Nuclear bodies in neurodegenerative disease

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1783, Issue 11, 2008, Pages 2195-2206

  Woulfe, John ^a,b  

^a UNIVERSITY OF OTTAWA   (Canada)

^b Microbiology   (Canada)

Author keywords

Alzheimer's disease; Frontotemporal dementia; Neurodegenerative disease; Nuclear body; Nuclear inclusion; Spinal muscular atrophy

Indexed keywords

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; CELL FUNCTION; CELL NUCLEUS; CELL NUCLEUS INCLUSION BODY; DEGENERATIVE DISEASE; FRONTOTEMPORAL DEMENTIA; HEREDITARY SPINAL MUSCULAR ATROPHY; HUMAN; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; POLYGLUTAMINOPATHY; PRION DISEASE; PRIORITY JOURNAL; REVIEW; SYNUCLEINOPATHY; TAUOPATHY;

ANIMALS; CELL NUCLEUS; HUMANS; INTRANUCLEAR INCLUSION BODIES; MUSCULAR ATROPHY, SPINAL; NEURODEGENERATIVE DISEASES;

EID: 53249095885     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2008.05.005     Document Type: Review

References (159)

1. Ross C.A., and Poirier M.A. Protein aggregation and neurodegenerative disease. Nat. Med. 10 Suppl (2004) S10-S17
2. Davies S.W., Turmaine M., Cozens B.A., DiFiglia M., Sharp A.H., Ross C.A., Scherzinger E., Wanker E.E., Mangiarini L., and Bates G.P. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 90 (1997) 537-548
3. Becher M.W., Kotzuk J.A., Sharp A.H., Davies S.W., Bates G.P., Price D.L., and Ross C.A. Intranuclear neuronal inclusions in Huntington's disease and dentatorubral and pallidoluysian atrophy: correlation between the density of inclusions and IT15 CAG triplet repeat length. Neurobiol. Dis. 4 (1998) 387-397
4. Woulfe J.M. Abnormalities of the nucleus and nuclear inclusions in neurodegenerative disease: a work in progress. Neuropathol. Appl. Neurobiol. 33 (2007) 2-42
5. Chu C.T., Plowey E.D., Wang Y., Patel V., and Jordan-Sciutto K.L. Location, location, location: altered transcription factor trafficking in neurodegeneration. J. Neuropathol. Exp. Neurol. 66 (2007) 873-883
6. Sergeant N., Sablonniere B., Schraen-Maschke S., Ghestem A., Maurage C.A., Wattez A., Vermersch P., and Delacourte A. Dysregulation of human brain microtubule-associated tau mRNA maturation in myotonic dystrophy type 1. Hum. Mol. Genet. 10 (2001) 2143-2155
7. Lamond A.I., and Sleeman J.E. Nuclear substructure and dynamics. Curr. Biol. 13 (2003) R825-828
8. Borden K.L. Pondering the promyelocytic leukemia protein (PML) puzzle: possible functions for PML nuclear bodies. Mol. Cell. Biol. 22 (2002) 5259-5269
9. Lamond A.I., and Spector D.L. Nuclear speckles: a model for nuclear organelles. Nat. Rev., Mol. Cell Biol. 4 (2003) 605-612
10. Grimwade D., and Solomon E. Characterisation of the PML/RAR alpha rearrangement associated with t(15;17) acute promyelocytic leukaemia. Curr. Top. Microbiol. Immunol. 220 (1997) 81-112
11. Zimber A., Nguyen Q.D., and Gespach C. Nuclear bodies and compartments: functional roles and cellular signalling in health and disease. Cell. Signal. 16 (2004) 1085-1104
12. Strudwick S., and Borden K.L. Finding a role for PML in APL pathogenesis: a critical assessment of potential PML activities. Leukemia 16 (2002) 1906-1917
13. van Koningsbruggen S., Straasheijm K.R., Sterrenburg E., de Graaf N., Dauwerse H.G., Frants R.R., and van der Maarel S.M. FRG1P-mediated aggregation of proteins involved in pre-mRNA processing. Chromosoma 116 (2007) 53-64
14. Francisconi S., Codenotti M., Ferrari-Toninelli G., Uberti D., and Memo M. Preservation of DNA integrity and neuronal degeneration. Brain Res. Brain Res. Rev. 48 (2005) 347-351
15. Valero J., Berciano M.T., Weruaga E., Lafarga M., and Alonso J.R. Pre-neurodegeneration of mitral cells in the pcd mutant mouse is associated with DNA damage, transcriptional repression, and reorganization of nuclear speckles and Cajal bodies. Mol. Cell. Neurosci. 33 (2006) 283-295
16. Harris A., Morgan J.I., Pecot M., Soumare A., Osborne A., and Soares H.D. Regenerating motor neurons express Nna1, a novel ATP/GTP-binding protein related to zinc carboxypeptidases. Mol. Cell. Neurosci. 16 (2000) 578-596
17. Pearn J. Incidence, prevalence, and gene frequency studies of chronic childhood spinal muscular atrophy. J. Med. Genet. 15 (1978) 409-413
18. Melki J., Lefebvre S., Burglen L., Burlet P., Clermont O., Millasseau P., Reboullet S., Benichou B., Zeviani M., Le Paslier D., et al. De novo and inherited deletions of the 5q13 region in spinal muscular atrophies. Science 264 (1994) 1474-1477
19. Lefebvre S., Burglen L., Reboullet S., Clermont O., Burlet P., Viollet L., Benichou B., Cruaud C., Millasseau P., Zeviani M., et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell 80 (1995) 155-165
20. Rochette C.F., Gilbert N., and Simard L.R. SMN gene duplication and the emergence of the SMN2 gene occurred in distinct hominids: SMN2 is unique to Homo sapiens. Hum. Genet. 108 (2001) 255-266
21. Cartegni L., Hastings M.L., Calarco J.A., de Stanchina E., and Krainer A.R. Determinants of exon 7 splicing in the spinal muscular atrophy genes, SMN1 and SMN2. Am. J. Hum. Genet. 78 (2006) 63-77
22. Feldkotter M., Schwarzer V., Wirth R., Wienker T.F., and Wirth B. Quantitative analyses of SMN1 and SMN2 based on real-time lightCycler PCR: fast and highly reliable carrier testing and prediction of severity of spinal muscular atrophy. Am. J. Hum. Genet. 70 (2002) 358-368
23. Kolb S.J., Battle D.J., and Dreyfuss G. Molecular functions of the SMN complex. J. Child Neurol. 22 (2007) 990-994
24. Liu Q., and Dreyfuss G. A novel nuclear structure containing the survival of motor neurons protein. EMBO J. 15 (1996) 3555-3565
25. Coovert D.D., Le T.T., McAndrew P.E., Strasswimmer J., Crawford T.O., Mendell J.R., Coulson S.E., Androphy E.J., Prior T.W., and Burghes A.H. The survival motor neuron protein in spinal muscular atrophy. Hum. Mol. Genet. 6 (1997) 1205-1214
26. Hebert M.D., Szymczyk P.W., Shpargel K.B., and Matera A.G. Coilin forms the bridge between Cajal bodies and SMN, the spinal muscular atrophy protein. Genes Dev. 15 (2001) 2720-2729
27. Lorson C.L., Strasswimmer J., Yao J.M., Baleja J.D., Hahnen E., Wirth B., Le T., Burghes A.H., and Androphy E.J. SMN oligomerization defect correlates with spinal muscular atrophy severity. Nat. Genet. 19 (1998) 63-66
28. Matera A.G., and Frey M.R. Coiled bodies and gems: Janus or gemini?. Am. J. Hum. Genet. 63 (1998) 317-321
29. Girard C., Neel H., Bertrand E., and Bordonne R. Depletion of SMN by RNA interference in HeLa cells induces defects in Cajal body formation. Nucleic Acids Res. 34 (2006) 2925-2932
30. Frugier T., Tiziano F.D., Cifuentes-Diaz C., Miniou P., Roblot N., Dierich A., Le Meur M., and Melki J. Nuclear targeting defect of SMN lacking the C-terminus in a mouse model of spinal muscular atrophy. Hum. Mol. Genet. 9 (2000) 849-858
31. Arrasate M., Mitra S., Schweitzer E.S., Segal M.R., and Finkbeiner S. Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431 (2004) 805-810
32. McCampbell A., Taylor J.P., Taye A.A., Robitschek J., Li M., Walcott J., Merry D., Chai Y., Paulson H., Sobue G., and Fischbeck K.H. CREB-binding protein sequestration by expanded polyglutamine. Hum. Mol. Genet. 9 (2000) 2197-2202
33. Shimohata T., Onodera O., and Tsuji S. Interaction of expanded polyglutamine stretches with nuclear transcription factors leads to aberrant transcriptional regulation in polyglutamine diseases. Neuropathology 20 (2000) 326-333
34. Skinner P.J., Koshy B.T., Cummings C.J., Klement I.A., Helin K., Servadio A., Zoghbi H.Y., and Orr H.T. Ataxin-1 with an expanded glutamine tract alters nuclear matrix-associated structures. Nature 389 (1997) 971-974
35. Tait D., Riccio M., Sittler A., Scherzinger E., Santi S., Ognibene A., Maraldi N.M., Lehrach H., and Wanker E.E. Ataxin-3 is transported into the nucleus and associates with the nuclear matrix. Hum. Mol. Genet. 7 (1998) 991-997
36. Chai Y., Koppenhafer S.L., Shoesmith S.J., Perez M.K., and Paulson H.L. Evidence for proteasome involvement in polyglutamine disease: localization to nuclear inclusions in SCA3/MJD and suppression of polyglutamine aggregation in vitro. Hum. Mol. Genet. 8 (1999) 673-682
37. Kaytor M.D., and Warren S.T. Aberrant protein deposition and neurological disease. J. Biol. Chem. 274 (1999) 37507-37510
38. Yamada M., Sato T., Shimohata T., Hayashi S., Igarashi S., Tsuji S., and Takahashi H. Interaction between neuronal intranuclear inclusions and promyelocytic leukemia protein nuclear and coiled bodies in CAG repeat diseases. Am. J. Pathol. 159 (2001) 1785-1795
39. Yamada M., Wood J.D., Shimohata T., Hayashi S., Tsuji S., Ross C.A., and Takahashi H. Widespread occurrence of intranuclear atrophin-1 accumulation in the central nervous system neurons of patients with dentatorubral-pallidoluysian atrophy. Ann. Neurol. 49 (2001) 14-23
40. Takahashi J., Fujigasaki H., Zander C., El Hachimi K.H., Stevanin G., Durr A., Lebre A.S., Yvert G., Trottier Y., The H., Hauw J.J., Duyckaerts C., and Brice A. Two populations of neuronal intranuclear inclusions in SCA7 differ in size and promyelocytic leukaemia protein content. Brain 125 (2002) 1534-1543
41. Takahashi J., Fujigasaki H., Iwabuchi K., Bruni A.C., Uchihara T., El Hachimi K.H., Stevanin G., Durr A., Lebre A.S., Trottier Y., de The H., Tanaka J., Hauw J.J., Duyckaerts C., and Brice A. PML nuclear bodies and neuronal intranuclear inclusion in polyglutamine diseases. Neurobiol. Dis. 13 (2003) 230-237
42. Takahashi-Fujigasaki J., Arai K., Funata N., and Fujigasaki H. SUMOylation substrates in neuronal intranuclear inclusion disease. Neuropathol. Appl. Neurobiol. 32 (2006) 92-100
43. Fu L., Gao Y.S., Tousson A., Shah A., Chen T.L., Vertel B.M., and Sztul E. Nuclear aggresomes form by fusion of PML-associated aggregates. Mol. Biol. Cell 16 (2005) 4905-4917
44. Dovey C.L., Varadaraj A., Wyllie A.H., and Rich T. Stress responses of PML nuclear domains are ablated by ataxin-1 and other nucleoprotein inclusions. J. Pathol. 203 (2004) 877-883
45. Freemont P.S. RING for destruction?. Curr. Biol. 10 (2000) R84-87
46. Eskiw C.H., Dellaire G., Mymryk J.S., and Bazett-Jones D.P. Size, position and dynamic behavior of PML nuclear bodies following cell stress as a paradigm for supramolecular trafficking and assembly. J. Cell Sci. 116 (2003) 4455-4466
47. Sun J., Xu H., Negi S., Subramony S.H., and Hebert M.D. Differential effects of polyglutamine proteins on nuclear organization and artificial reporter splicing. J. Neurosci. Res. 85 (2007) 2306-2317
48. Navascues J., Bengoechea R., Tapia O., Vaque J.P., Lafarga M., and Berciano M.T. Characterization of a new SUMO-1 nuclear body (SNB) enriched in pCREB, CBP, c-Jun in neuron-like UR61 cells. Chromosoma 116 (2007) 441-451
49. Muller S., Hoege C., Pyrowolakis G., and Jentsch S. SUMO, ubiquitin's mysterious cousin. Nat. Rev., Mol. Cell Biol. 2 (2001) 202-210
50. Girdwood D.W., Tatham M.H., and Hay R.T. SUMO and transcriptional regulation. Semin. Cell Dev. Biol. 15 (2004) 201-210
51. Johnson E.S. Protein modification by SUMO. Annu. Rev. Biochem. 73 (2004) 355-382
52. Dorval V., and Fraser P.E. SUMO on the road to neurodegeneration. Biochim. Biophys. Acta 1773 (2007) 694-706
53. Lieberman A.P. SUMO, a ubiquitin-like modifier implicated in neurodegeneration. Exp. Neurol. 185 (2004) 204-207
54. Pountney D.L., Huang Y., Burns R.J., Haan E., Thompson P.D., Blumbergs P.C., and Gai W.P. SUMO-1 marks the nuclear inclusions in familial neuronal intranuclear inclusion disease. Exp. Neurol. 184 (2003) 436-446
55. Villagra N.T., Navascues J., Casafont I., Val-Bernal J.F., Lafarga M., and Berciano M.T. The PML-nuclear inclusion of human supraoptic neurons: a new compartment with SUMO-1- and ubiquitin-proteasome-associated domains. Neurobiol. Dis. 21 (2006) 181-193
56. Woulfe J. PML-immunoreactive neuronal intranuclear rodlets in the human brain. Neuropathol. Appl. Neurobiol. 26 (2000) 161-171
57. Hardy J., and Myers A. Genetic variability in expression of proteins and the risk of sporadic neurologic diseases. Neurology 68 (2007) 632-633
58. Guyant-Marechal L., Rovelet-Lecrux A., Goumidi L., Cousin E., Hannequin D., Raux G., Penet C., Ricard S., Mace S., Amouyel P., Deleuze J.F., Frebourg T., Brice A., Lambert J.C., and Campion D. Variations in the APP gene promoter region and risk of Alzheimer disease. Neurology 68 (2007) 684-687
59. Metuzals J., Robitaille Y., Houghton S., Gauthier S., and Leblanc R. Paired helical filaments and the cytoplasmic-nuclear interface in Alzheimer's disease. J. Neurocytol. 17 (1988) 827-833
60. Sheffield L.G., Miskiewicz H.B., Tannenbaum L.B., and Mirra S.S. Nuclear pore complex proteins in Alzheimer disease. J. Neuropathol. Exp. Neurol. 65 (2006) 45-54
61. al-Maghrabi J., Tierney M., and Ang L.C. Glial intranuclear inclusion bodies in a patient with Alzheimer's disease. Acta Neuropathol. (Berl) 99 (2000) 695-698
62. Toper S., Bannister C.M., Lincoln J., Mann D.M., and Yates P.O. Nuclear inclusions in Alzheimer's disease. Neuropathol. Appl. Neurobiol. 6 (1980) 245-253
63. Selkoe D.J. Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81 (2001) 741-766
64. Selkoe D.J. Translating cell biology into therapeutic advances in Alzheimer's disease. Nature 399 (1999) A23-31
65. De Strooper B., and Annaert W. Proteolytic processing and cell biological functions of the amyloid precursor protein. J. Cell Sci. 113 Pt 11 (2000) 1857-1870
66. Cao X., and Sudhof T.C. Dissection of amyloid-beta precursor protein-dependent transcriptional transactivation. J. Biol. Chem. 279 (2004) 24601-24611
67. Cao X., and Sudhof T.C. A transcriptionally [correction of transcriptively] active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293 (2001) 115-120
68. Muresan Z., and Muresan V. A phosphorylated, carboxy-terminal fragment of beta-amyloid precursor protein localizes to the splicing factor compartment. Hum. Mol. Genet. 13 (2004) 475-488
69. Robakis N.K. An Alzheimer's disease hypothesis based on transcriptional dysregulation. Amyloid 10 (2003) 80-85
70. Sajdel-Sulkowska E.M., and Marotta C.A. Alzheimer's disease brain: alterations in RNA levels and in a ribonuclease-inhibitor complex. Science 225 (1984) 947-949
71. Mizukami K., Ishikawa M., Iwakiri M., Ikonomovic M.D., Dekosky S.T., Kamma H., and Asada T. Immunohistochemical study of the hnRNP A2 and B1 in the hippocampal formations of brains with Alzheimer's disease. Neurosci. Lett. 386 (2005) 111-115
72. Rouaux C., Loeffler J.P., and Boutillier A.L. Targeting CREB-binding protein (CBP) loss of function as a therapeutic strategy in neurological disorders. Biochem. Pharmacol. 68 (2004) 1157-1164
73. Rouaux C., Jokic N., Mbebi C., Boutillier S., Loeffler J.P., and Boutillier A.L. Critical loss of CBP/p300 histone acetylase activity by caspase-6 during neurodegeneration. EMBO J. 22 (2003) 6537-6549
74. Saura C.A., Choi S.Y., Beglopoulos V., Malkani S., Zhang D., Shankaranarayana Rao B.S., Chattarji S., Kelleher III R.J., Kandel E.R., Duff K., Kirkwood A., and Shen J. Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 42 (2004) 23-36
75. Song W., Nadeau P., Yuan M., Yang X., Shen J., and Yankner B.A. Proteolytic release and nuclear translocation of Notch-1 are induced by presenilin-1 and impaired by pathogenic presenilin-1 mutations. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 6959-6963
76. Maccioni R.B., Munoz J.P., and Barbeito L. The molecular bases of Alzheimer's disease and other neurodegenerative disorders. Arch. Med. Res. 32 (2001) 367-381
77. Drubin D.G., and Kirschner M.W. Tau protein function in living cells. J. Cell Biol. 103 (1986) 2739-2746
78. Brady R.M., Zinkowski R.P., and Binder L.I. Presence of tau in isolated nuclei from human brain. Neurobiol. Aging 16 (1995) 479-486
79. Lu Q., and Wood J.G. Functional studies of Alzheimer's disease tau protein. J. Neurosci. 13 (1993) 508-515
80. Lambert M.P., Sabo S., Zhang C., Enam S.A., and Klein W.L. Constitutive Alzheimer's-type tau epitopes in a neuritogenic rat CNS cell line. Neurobiol. Aging 16 (1995) 583-589
81. Thurston V.C., Zinkowski R.P., and Binder L.I. Tau as a nucleolar protein in human nonneural cells in vitro and in vivo. Chromosoma 105 (1996) 20-30
82. Hua Q., and He R.Q. Tau could protect DNA double helix structure. Biochim. Biophys. Acta 1645 (2003) 205-211
83. Sjoberg M.K., Shestakova E., Mansuroglu Z., Maccioni R.B., and Bonnefoy E. Tau protein binds to pericentromeric DNA: a putative role for nuclear tau in nucleolar organization. J. Cell Sci. 119 (2006) 2025-2034
84. Carmo-Fonseca M., Mendes-Soares L., and Campos I. To be or not to be in the nucleolus. Nat. Cell Biol. 2 (2000) E107-112
85. Hua Q., and He R.Q. Effect of phosphorylation and aggregation on tau binding to DNA. Prot. Peptide Letters 9 (2002) 349-357
86. da Silva A.M., Payao S.L., Borsatto B., Bertolucci P.H., and Smith M.A. Quantitative evaluation of the rRNA in Alzheimer's disease. Mech. Ageing Dev. 120 (2000) 57-64
87. Payao S.L., Smith M.A., Winter L.M., and Bertolucci P.H. Ribosomal RNA in Alzheimer's disease and aging. Mech. Ageing Dev. 105 (1998) 265-272
88. Gertz H.J., Schoknecht G., Kruger H., and Cervos-Navarro J. Stability of cell size and nucleolar size in tangle-bearing neurons of the hippocampus in Alzheimer's disease. Brain Res. 487 (1989) 373-375
89. Donmez-Altuntas H., Akalin H., Karaman Y., Demirtas H., Imamoglu N., and Ozkul Y. Evaluation of the nucleolar organizer regions in Alzheimer's disease. Gerontology 51 (2005) 297-301
90. Lu W., Tang H., Fan M., Mi R., Wang L., and Jia J. Research on nucleolar organizer regions of hippocampal neuron in Alzheimer's disease. Chin. Med. J. (Engl) 111 (1998) 282-284
91. Trinczek B., Biernat J., Baumann K., Mandelkow E.M., and Mandelkow E. Domains of tau protein, differential phosphorylation, and dynamic instability of microtubules. Mol. Biol. Cell 6 (1995) 1887-1902
92. D'Souza I., and Schellenberg G.D. Determinants of 4-repeat tau expression. Coordination between enhancing and inhibitory splicing sequences for exon 10 inclusion. J. Biol. Chem. 275 (2000) 17700-17709
93. Grimes C.A., and Jope R.S. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog. Neurobiol. 65 (2001) 391-426
94. Ferrer I., Barrachina M., and Puig B. Glycogen synthase kinase-3 is associated with neuronal and glial hyperphosphorylated tau deposits in Alzheimer's disease, Pick's disease, progressive supranuclear palsy and corticobasal degeneration. Acta Neuropathol. (Berl) 104 (2002) 583-591
95. Hernandez F., Perez M., Lucas J.J., Mata A.M., Bhat R., and Avila J. Glycogen synthase kinase-3 plays a crucial role in tau exon 10 splicing and intranuclear distribution of SC35. Implications for Alzheimer's disease. J. Biol. Chem. 279 (2004) 3801-3806
96. Woulfe J., and Munoz D. Tubulin immunoreactive neuronal intranuclear inclusions in the human brain. Neuropathol. Appl. Neurobiol. 26 (2000) 161-171
97. Seite R., Mei N., and Vuillet-Luciani J. Effect of electrical stimulation on nuclear microfilaments and microtubules of sympathetic neurons submitted to cycloheximide. Brain Res. 50 (1973) 419-423
98. Lafarga M., Berciano M.T., and Andres M.A. Protein-synthesis inhibition induces perichromatin granule accumulation and intranuclear rodlet formation in osmotically stimulated supraoptic neurons. Anat. Embryol. (Berl) 187 (1993) 363-369
99. Woulfe J., Gray D., Prichett-Pejic W., Munoz D.G., and Chretien M. Intranuclear rodlets in the substantia nigra: interactions with marinesco bodies, ubiquitin, and promyelocytic leukemia protein. J. Neuropathol. Exp. Neurol. 63 (2004) 1200-1207
100. Masurovsky E.B., Benitez H.H., Kim S.U., and Murray M.R. Origin, development, and nature of intranuclear rodlets and associated bodies in chicken sympathetic neurons. J. Cell Biol. 44 (1970) 172-191
101. Woulfe J.M., Hammond R., Richardson B., Sooriabalan D., Parks W., Rippstein P., and Munoz D.G. Reduction of neuronal intranuclear rodlets immunoreactive for tubulin and glucocorticoid receptor in Alzheimer's disease. Brain Pathol. 12 (2002) 300-307
102. Beyer K., and Ariza A. Protein aggregation mechanisms in synucleinopathies: commonalities and differences. J. Neuropathol. Exp. Neurol. 66 (2007) 965-974
103. Maroteaux L., Campanelli J.T., and Scheller R.H. Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J. Neurosci. 8 (1988) 2804-2815
104. Goers J., Manning-Bog A.B., McCormack A.L., Millett I.S., Doniach S., Di Monte D.A., Uversky V.N., and Fink A.L. Nuclear localization of alpha-synuclein and its interaction with histones. Biochemistry 42 (2003) 8465-8471
105. McLean P.J., Ribich S., and Hyman B.T. Subcellular localization of alpha-synuclein in primary neuronal cultures: effect of missense mutations. J. Neural Transm., Suppl. (2000) 53-63
106. Nishie M., Mori F., Yoshimoto M., Takahashi H., and Wakabayashi K. A quantitative investigation of neuronal cytoplasmic and intranuclear inclusions in the pontine and inferior olivary nuclei in multiple system atrophy. Neuropathol. Appl. Neurobiol. 30 (2004) 546-554
107. Masliah E., Rockenstein E., Veinbergs I., Mallory M., Hashimoto M., Takeda A., Sagara Y., Sisk A., and Mucke L. Dopaminergic loss and inclusion body formation in alpha-synuclein mice: implications for neurodegenerative disorders. Science 287 (2000) 1265-1269
108. Kontopoulos E., Parvin J.D., and Feany M.B. Alpha-synuclein acts in the nucleus to inhibit histone acetylation and promote neurotoxicity. Hum. Mol. Genet. 15 (2006) 3012-3023
109. Specht C.G., Tigaret C.M., Rast G.F., Thalhammer A., Rudhard Y., and Schoepfer R. Subcellular localisation of recombinant alpha- and gamma-synuclein. Mol. Cell. Neurosci. 28 (2005) 326-334
110. Gertz H.J., Siegers A., and Kuchinke J. Stability of cell size and nucleolar size in Lewy body containing neurons of substantia nigra in Parkinson's disease. Brain Res. 637 (1994) 339-341
111. Bancher C., Lassmann H., Budka H., Jellinger K., Grundke-Iqbal I., Iqbal K., Wiche G., Seitelberger F., and Wisniewski H.M. An antigenic profile of Lewy bodies: immunocytochemical indication for protein phosphorylation and ubiquitination. J. Neuropathol. Exp. Neurol. 48 (1989) 81-93
112. Kettner M., Willwohl D., Hubbard G.B., Rub U., Dick Jr. E.J., Cox A.B., Trottier Y., Auburger G., Braak H., and Schultz C. Intranuclear aggregation of nonexpanded ataxin-3 in marinesco bodies of the nonhuman primate substantia nigra. Exp. Neurol. 176 (2002) 117-121
113. Kumada S., Uchihara T., Hayashi M., Nakamura A., Kikuchi E., Mizutani T., and Oda M. Promyelocytic leukemia protein is redistributed during the formation of intranuclear inclusions independent of polyglutamine expansion: an immunohistochemical study on Marinesco bodies. J. Neuropathol. Exp. Neurol. 61 (2002) 984-991
114. Takahashi-Fujigasaki J., and Fujigasaki H. Histone deacetylase (HDAC) 4 involvement in both Lewy and Marinesco bodies. Neuropathol. Appl. Neurobiol. 32 (2006) 562-566
115. Yuen P., and Baxter D.W. The morphology of Marinesco bodies (paranucleolar corpuscles) in the melanin-pigmented nuclei of the brain-stem. J. Neurol. Neurosurg. Psychiatry 26 (1963) 178-183
116. Hirai S., Morimatsu M., Muramatsu A., Eto F., and Yoshikawa M. Aging of the substantia nigra, with special reference to Marinesco body. Nippon. Ronen. Igakkai. Zasshi. 14 (1977) 6-13
117. Fujigasaki H., Uchihara T., Takahashi J., Matsushita H., Nakamura A., Koyano S., Iwabuchi K., Hirai S., and Mizusawa H. Preferential recruitment of ataxin-3 independent of expanded polyglutamine: an immunohistochemical study on Marinesco bodies. J. Neurol. Neurosurg. Psychiatry 71 (2001) 518-520
118. Kanaan N.M., Kordower J.H., and Collier T.J. Age-related accumulation of Marinesco bodies and lipofuscin in rhesus monkey midbrain dopamine neurons: relevance to selective neuronal vulnerability. J. Comp. Neurol. 502 (2007) 683-700
119. Beach T.G., Walker D.G., Sue L.I., Newell A., Adler C.C., and Joyce J.N. Substantia nigra Marinesco bodies are associated with decreased striatal expression of dopaminergic markers. J. Neuropathol. Exp. Neurol. 63 (2004) 329-337
120. Tetrud J.W., and Langston J.W. MPTP-induced parkinsonism as a model for Parkinson's disease. Acta Neurol. Scand., Suppl. 126 (1989) 35-40
121. Lamba W., Prichett W., Munoz D., Park D.S., and Woulfe J.M. MPTP induces intranuclear rodlet formation in midbrain dopaminergic neurons. Brain Res. 1066 (2005) 86-91
122. Nakamura A., Kitami T., Mori H., Mizuno Y., and Hattori N. Nuclear localization of the 20S proteasome subunit in Parkinson's disease. Neurosci. Lett. 406 (2006) 43-48
123. Neary D., Snowden J.S., Gustafson L., Passant U., Stuss D., Black S., Freedman M., Kertesz A., Robert P.H., Albert M., Boone K., Miller B.L., Cummings J., and Benson D.F. Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 51 (1998) 1546-1554
124. McKhann G.M., Albert M.S., Grossman M., Miller B., Dickson D., and Trojanowski J.Q. Clinical and pathological diagnosis of frontotemporal dementia: report of the work group on frontotemporal dementia and Pick's disease. Arch. Neurol. 58 (2001) 1803-1809
125. Chow T.W., Miller B.L., Hayashi V.N., and Geschwind D.H. Inheritance of frontotemporal dementia. Arch. Neurol. 56 (1999) 817-822
126. Josephs K.A., Holton J.L., Rossor M.N., Godbolt A.K., Ozawa T., Strand K., Khan N., Al-Sarraj S., and Revesz T. Frontotemporal lobar degeneration and ubiquitin immunohistochemistry. Neuropathol. Appl. Neurobiol. 30 (2004) 369-373
127. Mitsuyama Y. Presenile dementia with motor neuron disease in Japan: clinico-pathological review of 26 cases. J. Neurol. Neurosurg. Psychiatry 47 (1984) 953-959
128. Jackson M., Lennox G., and Lowe J. Motor neurone disease-inclusion dementia. Neurodegeneration 5 (1996) 339-350
129. Kovach M.J., Waggoner B., Leal S.M., Gelber D., Khardori R., Levenstien M.A., Shanks C.A., Gregg G., Al-Lozi M.T., Miller T., Rakowicz W., Lopate G., Florence J., Glosser G., Simmons Z., Morris J.C., Whyte M.P., Pestronk A., and Kimonis V.E. Clinical delineation and localization to chromosome 9p13.3-p12 of a unique dominant disorder in four families: hereditary inclusion body myopathy, Paget disease of bone, and frontotemporal dementia. Mol. Genet. Metab. 74 (2001) 458-475
130. Josephs K.A., Holton J.L., Rossor M.N., Braendgaard H., Ozawa T., Fox N.C., Petersen R.C., Pearl G.S., Ganguly M., Rosa P., Laursen H., Parisi J.E., Waldemar G., Quinn N.P., Dickson D.W., and Revesz T. Neurofilament inclusion body disease: a new proteinopathy?. Brain 126 (2003) 2291-2303
131. Cairns N.J., Grossman M., Arnold S.E., Burn D.J., Jaros E., Perry R.H., Duyckaerts C., Stankoff B., Pillon B., Skullerud K., Cruz-Sanchez F.F., Bigio E.H., Mackenzie I.R., Gearing M., Juncos J.L., Glass J.D., Yokoo H., Nakazato Y., Mosaheb S., Thorpe J.R., Uryu K., Lee V.M., and Trojanowski J.Q. Clinical and neuropathologic variation in neuronal intermediate filament inclusion disease. Neurology 63 (2004) 1376-1384
132. Mackenzie I.R., and Feldman H.H. Ubiquitin immunohistochemistry suggests classic motor neuron disease, motor neuron disease with dementia, and frontotemporal dementia of the motor neuron disease type represent a clinicopathologic spectrum. J. Neuropathol. Exp. Neurol. 64 (2005) 730-739
133. Woulfe J., Kertesz A., and Munoz D.G. Frontotemporal dementia with ubiquitinated cytoplasmic and intranuclear inclusions. Acta Neuropathol. (Berl) 102 (2001) 94-102
134. Mackenzie I.R., Baker M., West G., Woulfe J., Qadi N., Gass J., Cannon A., Adamson J., Feldman H., Lindholm C., Melquist S., Pettman R., Sadovnick A.D., Dwosh E., Whiteheart S.W., Hutton M., and Pickering-Brown S.M. A family with tau-negative frontotemporal dementia and neuronal intranuclear inclusions linked to chromosome 17. Brain 129 (2006) 853-867
135. Pirici D., Vandenberghe R., Rademakers R., Dermaut B., Cruts M., Vennekens K., Cuijt I., Lubke U., Ceuterick C., Martin J.J., Van Broeckhoven C., and Kumar-Singh S. Characterization of ubiquitinated intraneuronal inclusions in a novel Belgian frontotemporal lobar degeneration family. J. Neuropathol. Exp. Neurol. 65 (2006) 289-301
136. Mackenzie I.R., and Feldman H. Neuronal intranuclear inclusions distinguish familial FTD-MND type from sporadic cases. Acta Neuropathol. (Berl) 105 (2003) 543-548
137. Baker M., Mackenzie I.R., Pickering-Brown S.M., Gass J., Rademakers R., Lindholm C., Snowden J., Adamson J., Sadovnick A.D., Rollinson S., Cannon A., Dwosh E., Neary D., Melquist S., Richardson A., Dickson D., Berger Z., Eriksen J., Robinson T., Zehr C., Dickey C.A., Crook R., McGowan E., Mann D., Boeve B., Feldman H., and Hutton M. Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 442 (2006) 916-919
138. Cruts M., Gijselinck I., van der Zee J., Engelborghs S., Wils H., Pirici D., Rademakers R., Vandenberghe R., Dermaut B., Martin J.J., van Duijn C., Peeters K., Sciot R., Santens P., De Pooter T., Mattheijssens M., Van den Broeck M., Cuijt I., Vennekens K., De Deyn P.P., Kumar-Singh S., and Van Broeckhoven C. Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 442 (2006) 920-924
139. He Z., and Bateman A. Progranulin (granulin-epithelin precursor, PC-cell-derived growth factor, acrogranin) mediates tissue repair and tumorigenesis. J. Mol. Med. 81 (2003) 600-612
140. Skibinski G., Parkinson N.J., Brown J.M., Chakrabarti L., Lloyd S.L., Hummerich H., Nielsen J.E., Hodges J.R., Spillantini M.G., Thusgaard T., Brandner S., Brun A., Rossor M.N., Gade A., Johannsen P., Sorensen S.A., Gydesen S., Fisher E.M., and Collinge J. Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat. Genet. 37 (2005) 806-808
141. Vance C., Al-Chalabi A., Ruddy D., Smith B.N., Hu X., Sreedharan J., Siddique T., Schelhaas H.J., Kusters B., Troost D., Baas F., de Jong V., and Shaw C.E. Familial amyotrophic lateral sclerosis with frontotemporal dementia is linked to a locus on chromosome 9p13.2-21.3. Brain 129 (2006) 868-876
142. Morita M., Al-Chalabi A., Andersen P.M., Hosler B., Sapp P., Englund E., Mitchell J.E., Habgood J.J., de Belleroche J., Xi J., Jongjaroenprasert W., Horvitz H.R., Gunnarsson L.G., and Brown Jr. R.H. A locus on chromosome 9p confers susceptibility to ALS and frontotemporal dementia. Neurology 66 (2006) 839-844
143. Watts G.D., Wymer J., Kovach M.J., Mehta S.G., Mumm S., Darvish D., Pestronk A., Whyte M.P., and Kimonis V.E. Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nat. Genet. 36 (2004) 377-381
144. Woodman P.G. p97, a protein coping with multiple identities. J. Cell Sci. 116 (2003) 4283-4290
145. Wang Q., Song C., and Li C.C. Molecular perspectives on p97-VCP: progress in understanding its structure and diverse biological functions. J. Struct. Biol. 146 (2004) 44-57
146. Neumann M., Sampathu D.M., Kwong L.K., Truax A.C., Micsenyi M.C., Chou T.T., Bruce J., Schuck T., Grossman M., Clark C.M., McCluskey L.F., Miller B.L., Masliah E., Mackenzie I.R., Feldman H., Feiden W., Kretzschmar H.A., Trojanowski J.Q., and Lee V.M. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314 (2006) 130-133
147. Neumann M., Mackenzie I.R., Cairns N.J., Boyer P.J., Markesbery W.R., Smith C.D., Taylor J.P., Kretzschmar H.A., Kimonis V.E., and Forman M.S. TDP-43 in the ubiquitin pathology of frontotemporal dementia with VCP gene mutations. J. Neuropathol. Exp. Neurol. 66 (2007) 152-157
148. Zhang Y.J., Xu Y.F., Dickey C.A., Buratti E., Baralle F., Bailey R., Pickering-Brown S., Dickson D., and Petrucelli L. Progranulin mediates caspase-dependent cleavage of TAR DNA binding protein-43. J. Neurosci. 27 (2007) 10530-10534
149. Buratti E., Dork T., Zuccato E., Pagani F., Romano M., and Baralle F.E. Nuclear factor TDP-43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping. EMBO J. 20 (2001) 1774-1784
150. Buratti E., and Baralle F.E. Characterization and functional implications of the RNA binding properties of nuclear factor TDP-43, a novel splicing regulator of CFTR exon 9. J. Biol. Chem. 276 (2001) 36337-36343
151. Wang I.F., Reddy N.M., and Shen C.K. Higher order arrangement of the eukaryotic nuclear bodies. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 13583-13588
152. Neumann M., Igaz L.M., Kwong L.K., Nakashima-Yasuda H., Kolb S.J., Dreyfuss G., Kretzschmar H.A., Trojanowski J.Q., and Lee V.M. Absence of heterogeneous nuclear ribonucleoproteins and survival motor neuron protein in TDP-43 positive inclusions in frontotemporal lobar degeneration. Acta Neuropathol. 113 (2007) 543-548
153. Mitchell J.D., and Borasio G.D. Amyotrophic lateral sclerosis. Lancet 369 (2007) 2031-2041
154. Sreedharan J., Blair I.P., Tripathi V.B., Hu X., Vance C., Rogelj B., Ackerley S., Durnall J.C., Williams K.L., Buratti E., Baralle F., de Belleroche J., Mitchell J.D., Leigh P.N., Al-Chalabi A., Miller C.C., Nicholson G., and Shaw C.E. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319 (2008) 1668-1672
155. Sanelli T., Xiao S., Horne P., Bilbao J., Zinman L., and Robertson J. Evidence that TDP-43 is not the major ubiquitinated target within the pathological inclusions of amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 66 (2007) 1147-1153
156. Kakita A., Oyanagi K., Nagai H., and Takahashi H. Eosinophilic intranuclear inclusions in the hippocampal pyramidal neurons of a patient with amyotrophic lateral sclerosis. Acta Neuropathol. (Berl) 93 (1997) 532-536
157. Seilhean D., Takahashi J., El Hachimi K.H., Fujigasaki H., Lebre A.S., Biancalana V., Durr A., Salachas F., Hogenhuis J., de The H., Hauw J.J., Meininger V., Brice A., and Duyckaerts C. Amyotrophic lateral sclerosis with neuronal intranuclear protein inclusions. Acta Neuropathol. (Berl) 108 (2004) 81-87
158. Gibb S.L., Boston-Howes W., Lavina Z.S., Gustincich S., Brown Jr. R.H., Pasinelli P., and Trotti D. A caspase-3-cleaved fragment of the glial glutamate transporter EAAT2 is sumoylated and targeted to promyelocytic leukemia nuclear bodies in mutant SOD1-linked amyotrophic lateral sclerosis. J. Biol. Chem. 282 (2007) 32480-32490
159. Meaburn K.J., and Misteli T. Cell biology: chromosome territories. Nature 445 (2007) 379-781