Widespread nuclear and cytoplasmic accumulation of mutant androgen receptor in SBMA patients

Brain

Volumn 128, Issue 3, 2005, Pages 659-670

  Adachi, Hiroaki ^a   Katsuno, Masahisa ^a   Minamiyama, Makoto ^a   Waza, Masahiro ^a   Sang, Chen ^a   Nakagomi, Yuji ^b   Kobayashi, Yasushi ^a   Tanaka, Fumiaki ^a   Doyu, Manabu ^a   Inukai, Akira ^a   Yoshida, Mari ^c   Hashizume, Yoshio ^c   Sobue, Gen ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b AICHI MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c AICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

Diffuse nuclear accumulation; Nuclear inclusion, cytoplasmic accumulation; Polyglutamine; Spinal and bulbar muscular atrophy

Indexed keywords

ANDROGEN RECEPTOR; CREATINE KINASE; GLUCOSE; POLYGLUTAMINE; PEPTIDE;

ADULT; AGED; ARTICLE; CAUSE OF DEATH; CELL INCLUSION; CELL NUCLEUS INCLUSION BODY; CLINICAL ARTICLE; GENE MUTATION; GOLGI COMPLEX; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KENNEDY DISEASE; MALE; MOTONEURON; MUSCLE WEAKNESS; ONSET AGE; PRIORITY JOURNAL; SENSORY NERVE CELL; STATISTICAL ANALYSIS; TRANSGENIC MOUSE; CELL NUCLEUS; CELL ORGANELLE; CYTOPLASM; ENZYME IMMUNOASSAY; GENETICS; METABOLISM; MIDDLE AGED; MUTATION; PATHOLOGY; SPINAL MUSCULAR ATROPHY; TISSUE DISTRIBUTION; ULTRASTRUCTURE;

AGED; AGED, 80 AND OVER; CELL NUCLEUS; CYTOPLASM; HUMANS; IMMUNOENZYME TECHNIQUES; INTRANUCLEAR INCLUSION BODIES; MALE; MIDDLE AGED; MUSCULAR ATROPHY, SPINAL; MUTATION; ORGANELLES; PEPTIDES; RECEPTORS, ANDROGEN; TISSUE DISTRIBUTION;

EID: 20144362557     PISSN: 00068950     EISSN: None     Source Type: Journal    
DOI: 10.1093/brain/awh381     Document Type: Article

References (54)

1. Adachi H, Kume A, Li M, Nakagomi Y, Niwa H, Do J, et al. Transgenic mice with an expanded CAG repeat controlled by the human AR promoter show polyglutamine nuclear inclusions and neuronal dysfunction without neuronal cell death. Hum Mol Genet 2001; 10: 1039-48.
2. Adachi H, Katsuno M, Minamiyama M, Sang C, Pagoulatos G, Angelidis C, et al. Heat shock protein 70 chaperone overexpression ameliorates phenotypes of the spinal and bulbar muscular atrophy transgenic mouse model by reducing nuclear-localized mutant androgen receptor protein. J Neurosci 2003; 23: 2203-11.
3. Arbizu T, Santamaria J, Gomez JM, Quilez A, Serra JP. A family with adult spinal and bulbar muscular atrophy, X-linked inheritance and associated testicular failure. J Neurol Sci 1983; 59: 371-82.
4. Bates G. Huntingtin aggregation and toxicity in Huntington's disease. Lancet 2003; 361: 1642-4.
5. Chevalier-Larsen ES, O'Brien CJ, Wang H, Jenkins SC, Holder L, Lieberman AP, et al. Castration restores function and neurofilament alterations of aged symptomatic males in a transgenic mouse model of spinal and bulbar muscular atrophy. J Neurosci 2004; 24: 4778-86.
6. Doyu M, Sobue G, Mukai E, Kachi T, Yasuda T, Mitsuma T, et al. Severity of X-linked recessive bulbospinal neuronopathy correlates with size of the tandem CAG repeat in androgen receptor gene. Ann Neurol 1992; 32: 707-10.
7. Garden GA, Libby RT, Fu YH, Kinoshita Y, Huang J, Possin DE, et al. Polyglutamine-expanded ataxin-7 promotes non-cell-autonomous Purkinje cell degeneration and displays proteolytic cleavage in ataxic transgenic mice. J Neurosci 2002; 22: 4897-905.
8. Huynh DP, Yang HT, Vakharia H, Nguyen D, Pulst SM. Expansion of the polyQ repeat in ataxin-2 alters its Golgi localization, disrupts the Golgi complex and causes cell death. Hum Mol Genet 2003; 12: 1485-96.
9. Igarashi S, Tanno Y, Onodera O, Yamazaki M, Sato S, Ishikawa A, et al. Strong correlation between the number of CAG repeats in androgen receptor genes and the clinical onset of features of spinal and bulbar muscular atrophy. Neurology 1992; 42: 2300-2.
10. Ishisaka R, Utsumi T, Yabuki M, Kanno T, Furuno T, Inoue M, et al. Activation of caspase-3-like protease by digitonin-treated lysosomes. FEBS Lett 1998; 435: 233-6.
11. Katsuno M, Adachi H, Kume A, Li M, Nakagomi Y, Niwa H, et al. Testosterone reduction prevents phenotypic expression in a transgenic mouse model of spinal and bulbar muscular atrophy. Neuron 2002; 35: 843-54.
12. Katsuno M, Adachi H, Doyu M, Minamiyama M, Sang C, Kobayashi Y, et al. Leuprorelin rescues polyglutamine-dependent phenotypes in a transgenic mouse model of spinal and bulbar muscular atrophy. Nat Med 2003; 9: 768-73.
13. Kegel KB, Kim M, Sapp E, McIntyre C, Castano JG, Aronin N, et al. Huntingtin expression stimulates endosomal-lysosomal activity, endosome tubulation and autophagy. J Neurosci 2000; 20: 7268-78.
14. Kennedy WR, Alter M, Sung JH. Progressive proximal spinal and bulbar muscular atrophy of late onset. A sex-linked recessive trait. Neurology 1968; 18: 671-80.
15. La Spada AR, Wilson EM, Lubahn DB, Harding AE, Fischbeck KH. Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature 1991; 352: 77-9.
16. La Spada AR, Roling DB, Harding AE, Warner CL, Spiegel R, Hausmanowa-Petrusewicz I, et al. Meiotic stability and genotype-phenotype correlation of the trinucleotide repeat in X-linked spinal and bulbar muscular atrophy. Nat Genet 1992; 2: 301-4.
17. Li M, Sobue G, Doyu M, Mukai E, Hashizume Y, Mitsuma T. Primary sensory neurons in X-linked recessive bulbospinal neuropathy: histopathology and androgen receptor gene expression. Muscle Nerve 1995; 18: 301-8.
18. Li M, Miwa S, Kobayashi Y, Merry DE, Yamamoto M, Tanaka F, et al. Nuclear inclusions of the androgen receptor protein in spinal and bulbar muscular atrophy. Ann Neurol 1998a; 44: 249-54.
19. Li M, Nakagomi Y, Kobayashi Y, Merry DE, Tanaka F, Doyu M, et al. Nonneural nuclear inclusions of androgen receptor protein in spinal and bulbar muscular atrophy. Am J Pathol 1998b; 153: 695-701.
20. Lieberman AP, Harmison G, Strand AD, Olson JM, Fischbeck KH. Altered transcriptional regulation in cells expressing the expanded polyglutamine androgen receptor. Hum Mol Genet 2002; 11: 1967-76.
21. Lin CH, Tallaksen-Greene S, Chien WM, Cearley JA, Jackson WS, Crouse AB, et al. Neurological abnormalities in a knock-in mouse model of Huntington's disease. Hum Mol Genet 2001; 10: 137-44.
22. Mariotti C, Castellotti B, Pareyson D, Testa D, Eoli M, Antozzi C, et al. Phenotypic manifestations associated with CAG-repeat expansion in the androgen receptor gene in male patients and heterozygous females: a clinical and molecular study of 30 families. Neuromuscul Disord 2000; 10: 391-7.
23. McCampbell A, Taylor JP, Taye AA, Robitschek J, Li M, Walcott J, et al. CREB-binding protein sequestration by expanded polyglutamine. Hum Mol Genet 2000; 9: 2197-202.
24. McCampbell A, Taye AA, Whitty L, Penney E, Steffan JS, Fischbeck KH. Histone deacetylase inhibitors reduce polyglutamine toxicity. Proc Natl Acad Sci USA 2001; 98: 15179-84.
25. Michalik A, Van Broeckhoven C. Pathogenesis of polyglutamine disorders: aggregation revisited. Hum Mol Genet 2003; 12: R173-86.
26. Minamiyama M, Katsuno M, Adachi H, Waza M, Sang C, Kobayashi Y, et al. Sodium butyrate ameliorates phenotypic expression in a transgenic mouse model of spinal and bulbar muscular atrophy. Hum Mol Genet 2004; 13: 1183-92.
27. Pinto AD, Lang AE, Chen R. The cerebellothalamocortical pathway in essential tremor. Neurology 2003; 60: 1985-7.
28. Ravikumar B, Duden R, Rubinsztein DC. Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum Mol Genet 2002; 11: 1107-17.
29. Ross CA. Polyglutamine pathogenesis: emergence of unifying mechanisms for Huntington's disease and related disorders. Neuron 2002; 35: 819-22.
30. Ross CA, Poirier MA, Wanker EE, Amzel M. Polyglutamine fibrillogenesis: the pathway unfolds. Proc Natl Acad Sci USA 2003; 100: 1-3.
31. Sapp E, Schwarz C, Chase K, Bhide PG, Young AB, Penney J, et al. Huntingtin localization in brains of normal and Huntington's disease patients. Ann Neurol 1997; 42: 604-12.
32. Schilling G, Wood JD, Duan K, Slunt HH, Gonzales V, Yamada M, et al. Nuclear accumulation of truncated atrophin-1 fragments in a transgenic mouse model of DRPLA. Neuron 1999; 24: 275-86.
33. Schmidt BJ, Greenberg CR, Allingham-Hawkins DJ, Spriggs EL. Expression of X-linked bulbospinal muscular atrophy (Kennedy disease) in two homozygous women. Neurology 2002; 59: 770-2.
34. Simeoni S, Mancini MA, Stenoien DL, Marcelli M, Weigel NL, Zanisi M, et al. Motoneuronal cell death is not correlated with aggregate formation of androgen receptors containing an elongated polyglutamine tract. Hum Mol Genet 2000; 9: 133-44.
35. Sobue G, Hashizume Y, Mukai E, Hirayama M, Mitsuma T, Takahashi A. X-linked recessive bulbospinal neuronopathy. A clinicopathological study. Brain 1989; 12: 209-32.
36. Sobue G, Doyu M, Kachi T, Yasuda T, Mukai E, Kumagai T, et al. Subclinical phenotypic expressions in heterozygous females of X-linked recessive bulbospinal neuronopathy. J Neurol Sci 1993; 117: 74-8.
37. Sperfeld AD, Karitzky J, Brummer D, Schreiber H, Haussler J, Ludolph AC, et al. X-linked bulbospinal neuronopathy: Kennedy disease. Arch Neurol 2002; 59: 1921-6.
38. Steffan JS, Bodai L, Pallos J, Poelman M, McCampbell A, Apostol BL, et al. Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature 2001; 413: 739-43.
39. Tanaka F, Doyu M, Ito Y, Matsumoto M, Mitsuma T, Abe K, et al. Founder effect in spinal and bulbar muscular atrophy (SBMA). Hum Mol Genet 1996; 5: 1253-7.
40. Tanaka F, Reeves MF, Ito Y, Matsumoto M, Li M, Miwa S, et al. Tissue-specific somatic mosaicism in spinal and bulbar muscular atrophy (SBMA) is dependent on CAG repeat length and androgen receptor gene expression level. Am J Hum Genet 1999; 65: 966-73.
41. Tanaka M, Morishima I, Akagi T, Hashikawa T, Nukina N. Intra- and intermolecular beta-plated sheet formation in glutamine-repeat inserted myoglobin as a model for polyglutamine diseases. J Biol Chem 2001; 276: 45470-5.
42. Tanaka M, Machida Y, Nishikawa Y, Akagi T, Hashikawa T, Fujisawa T, et al. Expansion of polyglutamine induces the formation of quasi-aggregate in the early stage of protein fibrillization. J Biol Chem 2003; 278: 34717-24.
43. Taylor JP, Tanaka F, Robitschek J, Sandoval CM, Taye A, Markovic-Plese S, et al. Aggresomes protect cells by enhancing the degradation of toxic polyglutamine-containing protein. Hum Mol Genet 2003; 12: 749-57.
44. Terao S, Sobue G, Hashizume Y, Li M, Inagaki T, Mitsuma T. Age-related changes in human spinal ventral horn cells with special reference to the loss of small neurons in the intermediate zone: a quantitative analysis. Acta Neuropathol (Berl) 1996; 92: 109-14.
45. Trottier Y, Lutz Y, Stevanin G, Imbert G, Devys D, Cancel G, et al. Polyglutamine expansion as a pathological epitope in Huntingtin's disease and four dominant cerebellar ataxias. Nature 1995; 378: 403-6.
46. Walcott JL, Merry DE. Ligand promotes intranuclear inclusions in a novel cell model of spinal and bulbar muscular atrophy. J Biol Chem 2002a; 277: 50855-9.
47. Walcott JL, Merry DE. Trinucleotide repeat disease. The androgen receptor in spinal and bulbar muscular atrophy. Vitam Horm 2002b; 65: 127-47.
48. Watase K, Weeber EJ, Xu B, Antalffy B, Yuva-Paylor L, Hashimoto K, et al. A long CAG repeat in the mouse Sca1 locus replicates SCA1 features and reveals the impact of protein solubility on selective neurodegeneration. Neuron 2002; 34: 905-19.
49. Yamada M, Wood JD, Shimohata T, Hayashi S, Tsuji S, Ross CA, et al. Widespread occurrence of intranuclear atrophin-1 accumulation in the central nervous system neurons of patients with dentatorubral-pallidoluysian atrophy. Ann Neurol 2001a; 49: 14-23.
50. Yamada M, Hayashi S, Tsuji S, Takahashi H. Involvement of the cerebral cortex and autonomic ganglia in Machado-Joseph disease. Acta Neuropathol (Berl) 2001b; 101: 140-4.
51. Yamada M, Sato T, Tsuji S, Takahashi H. Oligodendrocytic polyglutamine pathology in dentatorubral-pallidoluysian atrophy. Ann Neurol 2002a; 52: 670-4.
52. Yamada M, Tsuji S, Takahashi H. Involvement of lysosomes in the pathogenesis of CAG repeat diseases. Ann Neurol 2002b; 52: 498-503.
53. Yoo SY, Pennesi ME, Weeber EJ, Xu B, Atkinson R, Chen S, et al. SCA7 knock in mice model human SCA7 and reveal gradual accumulation of mutant ataxin-7 in neurons and abnormalities in short-term plasticity. Neuron 2003; 37: 383-401.
54. Yvert G, Lindenberg KS, Picaud S, Landwehrmeyer GB, Sahel JA, Mandel JL. Expanded polyglutamines induce neurodegeneration and trans-neuronal alterations in cerebellum and retina of SCA7 transgenic mice. Hum Mol Genet 2000; 9: 2491-506.