle H. 1999. Transgenic Lewis rats overexpressing the proteolipid protein gene: Myelin degeneration and its effect on T cell-mediated experimental autoimmune encephalomyelitis. Acta Neuropathol (Berl) 97:595-606.
8. Butt AM, Ibrahim M, Gregson N, Berry M. 1998. Differential expression of the L- and S-isoforms of myelin associated glycoprotein (MAG) in oligodendrocyte unit phenotypes in the adult rat anterior medullary velum. J Neurocytol 27:271-280.
9. Cerghet M, Bessert DA, Nave KA, Skoff RP. 2001. Differential expression of apoptotic markers in jimpy and in Plp overexpressors: Evidence for different apoptotic pathways. J Neurocytol 30:841-855.
10. Chies R, Nobbio L, Edomi P, Schenone A, Schneider C, Brancolini C. 2003. Alterations in the Arf6-regulated plasma membrane endosomal recycling pathway in cells overexpressing the tetraspan protein Gas3/PMP22. J Cell Sci 116:987-999.
11. Griffiths IR, Duncan ID, McCulloch M. 1981. Shaking pup: A disorder of central myelination in the spaniel dog. II. Ultrastructural observations on the white matter of cervical spinal cord. J Neurocytol 10:847-858.
12. Griffiths IR, Klugmann M, Anderson TJ, Yool D, Thomson CE, Schwab MH, Schneider A, Zimmermann F, McCulloch MC, Nadon NL, Nave K-A. 1998. Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280:1610-1613.
13. Harding B, Ellis D, Malcolm S. 1995. A case of Pelizaeus-Merzbacher disease showing increased dosage of the proteolipid protein gene. Neuropathol Appl Neurobiol 21:111-115.
14. Hudson LD, Garbern JY, Kamholz JA. 2004. Pelizaeus-Merzbacher disease. In: Lazzarini RA, Griffin JW, Lassmann H, Nave K-A, Miller RH, Trapp BD, editors. Myelin biology and disorders. Amsterdam: Elsevier. pp 867-885.
15. Huxley C, Passage E, Robertson AM, Youl B, Huston S, Manson A, Sabéran-Djoniedi D, Figarella-Branger D, Pellissier JF, Thomas PK, Fontés M. 1998. Correlation between varying levels ofPMP22 expression and the degree of demyelination and reduction in nerve conduction velocity in transgenic mice. Hum Mol Genet 7:449-458.
16. Inoue K. 2005. PLP1-related inherited dysmyelinating disorders: Pelizaeus-Merzbacher disease and spastic paraplegia type 2. Neurogenetics 6:1-16.
17. Inoue Y, Kagawa T, Matsumura Y, Ikenaka K, Mikoshiba K. 1996. Cell death of oligodendrocytes or demyelination induced by overexpression of proteolipid protein depending on expressed gene dosage. Neurosci Res 25:161-172.
18. Kagawa T, Ikenaka K, Inoue Y, Kuriyama S, Tsujii T, Nakao J, Nakajima K, Aruga J, Okano H, Mikoshiba K. 1994. Glial cell degeneration and hypomyelination caused by overexpression of myelin proteolipid protein gene. Neuron 13:427-442.
19. Kirmani BF, Jacobowitz DM, Namboodiri MAA. 2003. Developmental increase of aspartoacylase in oligodendrocytes parallels CNS myelination. Brain Res Dev Brain Res 140:105-115.
20. Klugmann M, Schwab MH, Pühlhofer A, Schneider A, Zimmermann F, Griffiths IR, Nave K-A. 1997. Assembly of CNS myelin in the absence of proteolipid protein. Neuron 18:59-70.
21. Koeppen AH. 2005. A brief history of Pelizaeus-Merzbacher disease and proteolipid protein. J Neurol Sci 228:198-200.
22. Madhavarao CN, Moffett JR, Moore RA, Viola RE, Namboodiri MAA, Jacobowitz DM. 2004. Immunohistochemical localization of asparoacylase in the rat central nervous system. J Comp Neurol 472:318-329.
23. McLaughlin M, Barrie JA, Karim SA, Montague P, Edgar JM, Kirkham D, Thomson CE, Griffiths IR. 2006a. Processing of PLP in a model of Pelizaeus-Merzbacher disease/SPG2 due to the rumpshaker mutation. Glia 53:715-722.
24. McLaughlin M, Karim SA, Montague P, Barrie JA, Kirkham D, Griffiths IR, Edgar JM. 2006b. Genetic background influences UPR but not PLP processing in the rumpshaker model of PMD/SPG2. Neurochem Res (in press).
25. McPhilemy K, Mitchell LS, Griffiths IR, Morrison S, Deary AW, Sommer I, Kennedy PGE. 1990. Effect of optic nerve transection upon myelin protein gene expression by oligodendrocytes: Evidence for axonal influences on gene expression. J Neurocytol 19:494-503.
26. Mehl E, Wolfgram F. 1969. Meylin types with different protein components in the same species. J Neurochem 16:1091-1097.
27. Montague P, Barrie JA, Thomson CE, Kirkham D, McCallion AS, Davies RW, Kennedy PGE, Griffiths IR. 1998. Cytoskeletal and nuclear localization of MOBP polypeptides. Eur J Neurosci 10:1321-1328.
28. Nave K-A, Griffiths IR. 2004. Models of Pelizaeus-Merzbacher disease. In: Lazzarini RA, Griffin JW, Lassmann H, Nave K-A, Miller RH, Trapp BD, editors. Myelin biology and disorders. Amsterdam: Elsevier. pp 1125-1142.
29. Niemann S, Sereda MW, Suter U, Griffiths IR, Nave KA. 2000. Uncoupling of myelin assembly and Schwann cell differentiation by transgenic overexpression of peripheral myelin protein 22. J Neurosci 20:4120-4128.
30. Readhead C, Schneider A, Griffiths IR, Nave K-A. 1994. Premature arrest of myelin formation in transgenic mice with increased proteolipid protein gene dosage. Neuron 12:583-595.
31. Sereda M, Griffiths IR, Pühlhofer A, Stewart H, Rossner MJ, Zimmermann F, Magyar JP, Schneider A, Hund E, Meinck HM, Suter U, Nave K-A. 1996. A transgenic rat model of Charcot-Marie-Tooth disease. Neuron 16:1049-1060.
32. Shine HD, Readhead C, Popko B, Hood L, Sidman RL. 1992. Morphometric analysis of normal, mutant and transgenic CNS: Correlation of myelin basic protein expression to myelinogenesis. J Neurochem 58:342-349.
33. Simons M, Krämer EM, Macchi P, Rathke-Hartlieb S, Trotter J, Nave K-A, Schulz JB. 2002. Overexpression of the myelin proteolipid protein leads to accumulation of cholesterol and proteolipid protein in endosomes/lysosomes: Implications for Pelizaeus-Merzbacher disease. J Cell Biol 157:327-336.
34. Southwood C, Gow A. 2001. Molecular pathways of oligodendrocyte apoptosis revealed by mutations in the proteolipid protein gene. Microsc Res Tech 52:700-708.
35. Southwood CM, Garbern J, Jiang W, Gow A. 2002. The unfolded protein response modulates disease severity in Pelizaeus-Merzbacher disease. Neuron 36:585-596.
36. Thomson CE, Vouyiouklis DA, Barrie JA, Wease KN, Montague P. 2005. Plp Gene regulation in the developing murine optic nerve: Correlation with oligodendroglial process alignment along the axons. Dev Neurosci 27:27-36.
37. Trajkovic K, Dhaunchak AS, Goncalves JT, Wenzel D, Schneider A, Bunt G, Nave KA, Simons M. 2006. Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites. J Cell Biol 172:937-948.
38. Trapp BD, Nishiyama A, Cheng D, Macklin E. 1997. Differentiation and death of premyelinating oligodendrocytes in developing rodent brain. J Cell Biol 137:459-468.
39. Wolf NI, Sistermans EA, Cundall M, Hobson GM, Davis-Williams AP, Palmer R, Stubbs P, Davies S, Endziniene M, Wu Y, Chong WK, Malcolm S, Surtees R, Garbern JY, Woodward KJ. 2005. Three or more copies of the proteolipid protein gene PLP1 cause severe Pelizaeus-Merzbacher disease. Brain 128:743-751.
40. Woodward K, Kendall E, Vetrie D, Malcolm S. 1998. Pelizaeus-Merzbacher disease: Identification of Xq22 proteolipid-protein duplications and characterization of breakpoints by interphase FISH. Am J Hum Genet 63:207-217.
41. 0 Glycoprotein overexpression causes congenital hypomyelination of peripheral nerves. J Cell Biol 148:1021-1033.
42. 0 protein. J Cell Biol 148:1009-1020.
43. Yool DA, Klugmann M, McLaughlin M, Vouyiouklis DA, Dimou L, Barrie JA, McCulloch MC, Nave K-A, Griffiths IR. 2001. Myelin proteolipid proteins promote the interaction of oligodendrocytes and axons. J Neurosci Res 63:151-164.