Basal and stress-induced Hsp70 are modulated by ataxin-3

Cell Stress and Chaperones

Volumn 17, Issue 6, 2012, Pages 729-742

  Reina, Christopher P ^a,b   Nabet, Barzin Y ^a   Young, Peter D ^a   Pittman, Randall N ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Homeostasis; Hsf1; Hsp70 regulation; Proteostasis; SCA3 MJD; Stress

Indexed keywords

ATAXIN 3; AZETIDINE 2 CARBOXYLIC ACID; CADMIUM; CELL ENZYME; CHAPERONE; CHAPERONIN 60; DEUBIQUITINASE; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN 110; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HEAT SHOCK TRANSCRIPTION FACTOR 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; CELL LEVEL; CELL STRESS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INACTIVATION; FIBROBLAST; GENE ACTIVITY; GENE MUTATION; GENETIC TRANSFECTION; HEAT SHOCK RESPONSE; HOMEOSTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REPORTER GENE; WESTERN BLOTTING;

ANIMALS; AZETIDINECARBOXYLIC ACID; BRAIN; CADMIUM; CELLS, CULTURED; FIBROBLASTS; GENE EXPRESSION; HSP70 HEAT-SHOCK PROTEINS; MICE; MICE, KNOCKOUT; MOLECULAR CHAPERONES; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; TEMPERATURE; TRANSCRIPTION FACTORS;

MUS;

EID: 84868140148     PISSN: 13558145     EISSN: 14661268     Source Type: Journal    
DOI: 10.1007/s12192-012-0346-2     Document Type: Article

References (82)

1. Abravaya K, Myers MP, Murphy SP, Morimoto RI (1992) The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev 6:1153-1164
2. Anckar J, Sistonen L (2011) Regulation of Hsf1 function in the heat stress response: implications in aging and disease. Annu Rev Biochem 80:1089-1115
3. Araujo J, Breuer P, Dieringer S, Krauss S, Dorn S, Klockgether T, Wuellner U, Evert BO (2011) FOXO4-depenent upregulation of superoxide dismutase-2 in response to oxidative stress is impaired in spinocerebellar ataxia type 3. Hum Mol Genet 20:2928-2941
4. Beere HM, Green DR (2001) Stress management - heat shock protein-70 and the regulation of apoptosis. Trends Cell Biol 11:6-10 (Pubitemid 32056181)
5. Bevilacqua A, Fiorenza MT, Mangia F (1997) Developmental activation of an episomic hsp70 gene promoter in two-cell mouse embryos by transcription factor Sp1. Nucleic Acids Res 25:1333-1338 (Pubitemid 27303659)
6. Bevilacqua A, Fiorenza MT, Mangia F (2000) A developmentally regulated GAGA box-binding factor and Sp1 are required for transcription of the hsp70.1 gene at the onset of mouse zygotic genome activation. Dev 127:1541-1551 (Pubitemid 30232604)
7. Bucciantini M, Giannoni E, Chiti F, Baroni F, Dobson CM, Stefani M (2002) Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nat 416:507-511 (Pubitemid 34288846)
8. Bukau B, Weissman J, Horwich A (2006) Molecular chaperones and protein quality control. Cell 125:443-451
9. Burnett BG, Pittman RN (2005) The polyglutamine neurodegenerative protein ataxin3 regulates aggresome formation. PNAS 102:4330-4335 (Pubitemid 40397111)
10. Burnett B, Li F, Pittman RN (2003) The polyglutamine neurodegenerative protein ataxin-3 binds polyubiquitylated proteins and has ubiquitin protease activity. Hum Mol Genet 12:3195-3205 (Pubitemid 37508890)
11. Calderwood SK, Murshid A, Prince T (2009) The shock of aging: molecular chaperones and the heat shock response in longevity and aging. Gerontol 55:550-558
12. Carrell RW, Lomas DA (1997) Conformation disease. Lancet 350:134-138
13. Christians E, Michel E, Adenot P, Mezger V, Rallu M, Morange M, Renard J-P (1997) Evidence for the involvement of mouse heat shock factor 1 in the atypical expression of the HSP70.1 heat shock gene during mouse zygotic genome activation. Mol Cell Biol 17:778-788 (Pubitemid 27044377)
14. Cowley BD, Muessel MJ, Douglass D, Wilkins W (1995) In vivo and in vitro osmotic regulation of HSP-70 and prostaglandin synthase gene expression in kidney cells. Am J Physiol 269: F854-F862
15. D'Souza SM, Brown IR (1998) Constitutive expression of heat shock proteins hsp90, hsc70, hsp70 and hsp60 in neural and non-neural tissues of the rat during postnatal development. Cell Stress Chaperones 3:188-199 (Pubitemid 28434683)
16. Doss-Pepe EW, Stenroos ES, Johnson WG, Madura K (2003) Ataxin-3 interactions with Rad23 and valosin-containing protein and its associations with ubiquitin chains and the proteasome are consistent with a role in ubiquitin-mediated proteolysis. Mol Cell Biol 23:6469-6483 (Pubitemid 37075759)
17. Durcan TM, Kontogiannea M, Thorarinsdottir T, Fallon L, Paulson HL, Fon EU (2010) The Machado-Joseph disease-associated mutant form of ataxin-3 regulates parkin ubiquitination and stability. Hum Mol Genet 20:141-154
18. Evert BO, Araujo J, Vieira-Saecker AM, deVos RA, Harendza S, Klockgether T, Wullner U (2006) Ataxin-3 represses transcription via chromatin binding, interaction with histone deacetylase 3, and histone deacetylation. J Neurosci 26:11474-11486 (Pubitemid 44772178)
19. Feder JH, Rossi JM, Solomon J, Solomon N, Lindquist S (1992) The consequences of expressing hsp70 in Drosophila cells at normal temperatures. Genes Dev 6:1402-1413
20. Greene JM, Larin Z, Taylor ICA, Prentice H, Gwinn KA, Kingston RE (1987) Multiple basal elements of a human hsp70 promoter function differently in human and rodent cell lines. Mol Cell Biol 7:3646-3655
21. Gupta AA, Morris JK, Zhang H, Bomhoff GL, Geiger PC, Stanford JA (2010) Age-related changes in Hsp25 expression in basal ganglia and cortex of F344/BN rats. Neurosci Lett 472:90-93
22. Harrison EM, Garden OJ, Ross JA, Wigmore SJ (2006) Firefly luciferase terminally degraded by mild heat exposure: implications for reporter assays. J Immunol Methods 310:182-185 (Pubitemid 43375987)
23. Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Sci 295:1852-1858 (Pubitemid 34214115)
24. Hartl FU, Hlodan R, Lander T (1994) Molecular chaperones in protein folding, the art of avoiding sticky situations. Trends Biochem Sci 19:20-25 (Pubitemid 24028727)
25. Hofmann K, Falquet L (2001) A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems. TIBS 26:347-350 (Pubitemid 32530646)
26. Imbriano C, Bolognese F, Gurtner A, Piaggio G, Mantovani R (2001) Hsp-CBF is an NF-Y-dependent coactivator of the heat shock promoters CCAAT boxes. J Biol Chem 276:26332-26339
27. Kawaguchi Y, Okamoto T, Taniwaki M, Aizawa M, Inoue M, Katayama S, Kimura J, Narumiya S, Kakizuka A (1994) CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nat Genet 8:221-228 (Pubitemid 24338732)
28. Krebs RA, Feder ME (1997) Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 2:60-71 (Pubitemid 27170407)
29. Kuhlbrodt K, Janiesch PC, Kevei E, Segref A, Barikbin R, Hoppe T (2011) The Machado-Joseph disease deubiquitylase ATX-3 couples longevity and proteostasis. Nat Cell Biol 13:273-281
30. Lee SS, Kennedy S, Tolonen AC, Ruvkun G (2003) DAF-16 targets genes that control C. elegans life-span and metabolism. Sci 300:644-647 (Pubitemid 36520589)
31. Li W, Herrler M, Landsberger N, Kaludov N, Ogryzko V, Nakatani Y, Wolffe AP (1998) Xenopus NF-Y pre-sets chromatin to potentiate p300 and acetylation-responsive transcription from the Xenopus hsp70 promoter in vivo. EMBO J 17:6300-6315 (Pubitemid 28497802)
32. Li CY, Lee JS, Ko YG, Kim JI, Seo JS (2000) Heat shock protein 70 inhibits apoptosis down stream of cytochrome c release and upstream of caspase-3 activation. J Biol Chem 275:25665-25671
33. Li F, Macfarlan T, Pittman RN, Chakravarti D (2002) Ataxin-3 is a histone-binding protein with two independent transcriptional corepressor activities. J Biol Chem 277:45004-45012 (Pubitemid 36159099)
34. Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631-677 (Pubitemid 19156675)
35. Locke M, Noble EG, Atkinson BG (1991) Inducible isoform of Hsp70 is constitutively expressed in a muscle fiber type specific pattern. Am J Physiol 261:C774-779
36. Manzerra P, Rush SJ, Brown IR (1997) Tissue-specific differences in heat shock protein hsc70 and hsp70 in the control and hyperthermic rabbit. J Cell Physiol 170:130-137 (Pubitemid 27076213)
37. Matos DA, de Macedo-Ribeiro S, Carvalho AL (2011) Polyglutamine diseases: the special case of ataxin-3 and Machado-Joseph disease. Prog Neurobiol 95:26-48
38. Milarski KL, Morimoto RI (1986) Expression of human hsp70 during the synthetic phase of the cell cyle. PNAS 83:9517-9521 (Pubitemid 17223391)
39. Milarski KL, Welch WJ, Morimoto RI (1989) Cell cycle-dependent association of Hsp70 with specific cellular proteins. J Cell Biol 108:413-423 (Pubitemid 19065843)
40. Morgan WD, Williams GT, Morimoto RI, Greene J, Kingston RE, Tjian R (1987) Two transcriptional activators, CCAAT-boxbinding transcription factor and heat shock transcription factor, interact with a human hsp70 gene promoter. Mol Cell Biol 7:1129-1138 (Pubitemid 17017434)
41. Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12:3788-3796 (Pubitemid 29024840)
42. Morimoto RI (2008) Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev 22:1427-1438 (Pubitemid 351793077)
43. Mosser DD, Duchaine J, Massie B (1993) The DNA-binding activity of the human heat shock transcription factor regulated in vivo by hsp70. Mol Cell Biol 13:5427-5438 (Pubitemid 23260646)
44. Muller E, Neuhofer W, Ohno A, Rucker S, Thurau K, Beck FX (1996) Heat shock proteins hsp25, hsp60, hsp72, hsp73 in isosmotic cortex and hyperosmotic medulla of rat kidney. Pflugers Arch 431:608-617
45. Nollen EAA, Morimoto RI (2002) Chaperoning signaling pathways: molecular chaperones as stress-sensing "heat shock" proteins. J Cell Sci 115:2809-2816
46. Noonan EJ, Place RF, Giardina C, Hightower LE (2007) Hsp70B' regulation and function. Cell Stress Chaperones 12:393-402
47. O'Neill DE, Noble EG (2004) Constitutive expression of inducible Hsp70 is linked to natural shifts in skeletal muscle phenotype. Acta Physiol Scand 181:35-41 (Pubitemid 38580921)
48. Ouyang H, Ali YO, Ravichandran M, Dong A, Arrowsmith CH, Zhai RG (2012) Protein aggregates are recruited to the aggresome by histone deacetylase 6 via unanchored ubiquitin C-termini. J Biol Chem 287:2317-2327
49. Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437-496 (Pubitemid 24011359)
50. Rabindran SK, Wisniewski J, Li L, Li GC, Wu C (1994) Interaction between heat shock factor and hsp70 is insufficient to suppress induction of DNA-binding activity in vivo. Mol Cell Biol 14:6552-6560 (Pubitemid 24299724)
51. Ray S, Lu Y, Kaufmann SH, Clay W, Fields AP, Brasier AR (2004) Genomic mechanisms of p210-BCR-ABL signaling: induction of heat shock protein 70 through the GATA response element confers resistance to paclitaxel-induced apoptosis. J Biol Chem 279:35604-35615 (Pubitemid 39100562)
52. Reina CP, Zhong X, Pittman RN (2010) Proteotoxic stress increases nuclear localization of ataxin-3. Hum Mol Genet 19:235-249
53. Rodrigues AJ, Coppola G, Santos C, Costa MC, Ailion M, Sequeiros J, Geschwind DH, Maciel P (2007) Functional genomics and biochemical characterization of the C. elegans orthologue of the Machado-Joseph disease protein ataxin-3. FASEB J 21:1126-1136 (Pubitemid 46495702)
54. Rodrigues AJ, Neves-Carvalho A, Teixeira-Castro A, Rokka A, Corthals G, Maciel P (2011) Absence of ataxin-3 leads to enhanced stress response in C. elegans. PLoS One 6:e18512
55. Salway KD, Gallagher EJ, Page MM, Stuart JA (2011) Higher levels of heat shock proteins in longer-lived mammals and birds. Mech Ageing Dev 132:287-297
56. Sanchez I, Mahlke C, Yuan J (2003) Pivotal role of oligomerization in expanded polyglutamine neurodegenerative disorders. Nat 421:373-379 (Pubitemid 36157935)
57. Scaglione KM, Zavodszky E, Podi SV, Patury S, Xu P, Gestwicki JE, Paulson HL (2011) Ube2w and ataxin-3 coordinately regulate the ubiquitin ligase CHIP. Mol Cell 43:599-612
58. Scheel H, Tomiuk S, Hofmann K (2003) Elucidation of ataxin-3 and ataxin-7 function by integrative bioinformatics. Hum Mol Genet 12:2845-2852 (Pubitemid 37407121)
59. Schmitt I, Linden M, Khazneh H, Evert BO, Breuer P, Klockgether T, Wuellner T (2007) Inactivation of the mouse Atxn3 (ataxin-3) gene increases protein ubiquitination. BiochemBiophys Res Commun 362:734-739 (Pubitemid 47368155)
60. Schug J, Overton GC (1997) TESS: Transcription Element Search Software on the WWW. http://www.cbil.upenn.edu/tess
61. Sherman MY, Goldberg AL (2001) Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron 29:15-32 (Pubitemid 32108719)
62. Taira T, Sawai M, Ideda M, Iguchi-Ariga SMM, Hirouoshi A (1999) Cell cycle-dependent switch of up and down-regulation of human hsp70 gene expression by interaction between c-myc and CBF/NF-Y. J Biol Chem 274:24270-24279
63. Thevenod F (2009) Cadmium and cellular signaling cascades: to be or not to be? Toxcol Appl Pharmacol 238:221-239
64. Todi SV, Winborn BJ, Scaglione KM, Blount JR, Travis SM, Paulson HL (2009) Ubiquitination directly enhances activity of the deubiquitinating enzyme ataxin-3. EMBO J 28:372-382
65. Tower J (2011) Heat shock proteins and Drosophila aging. Exp Gerontol 46:355-362
66. Vayssier M, Polla BS (1998) Heat shock proteins chaperoning life and death. Cell Stress Chaperones 3:221-227 (Pubitemid 29051821)
67. Voellmy R (1994) Transduction of the stress signal and mechanisms of transcriptional regulation of heat shock/stress protein gene expression in higher eukaryotes. Crit Rev Eukaryot Gene Expr 4:357-401
68. Volloch VZ, Sherman MY (1999) Oncogenic potential of hsp72. Oncog 18:3648-3651 (Pubitemid 29322390)
69. Walsh DM, Klyubin I, Fadeeva JV, Wolfe MS, Rowan MJ, Selko DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nat 416:535-539 (Pubitemid 34288854)
70. Wang G, Sawai S, Kotliarova S, Kanazawa I, Nukina N (2000) Ataxin- 3, the MJD1 gene product, interacts with the two human homologs of yeast DNA repair protein RAD23, HHR23A and HHR23B. Hum Mol Genet 9:1795-1803 (Pubitemid 30608613)
71. Wang Q, Li L, Ye Y (2006) Regulation of retrotranslocation by p97-associated deubiquitinating enzyme ataxin-3. J Cell Biol 174:963-971 (Pubitemid 44455185)
72. Warrick JM, Chan HYE, Gray-Board GL, Chai Y, Pauson HL, Bonini NM (1999) Supression of polyglutamine-mediated neurodeneration in Drosophila by the molecular chaperone hsp70. Nat Genet 23:425-428
73. Warrick JM,Morabito LM, Bilen J, Gordesky-Gold B, Faust LZ, Paulson HL, Bonini NM (2005) Ataxin-3 suppresses polyglutamine neurodegeneration in Drosophila by a ubiquitin-associated mechanism. Mol Cell 18:37-48 (Pubitemid 40444646)
74. Westerheide SD, Anckar J, Stevens SM, Sistonen L, Morimoto RI (2009) Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Sci 323:1063-1066
75. Williams GT, Morimoto RI (1990) Maximal stress-induced transcription from the human Hsp70 promoter requires interactions with the basal promoter elements independent of rational alignment. Mol Cell Biol 10:3125-3136
76. Williams GT, McClanahan K, Morimoto RI (1989) E1a transactivation of the human Hsp70 promoter is mediated through the basal transcriptional complex. Mol Cell Biol 9:2574-2587 (Pubitemid 19148134)
77. Winborn BJ, Travis SM, Todi SV, Scaglione KM, Xu P, Williams AJ, Cohen RE, Peng J, Paulson HL (2008) The deubiquitinating enzyme ataxin-3, a polyglutamine disease protein, edits Lys63 linkages in mixed linkage ubiquitin chains. J Biol Chem 283:26436-26443
78. Wu C (1995) Heat shock transcription factors: structure and regulation. Annu Rev Cell Dev Biol 11:441-469 (Pubitemid 26019611)
79. Wu BJ, Kingston RE, Morimoto RI (1986) Human Hsp70 promoter contains at least two distinct regulatory domains. PNAS USA 83:629-633 (Pubitemid 16035528)
80. Xiao C,Wu T, Ren A, Pan Q, Chen S, Wu F, Li X, Wang R, Hightower LE, Tanguay RM (2003) Basal and inducible levels of Hsp70 in patients with acute heat illness induced during training. Cell Stress Chaperones 8(1):86-92 (Pubitemid 36444094)
81. Xu D, Zalmas P, LaThangue NB (2008) A transcription cofactor required for the heat-shock response. EMBO Rep 9:662-669 (Pubitemid 351927687)
82. Zhong X, Pittman RN (2006) Ataxin-3 binds VCP/p97 and regulates retrotranslocation of ERAD substrates. Hum Mol Genet 15:2409-2420 (Pubitemid 44288695)