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

Journal of Neuroscience

Volumn 23, Issue 6, 2003, Pages 2203-2211

  Adachi, Hiroaki ^a   Katsuno, Masahisa ^a   Minamiyama, Makoto ^a   Sang, Chen ^a   Pagoulatos, Gerassimos ^b   Angelidis, Charalampos ^b   Kusakabe, Moriaki ^c   Yoshiki, Atsushi ^d   Kobayashi, Yasushi ^a   Doyu, Manabu ^a   Sobue, Gen ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF IOANNINA   (Greece)

^c ALOKA Company Ltd   (Japan)

^d RIKEN   (Japan)

Author keywords

Chaperone; HSP70; Polyglutamine; Protein degradation; SBMA; Transgenic mice

Indexed keywords

ANDROGEN RECEPTOR; CHAPERONE; HEAT SHOCK PROTEIN 70; MUTANT PROTEIN; POLYGLUTAMINE; PROTEASOME; UBIQUITIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; KENNEDY DISEASE; MOTOR NEURON DISEASE; MOUSE; NERVE CELL; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION; TRANSGENIC MOUSE;

EID: 0037444446     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-06-02203.2003     Document Type: Article

References (56)

1. Adachi H, Kume A, Li M, Nakagomi Y, Niwa H, Do J, Sang C, Kobayashi Y, Doyu M, Sobue G (2001) 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 10:1039-1048.
2. Bailey CK, Andriola IF, Kampinga HH, Merry DE (2002) Molecular chaperones enhance the degradation of expanded polyglutamine repeat androgen receptor in a cellular model of spinal and bulbar muscular atrophy. Hum Mol Genet 11:515-523.
3. Bukau KT, Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92:351-366.
4. Burke JR, Enghild JJ, Martin ME, Jou YS, Myers RM, Roses AD, Vance JM, Strittmatter WJ (1996) Huntingtin and DRPLA proteins selectively interact with the enzyme GAPDH. Nat Med 2:347-350.
5. Carmichael J, Chatellier J, Woolfson A, Milstein C, Fersht AR, Rubinsztein DC (2000) Bacterial and yeast chaperones reduce both aggregate formation and cell death in mammalian cell models of Huntington's disease. Proc Natl Acad Sci USA 97:9701-9705.
6. Chai Y, Koppenhafer SL, Bonini NM, Paulson HL (1999) Analysis of the role of heat shock protein (Hsp) molecular chaperones in polyglutamine disease. J Neurosci 19:10338-10347.
7. Chan HYE, Warrick JM, Gray-Board GL, Paulson HL, Bonini NM (2000) Mechanisms of chaperone suppression ofpolyglutamine disease: selectivity, synergy and modulation of protein solubility in Drosophila. Hum Mol Genet 9:2811-2820.
8. Chuang JZ, Zhou H, Zhu M, Li SH, Li XJ, Sung CH (2002) Characterization of a brain-enriched chaperone, MRJ, that inhibits Huntingtin aggregation and toxicity independently. J Biol Chem 277:19831-19838.
9. Connel P, Ballinger CA, Jiang J, Wu Y, Thompson LJ, Höfeld J, Patterson C (2001) The co-chaperone CHIP regulates protein triage decisions mediated by heat shock proteins. Nat Cell Biol 3:93-96.
10. Cummings CJ, Mancini MA, Antalffy B, DeFranco DB, Orr HT, Zoghbi HY (1998) Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCAI. Nat Genet 19:148-154.
11. Cummings CJ, Sun Y, Opal P, Antalffy B, Mestril R, Orr HT, Dillmann WH, Zoghbi HY (2001) Overexpression of inducible HSP70 chaperone suppresses neuropathology and improves motor function in SCA1 mice. Hum Mol Genet 10:1511-1518.
12. Doyu M, Sobue G, Mukai E, Kachi T, Yasuda T, Mitsuma T, Takahashi A (1992) Severity of X-linked recessive bulbospinal neuronopathy correlates with size of the tandem CAG repeat in androgen receptor gene. Ann Neurol 23:707-710.
13. Fernandez-Funez P, Nino-Rosales ML, de Gouyon B, She WC, Luchak JM, Martinez P, Turiegano E, Benito J, Capovilla M, Skinner PJ, McCall A, Canal I, Orr HT, Zoghbi HY, Botas J (2000) Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 408:101-106.
14. Gabai VL, Meriin AB, Yaglorn JA, Volloch VZ, Sherman MY (1998) Role of Hsp70 in regulation of stress-kinase JNK: implications in apoptosis and aging. FEBS Lett 438:1-4.
15. Hendricks JP, Hartl FU (1993) Molecular chaperone functions of heatshock proteins. Annu Rev Biochem 62:349-384.
16. Huynh DP, Figueroa K, Hoang N, Pulst SM (2000) Nuclear localization or inclusion body formation of ataxin-2 are not necessary for SCA2 pathogenesis in mouse or human. Nat Genet 26:44-50.
17. Igarashi S, Tanno Y, Onodera O, Yamazaki M, Sato S, Ishikawa A, Miyatani N, Nagashima M, Ishikawa Y, Sahashi K, Ibi T, Miyatake T, Tsuji S (1992) 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 42:2300-2302.
18. Jana NR, Tanaka M, Wang GH, Nukina N (2000) Polyglutamine length-dependent interaction of Hsp40 and Hsp70 family chaperones with truncated N-terminal huntingtin: their role in suppression of aggregation and cellular toxicity. Hum Mol Genet 9:2009-2018.
19. Jana NR, Zemskov EA, Wang GH, Nukina N (2001) Altered proteasomal function due to the expression of polyglutamine-expanded truncated N-terminal huntingtin induces apoptosis by caspase activation through mitochondrial cytochrome c release. Hum Mol Genet 10:1049-1059.
20. Kalchman MA, Koide HB, McCutcheon K, Graham RK, Nichol K, Nishiyama K, Kazemi-Esfarjani P, Lynn FC, Wellington C, Metzler M, Goldberg YP, Kanazawa I, Gietz RD, Hayden MR (1997) HIP1, a human homologue of S. cerevisiae Sla2p, interacts with membrane-associated huntingtin in the brain. Nat Genet 16:44-53.
21. Katsuno M, Adachi H, Kume A, Li M, Nakagomi Y, Niwa H, Sang C, Kobayashi Y, Doyu M, Sobue G (2002) Testosterone reduction prevents phenotypic expression in a transgenic mouse model of spinal and bulbar muscular atrophy. Neuron 35:843-854.
22. Kennedy WR, Alter M, Sung JH (1968) Progressive proximal spinal and bulbar muscular atrophy of late onset: a sex-linked recessive trait. Neurology 18:671-680.
23. Kobayashi Y, Sobue G (2001) Protective effect of chaperones on polyglutamine diseases. Brain Res Bull 56:165-168.
24. Kobayashi Y, Kume A, Li M, Doyu M, Hata M, Ohtsuka K, Sobue G (2000) Chaperones Hsp70 and Hsp40 suppress aggregate formation and apoptosis in cultured neuronal cells expressing truncated androgen receptor protein with expanded polyglutamine tract. J Biol Chem 275:8772-8778.
25. La Spada AR, Roling DB, Harding AE, Warner CL, Spiegel R, Hausmanowa-Petrusewicz I, Yee WC, Fischbeck KH (1992) Meiotic stability and genotype-phenotype correlation of the trinucleotide repeat in X-linked spinal and bulbar muscular atrophy. Nat Genet 2:301-304.
26. Li CY, Lee JS, Ko YG, Kim JI, Seo JS (2000) Heat shock protein 70 inhibits apoptosis downstream of cytochrome c release and upstream of caspase-3 activation. J Biol Chem 275:25665-25671.
27. Li M, Miwa S, Kobayashi Y, Merry DE, Tanaka F, Doyu M, Hashizume Y, Fischbeck KH, Sobue G (1998a) Nuclear inclusions of the androgen receptor protein in spinal and bulbar muscular atrophy. Ann Neurol 44:249-254.
28. Li M, Nakagomi Y, Kobayashi Y, Merry, DE, Tanaka F, Doyu M, Mitsuma T, Fischbeck KH, Sobue G (1998b) Nonneural nuclear inclusions of androgen receptor protein in spinal and bulbar muscular atrophy. Am J Pathol 153:695-701.
29. Li XJ, Li SH, Sharp AH, Nucifora Jr FC, Schilling G, Lanahan A, Worley P, Snyder SH, Ross CA (1995) A huntingtin-associated protein enriched in brain with implications for pathology. Nature 378:398-402.
30. Lüders J, Demand J, Höhfeld J (2000) The ubiquitin-related BAG-1 provides a link between the molecular chaperones Hsc70/Hsp70 and the proteasome. J Biol Chem 275:4613-4617.
31. Matilla A, Koshy BT, Cummings CJ, Isobe T, Orr HT, Zoghbi HY (1997) The cerebellar leucine-rich acidic nuclear protein interacts with ataxin-1. Nature 389:974-978.
32. McCampbell A, Taylor JP, Taye AA, Robitschek J, Li M, Walcott J, Merry D, Chai Y, Paulson H, Sobue G, Fischbeck KH (2000) CREB-binding protein sequestration by expanded polyglutamine. Hum Mol Genet 9:2197-2202.
33. Muchowski PJ, Schaffar G, Sittler A, Wanker EE, Hayer-Hartl MK, Hartl FU (2000) Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc Natl Acad Sci USA 97:7841-7846.
34. Murata S, Minami Y, Minami M, Chiba T, Tanaka K (2001) CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep 2:1133-1138.
35. Nucifora Jr FC, Sasaki M, Peters MF, Huang H, Cooper JK, Yamada M, Takahashi H, Tsuji S, Troncoso J, Dawson VL, Dawson TM, Ross CA (2001) Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science 291:2423-2428.
36. Opal P, Zoghbi HY (2002) The role of chaperones in polyglutamine disease. Trends Mol Med 8:232-236.
37. Plumier JC, Ross BM, Currie RW, Angelidis CE, Kaziaris H, Kollias G, Pagoulatos GN (1995) Transgenic mice expressing the human heat shock protein 70 have improved post-ischemic myocardial recovery. J Clin Invest 95:1854-1860.
38. Ross CA (2002) Polyglutamine pathogenesis: emergence of unifying mechanisms for Huntington's disease and related disorders. Neuron 35:819-822.
39. Schmidt T, Lindenberg KS, Krebs A, Schols L, Laccone F, Herms J, Rechsteiner M, Riess O, Landwehrmeyer GB (2002) Protein surveillance machinery in brains with spinocerebellar ataxia type 3: redistribution and differential recruitment of 26S proteasome subunits and chaperones to neuronal intranuclear inclusions. Ann Neurol 51:302-310.
40. Sherman MY, Goldberg AL (2001) Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron 29:15-32.
41. Shimohata T, Nakajima T, Yamada M, Uchida C, Onodera O, Naruse S, Kimura T, Koide R, Nozaki K, Sano Y, Ishiguro H, Sakoe K, Ooshima T, Sato A, Ikeuchi T, Oyake M, Sato T, Aoyagi Y, Hozumi I, Nagatsu T, et al. (2000) Expanded polyglutamine stretches interact with TAFII130, interfering with CREB-dependent transcription. Nat Genet 26:29-36.
42. Sittler A, Lurz R, Lueder G, Priller J, Hayer-Hartl MK, Hartl FU, Lehrach H, Wanker EE (2001) Geldanamycin activates a heat shock response and inhibits huntingtin aggregation in a cell culture model of Huntington's disease. Hum Mol Genet 10:1307-1315.
43. Sobue G, Hashizume Y, Mukai E, Hirayama M, Mitsuma T, Takahashi A (1989) X-linked recessive bulbospinal neuronopathy: a clinicopathological study. Brain 112:209-232.
44. Stenoien DL, Cummings CJ, Adams HP, Mancini MG, Patel K, DeMartino GN, Marcelli M, Weigel NL, Mancini MA (1999) Polyglutamine-expanded androgen receptors form aggregates that sequester heat shock proteins, proteasome components and SRC-1, and are suppressed by the HDJ-2 chaperone. Hum Mol Genet 8:731-741.
45. Takahashi A (2001) Hiroshi Kawahara (1858-1918). J Neurol 248:241-242.
46. Tanaka F, Doyu M, Ito Y, Matsumoto M, Mitsuma T, Abe K, Aoki M, Itoyama Y, Fischbeck KH, Sobue G (1996) Founder effect in spinal and bulbar muscular atrophy (SBMA). Hum Mol Genet 5:1253-1257.
47. Tanaka F, Reeves MF, Ito Y, Matsumoto M, Li M, Miwa S, Inukai A, Yamamoto M, Doyu M, Yoshida M, Hashizume Y, Terao S, Mitsuma T, Sobue G (1999) 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 65:966-973.
48. Terao S, Sobue G, Hashizume Y, Li M, Inagaki T, Mitsuma T (1996) 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) 92:109-114.
49. Waelter S, Boeddrich A, Lurz R, Scherzinger E, Lueder G, Lehrach H, Wanker EE (2001) Accumulation of mutant huntingtin fragments in aggresome-like inclusion bodies as a result of insufficient protein degradation. Mol Biol Cell 12:1393-1407.
50. Wanker EE, Scherzinger E, Heiser V, Sittler A, Eickhoff H, Lehrach H (1999) Membrane filter assay for detection of amyloid-like polyglutamine-containing protein aggregates. Methods Enzymol 309:375-386.
51. Waragai M, Lammers C, Takeuchi S, Imafuku I, Udagawa Y, Kanazawa I, Kawabata M, Mouradian MM, Okazawa H (1999) PQBP-1, a novel polyglutamine tract-binding protein,inhibits transcription activation by Brn-2 and affects cell survival. Hum Mol Genet 8:977-987.
52. Warrick JM, Chan HY, Gray-Board GL, Chai Y, Paulson HL, Bonini NM (1999) Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat Genet 23:425-428.
53. Yamada M, Wood JD, Shimohata T, Hayashi S, Tsuji S, Ross CA, Takahashi H (2001) Widespread occurrence ofintranuclear atrophin-1 accumulation in the central nervous system neurons of patients with dentatorubral-pallidoluysian atrophy. Ann Neurol 49:14-23.
54. Zander C, Takahashi J, Hachimi KHE, Fujigasaki H, Albanese V, Lebre AS, Stevanin G, Duyckaerts C, Brice A (2001) Similarities between spinocerebellar ataxia type 7 (SCA7) cell models and human brain: proteins recruited in inclusions and activation of caspase-3. Hum Mol Genet 10:2569-2579.
55. Zhou H, Li SH, Li XJ (2001) Chaperone suppression of cellular toxicity of huntingtin is independent of polyglutamine aggregation. J Biol Chem 276:48417-48424.
56. Zoghbi HY, Orr HT (2000) Glutamine repeats and neurodegeneration. Annu Rev Neurosci 23:217-247.