p25α relocalizes in oligodendroglia from myelin to cytoplasmic inclusions in multiple system atrophy

American Journal of Pathology

Volumn 171, Issue 4, 2007, Pages 1291-1303

  Song, Yun Ju C ^a   Lundvig, Ditte M S ^c   Huang, Yue ^a   Wei, Ping Gai ^b   Blumbergs, Peter C ^b   Højrup, Peter ^d   Otzen, Daniel ^e   Halliday, Glenda M ^a   Jensen, Poul H ^c  

^a NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^b FLINDERS UNIVERSITY   (Australia)

^c AARHUS UNIVERSITY   (Denmark)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^e AALBORG UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; MYELIN; MYELIN BASIC PROTEIN; PROTEIN P 25 ALPHA; PROTEIN P25; UNCLASSIFIED DRUG; NERVE PROTEIN; P25 PROTEIN, HUMAN;

ANIMAL TISSUE; ARTICLE; CELL AGGREGATION; CELL INCLUSION; CONTROLLED STUDY; GLIA CELL; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN DEGRADATION; SHY DRAGER SYNDROME; ANIMAL; CATTLE; CHEMISTRY; CYTOPLASM; METABOLISM; MYELIN SHEATH; NERVE FIBER; PATHOLOGY; SWINE;

ALPHA-SYNUCLEIN; ANIMALS; AXONS; CATTLE; CYTOPLASM; HUMANS; INCLUSION BODIES; MULTIPLE SYSTEM ATROPHY; MYELIN BASIC PROTEINS; MYELIN SHEATH; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; SWINE;

EID: 35348909482     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2007.070201     Document Type: Article

References (49)

1. Wilkins A, Majed H, Layfield R, Compston A, Chandran S: Oligodendrocytes promote neuronal survival and axonal length by distinct intracellular mechanisms: a novel role for oligodendrocyte-derived glial cell line-derived neurotrophic factor. J Neurosci 2003, 23:4967-4974
2. Boggs JM: Myelin basic protein: a multifunctional protein. Cell Mol Life Sci 2006, 63:1945-1961
3. Carré JL, Goetz BD, O'Connor LT, Bremer Q, Duncan ID: Mutations in the rat myelin basic protein gene are associated with specific alterations in other myelin gene expression. Neurosci Lett 2002, 330:17-20
4. Readhead C, Popko B, Takahashi N, Shine HD, Saavedra RA, Sidman RL, Hood L: Expression of a myelin basic protein gene in transgenic shiverer mice: correction of the dysmyelinating phenotype. Cell 1987, 48:703-712
5. Takahashi M, Tomizawa K, Fujita SC, Sato K, Uchida T, Imahori K: A brain-specific protein p25 is localized and associated with oligodendrocytes, neuropil, and fiber-like structures of the CA3 hippocampal region in the rat brain. J Neurochem 1993, 60:228-235
6. Takahashi M, Tomizawa K, Ishiguro K, Sato K, Omori A, Sato S, Shiratsuchi A, Uchida T, Imahori K: A novel brain-specific 25 kDa protein (p25) is phosphorylated by a Ser/Thr-Pro kinase (TPK II) from tau protein kinase fractions, FEBS Lett 1991, 289:37-43
7. Hlavanda E, Kovacs J, Olah J, Orosz F, Medzihradszky KF, Ovadi J: Brain-specific p25 protein binds to tubulin and microtubules and induces aberrant microtubule assemblies at substoichiometric concentrations. Biochemistry 2002, 41:8657-8664
8. Skjoerringe T, Lundvig DM, Jensen PH, Moos T: P25α/tubulin polymerization promoting protein expression by myelinating oligodendrocytes of the developing rat brain. J Neurochem 2006, 99:333-342
9. Akiyama K, Ichinose S, Omori A, Sakurai Y, Asou H: Study of expression of myelin basic proteins (MBPs) in developing rat brain using a novel antibody reacting with four major isoforms of MBP. J Neurosci Res 2002, 68:19-28
10. Otzen DE, Lundvig DM, Wimmer R, Nielsen LH, Pedersen JR, Jensen PH: p25α is flexible but natively folded and binds tubulin with oligomeric stoichiometry. Protein Sci 2005, 14:1396-1409
11. Lehotzky A, Tirian L, Tokesi N, Lenart P, Szabo B, Kovacs J, Ovadi J: Dynamic targeting of microtubules by TPPP/p25 affects cell survival. J Cell Sci 2004, 117:6249-6259
12. Goedert M, Spillantini MG, Davies SW: Filamentous nerve cell inclusions in neurodegenerative diseases. Curr Opin Neurobiol 1998, 8:619-632
13. Attems J, Quass M, Jellinger KA: Tau and alpha-synuclein brainstem pathology in Alzheimer disease: relation with extrapyramidal signs. Acta Neuropathol (Berl) 2007, 113:53-62
14. Papadopoulos D, Ewans L, Pham-Dinh D, Knott J, Reynolds R: Up-regulation of α-synuclein in neurons and glia in inflammatory demyelinating disease. Mol Cell Neurosci 2006, 31:597-612
15. Saito Y, Suzuki K, Hulette CM, Murayama S: Aberrant phosphorylation of α-synuclein in human Niemann-Pick type C1 disease. J Neuropathol Exp Neurol 2004, 63:323-328
16. Sidransky E: Gaucher disease: complexity in a "simple" disorder. Mol Genet Metab 2004, 83:6-15
17. Suzuki K, Iseki E, Katsuse O, Yamaguchi A, Katsuyama K, Aoki I, Yamanaka S, Kosaka K: Neuronal accumulation of α- and β-synucleins in the brain of a GM2 gangliosidosis mouse model. Neuroreport 2003, 14:551-554
18. Wirths O, Bayer TA: α-Synuclein, Aβ and Alzheimer's disease. Prog Neuropsychcpharmacol Biol Psychiatry 2003, 27:103-108
19. Dickson DW, Liu W, Hardy J, Farrer M, Mehta N, Uitti R, Mark M, Zimmerman T, Golbe L, Sage J, Sima A, D'Amato C, Albin R, Gilman S, Yen SH: Widespread alterations of α-synuclein in multiple system atrophy. Am J Pathol 1999, 155:1241-1251
20. Baker KG, Huang Y, McCann H, Gai WP, Jensen PH, Halliday GM: P25α immunoreactive but α-synuclein immunonegative neuronal inclusions in multiple system atrophy. Acta Neuropathol (Berl) 2006, 111:193-195
21. Wakabayashi K, Yoshimoto M, Tsuji S, Takahashi H: α-Synuclein immunoreactivity in glial cytoplasmic inclusions in multiple system atrophy. Neurosci Lett 1998, 249:180-182
22. Richter-Landsberg C, Gorath M, Trojanowski JQ, Lee VM: α-Synuclein is developmentally expressed in cultured rat brain oligodendrocytes. J Neurosci Res 2000, 62:9-14
23. Shults CW, Rockenstein E, Crews L, Adame A, Mante M, Larrea G, Hashimoto M, Song D, Iwatsubo T, Tsuboi K, Masliah E: Neurological and neurodegenerative alterations in a transgenic mouse model expressing human α-synuclein under oligodendrocyte promoter: implications for multiple system atrophy. J Neurosci 2005, 25:10689-10699
24. Yazawa I, Giasson BI, Sasaki R, Zhang B, Joyce S, Uryu K, Trojanowski JQ, Lee VM: Mouse model of multiple system atrophy α-synuclein expression in oligodendrocytes causes glial and neuronal degeneration. Neuron 2005, 45:847-859
25. Lindersson E, Lundvig D, Petersen C, Madsen P, Nyengaard JR, Hojrup P, Moos T, Otzen D, Gai WP, Blumbergs PC, Jensen PH: p25α stimulates α-synuclein aggregation and is co-localized with aggregated α-synuclein in α-synucleinopathies. J Biol Chem 2005, 280:5703-5715
26. Norton WT, Poduslo SE: Myelination in rat brain: method of myelin isolation. J Neurochem 1973, 21:749-757
27. Su M, Yoshida Y, Hirata Y, Watahiki Y, Nagata K: Primary involvement of the motor area in association with the nigrostriatal pathway in multiple system atrophy: neuropathological and morphometric evaluations. Acta Neuropathol (Berl) 2001, 101:57-64
28. Jellinger KA, Seppi K, Wenning GK: Grading of neuropathology in multiple system atrophy: proposal for a novel scale. Mov Disord 2005, 20(Suppl 12):S29-S36
29. Anderson JP, Walker DE, Goldstein JM, de Laat R, Banducci K, Caccavello RJ, Barbour R, Huang J, Kling K, Lee M, Diep L, Keim PS, Shen X, Chataway T, Schlossmacher MG, Seubert P, Schenk D, Sinha S, Gai WP, Chilcote TJ: Phosphorylation of Ser-129 is the dominant pathological modification of α-synuclein in familial and sporadic Lewy body disease. J Biol Chem 2006, 281:29739-29752
30. Shevchenko A, Wilm M, Vorm O, Jensen ON, Podtelejnikov AV, Neubauer G, Shevchenko A, Mortensen P, Mann M: A strategy for identifying gel-separated proteins in sequence databases by MS alone. Biochem Soc Trans 1996, 24:893-896
31. Hjerno K: PeakErazor: A Windows-Based Program for Improving Peptide Mass Searches. Edited by RM Kamp. Springer Verlag, 2004, pp 359-370
32. Peri S, Steen H, Pandey A: GPMAW - a software tool for analyzing proteins and peptides. Trends Biochem Sci 2001, 26:687-689
33. Takeda A, Hashimoto M, Mallory M, Sundsumo M, Hansen L, Masliah E: C-terminal α-synuclein immunoreactivity in structures other than Lewy bodies in neurodegenerative disorders. Acta Neuropathol (Berl) 2000, 99:296-304
34. Takeda A, Hashimoto M, Mallory M, Sundsumo M, Hansen L, Sisk A, Masliah E: Abnormal distribution of the non-Aβ component of Alzheimer's disease amyloid precursor/α-synuclein in Lewy body disease as revealed by proteinase K and formic acid pretreatment. Lab Invest 1998, 78:1169-1177
35. Halliday GM, Song YJ, Lepar G, Brooks WS, Kwok JB, Kersaitis C, Gregory G, Shepherd CE, Rahimi F, Sohofield PR, Kril JJ: Pick bodies in a family with presenilin-1 Alzheimer's disease. Ann Neurol 2005, 57:139-143
36. McLellan ME, Kajdasz ST, Hyman BT, Bacskai BJ: In vivo imaging of reactive oxygen species specifically associated with thioflavine S-positive amyloid plaques by multiphoton microscopy. J Neurosci 2003, 23:2212-2217
37. Kovács GG, Laszlo L, Kovacs J, Jensen PH, Lindersson E, Botond G, Molnar T, Perczel A, Hudecz F, Mezo G, Erdei A, Tirian L, Lehotzky A, Gelpi E, Budka H, Ovadi J: Natively unfolded tubulin polymerization promoting protein TPPP/p25 is a common marker of α-synucleinopathies. Neurobiol Dis 2004, 17:155-162
38. Papp MI, Kahn JE, Lantos PL: Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J Neurol Sci 1989, 94:79-100
39. Matsuo A, Akiguchi I, Lee GC, McGeer EG, McGeer PL, Kimura J: Myelin degeneration in multiple system atrophy detected by unique antibodies. Am J Pathol 1998, 153:735-744
40. Boiko T, Winckler B: Myelin under construction - teamwork required. J Cell Biol 2006, 172:799-801
41. Sternberger NH, Itoyama Y, Kies MW, Webster H deF: Immunocytochemical method to identify basic protein in myelin-forming oligodendrocytes of newborn rat CNS. J Neurocytol 1978, 7:251-263
42. Oláh J, Tokesi N, Vincze O, Horvath I, Lehotzky A, Erdei A, Szajli E, Medzihradszky KF, Orosz F, Kovacs GG, Ovadi J: Interaction of TPPP/p25 protein with glyceraldehyde-3-phosphate dehydrogenase and their co-localization in Lewy bodies. FEBS Lett 2006, 580:5807-5814
43. Martín CP, Vazquez J, Avila J, Moreno FJ: P24, a glycogen synthase kinase 3 (GSK 3) inhibitor. Biochim Biophys Acta 2002, 1586:113-122
44. Kovács GG, Gelpi E, Lehotzky A, Hoftberger R, Erdei A, Budka H, Ovadi J: The brain-specific protein TPPP/p25 in pathological protein deposits of neurodegenerative diseases. Acta Neuropathol (Berl) 2007, 113:153-161
45. Barbarese E, Brumwell C, Kwon S, Cui H, Carson JH: RNA on the road to myelin. J Neurocytol 1999, 28:263-270
46. Nilsson C, Markenroth Bloch K, Brockstedt S, Latt J, Widner H, Larsson EM: Tracking the neurodegeneration of parkinsonian disorders - a pilot study. Neuroradiology 2007, 49:111-119
47. Shiga K, Yamada K, Yoshikawa K, Mizuno T, Nishimura T, Nagakawa M: Local tissue anisotropy decreases in cerebellopetal fibers and pyramidal tract in MSA. J Neurol 2005, 252:589-596
48. Langerveld AJ, Mihalko D, DeLong C, Walburn J, Ide CF: Gene expression changes in postmortem tissue from the rostral pons of MSA patients. Mov Disord 2007, 22:766-777
49. Vogt IR, Lees AJ, Evert BO, Klockgether T, Bonin M, Wullner U: Transcriptional changes in MSA and PD putamen. Exp Neurol 2006, 199:465-478