Heat shock factor 1 ameliorates proteotoxicity in cooperation with the transcription factor NFAT

EMBO Journal

Volumn 29, Issue 20, 2010, Pages 3459-3469

  Hayashida, Naoki ^a   Fujimoto, Mitsuaki ^a   Tan, Ke ^a   Prakasam, Ramachandran ^a   Shinkawa, Toyohide ^a   Li, Liangping ^b   Ichikawa, Hitoshi ^c   Takii, Ryosuke ^a   Nakai, Akira ^a  

^a YAMAGUCHI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

Author keywords

heat shock; HSF; NFAT; polyglutamine; protein homeostasis

Indexed keywords

HEAT SHOCK TRANSCRIPTION FACTOR 1; POLYGLUTAMINE; SCAFFOLD PROTEIN; TRANSCRIPTION FACTOR NFAT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; EMBRYO; FEMALE; HOMEOSTASIS; HUMAN; HUMAN CELL; HUNTINGTON CHOREA; MALE; MAMMAL CELL; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALPHA-CRYSTALLIN B CHAIN; ANIMALS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; LIFE EXPECTANCY; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MOLECULAR CHAPERONES; NEOPLASM PROTEINS; NERVE TISSUE PROTEINS; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PEPTIDES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

MAMMALIA; MUS;

EID: 77958449033     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.225     Document Type: Article

References (62)

1. Akerfelt M, Trouillet D, Mezger V, Sistonen L (2007) Heat shock factors at a crossroad between stress and development. Ann NY Acad Sci 1113: 15-27
2. Balch WE, Morimoto RI, Dillin A, Kelly JW (2008) Adapting proteostasis for disease intervention. Science 319: 916-919
3. Bennett EJ, Shaler TA, Woodman B, Ryu KY, Zaitseva TS, Becker CH, Bates GP, Schulman H, Kopito RR (2007) Global changes to the ubiquitin system in Huntington's disease. Nature 448: 704-708
4. Bilen J, Bonini NM (2007) Genome-wide screen for modifiers of ataxin-3 neurodegeneration in Drosophila. PLoS Genet 3: 1950-1964
5. Birch-Machin I, Gao S, Huen D, McGirr R, White RA, Russell S (2005) Genomic analysis of heat-shock factor targets in Drosophila. Genome Biol 6: R63
6. Bukau B, Weissman J, Horwich A (2006) Molecular chaperones and protein quality control. Cell 125: 443-451
7. Carra S, Seguin SJ, Lambert H, Landry J (2008) HspB8 chaperone activity toward poly(Q)-containing proteins depends on its association with Bag3, a stimulator of macro-autophagy. J Biol Chem 283: 1437-1444
8. Cohen E, Bieschke J, Perciavalle RM, Kelly JW, Dillin A (2006) Opposing activities protect against age-onset proteotoxicity. Science 313: 1604-1610
9. Cohen E, Paulsson JF, Blinder P, Burstyn-Cohen T, Du D, Estepa G, Adame A, Pham HM, Holzenberger M, Kelly JW, Masliah E, Dillin A (2009) Reduced IGF-1 signaling delays age-associated proteo-toxicity in mice. Cell 139: 1157-1169
10. Dai C, Whitesell L, Rogers AB, Lindquist S (2007) Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 130: 1005-1018
11. Deguchi M, Iizuka T, Hata Y, Nishimura W, Hirao K, Yao I, Kawabe H, Takai Y (2000) PAPIN. A novel multiple PSD-95/Dlg-A/ZO-1 protein interacting with neural plakophilin-related armadillo repeat protein/delta-catenin and p0071. J Biol Chem 275: 29875-29880
12. Dirks RP, van Geel R, Hensen SM, van Genesen ST, Lubsen NH (2010) Manipulating heat shock factor-1 in Xenopus tadpoles: neuronal tissues are refractory to exogenous expression. PLoS One 5: e10158
13. Egan ME, Glöckner-Pagel J, Ambrose C, Cahill PA, Pappoe L, Balamuth N, Cho E, Canny S, Wagner CA, Geibel J, Caplan MJ (2002) Calcium-pump inhibitors induce functional surface expression of Delta F508-CFTR protein in cystic fibrosis epithelial cells. Nat Med 8: 485-492
14. 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
15. Fujimoto M, Hayashida N, Katoh T, Oshima K, Shinkawa T, Prakasam R, Tan K, Inouye S, Takii R, Nakai A (2010) A novel mouse HSF3 has the potential to activate non-classical heat shock genes during heat shock. Mol Biol Cell 21 : 106-116
16. Fujimoto M, Takaki E, Hayashi T, Kitaura Y, Tanaka Y, Inouye S, Nakai A (2005) Active HSF1 significantly suppresses polygluta-mine aggregate formation in cellular and mouse models. J Biol Chem 280: 34908-34916
17. Hahn JS, Hu Z, Thiele DJ, Iyer VR (2004) Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol Cell Biol 24: 5249-5256
18. Harris BZ, Lim WA (2001) Mechanism and role of PDZ domains in signaling complex assembly. J Cell Sci 114: 3219-3231
19. Hay DG, Sathasivam K, Tobaben S, Stahl B, Marber M, Mestril R, Mahal A, Smith DL, Woodman B, Bates GP (2004) Progressive decrease in chaperone protein levels in a mouse model of Huntington's disease and induction of stress proteins as a therapeutic approach. Hum Mol Genet 13: 1389-1405
20. Hayashida N, Inouye S, Fujimoto M, Tanaka Y, Izu H, Takaki E, Ichikawa H, Rho J, Nakai A (2006) A novel HSF1-mediated death pathway that is suppressed by heat shock proteins. EMBO J 25: 4773-4783
21. Hodge MR, Ranger AM, Charles de la Brousse F, Hoey T, Grusby MJ, Glimcher LH (1996) Hyperproliferation and dysregulation of IL-4 expression in NF-ATp-deficient mice. Immunity 4: 397-405
22. Hogan PG, Chen L, Nardone J, Rao A (2003) Transcriptional regulation by calcium, calcineurin, and NFAT. Gene Dev 17: 2205-2232
23. Homma S, Jin X, Wang G, Tu N, Min J, Yanasak N, Mivechi NF (2007) Demyelination, astrogliosis, and accumulation of ubiqui-tinated proteins, hallmarks of CNS disease in hsf1-deficient mice. J Neurosci 27: 7974-7986
24. Horsley V, Pavlath GK (2002) NFAT: ubiquitous regulator of cell differentiation and adaptation. J Cell Biol 156: 771-774
25. Hsu AL, Murphy CT, Kenyon C (2003) Regulation of aging and age-related disease by daf-16 and heat-shock factor. Science 300: 1142-1145
26. Inouye S, Fujimoto M, Nakamura T, Takaki E, Hayashida N, Hai T, Nakai A (2007) Heat shock transcription factor 1 opens chromatin structure of interleukin-6 promoter to facilitate binding of an activator or a repressor. J Biol Chem 282: 33210-33217
27. Inouye S, Katsuki K, Izu H, Fujimoto M, Sugahara K, Yamada S, Shinkai Y, Oka Y, Katoh Y, Nakai A (2003) Activation of heat shock genes is not necessary for protection by heat shock transcription factor 1 against cell death due to a single exposure to high temperatures. Mol Cell Biol 23: 5882-5895
28. Kazemi-Esfarjani P, Benzer S (2000) Genetic suppression of poly-glutamine toxicity in Drosophila. Science 287: 1837-1840
29. Li LP, Schlag PM, Blankenstein T (1997) Transient expression of SV 40 large T antigen by Cre/LoxP-mediated site-specific deletion in primary human tumor cells. Hum Gene Ther 8: 1695-1700
30. Lin DI, Barbash O, Kumar KG, Weber JD, Harper JW, Klein-Szanto AJ, Rustgi A, Fuchs SY, Diehl JA (2006) Phosphorylation-dependent ubiquitination of cyclin D1 by the SCF(FBX4-alphaB crystallin) complex. Mol Cell 24: 355-366
31. López-Rodríguez C, Aramburu J, Rakeman AS, Rao A (1999) NFAT5, a constitutively nuclear NFAT protein that does not cooperate with Fos and Jun. Proc Natl Acad Sci USA 96: 7214-7219
32. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, Hetherington C, Lawton M, Trottier Y, Lehrach H, Davies SW, Bates GP (1996) Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87: 493-506
33. McMillan DR, Xiao X, Shao L, Graves K, Benjamin IJ (1998) Targeted disruption of heat shock transcription factor 1 abolishes thermotolerance and protection against heat-inducible apoptosis. J Biol Chem 273: 7523-7528
34. Min JN, Huang L, Zimonjic DB, Moskophidis D, Mivechi NF (2007) Selective suppression of lymphomas by functional loss of Hsf1 in a p53-deficient mouse model for spontaneous tumors. Oncogene 26: 5086-5097
35. 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
36. Morimoto RI (2008) Proteotoxic stress and inducible chaperone networks in neuro-degenerative disease and aging. Genes Dev 22: 1427-1438
37. Morley JF, Morimoto RI (2004) Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol Biol Cell 15: 657-664
38. Mosser DD, Morimoto RI (2004) Molecular chaperones and the stress of oncogenesis. Oncogene 23: 2907-2918
39. Mu TW, Fowler DM, Kelly JW (2008) Partial restoration of mutant enzyme homeostasis in three distinct lysosomal storage disease cell lines by altering calcium homeostasis. PLoS Biol 6: e26
40. Muchowski PJ, Wacker JL (2005) Modulation of neurodegeneration by molecular chaperones. Nat Rev Neurosci 6: 11-22
41. Nakai A (2009) Heat shock transcription factors and sensory placode development. BMB Rep 42: 631-635
42. Nakai A, Kawazoe Y, Tanabe M, Nagata K, Morimoto RI (1995) The DNA-binding properties of two heat shock factors, HSF1 and HSF3 are induced in the avian erythroblast cell line HD6. Mol Cell Biol 15: 5168-5178
43. Nakai A, Suzuki M, Tanabe M (2000) Arrest of spermatogenesis in mice expressing an active heat shock transcription factor 1. EMBO J 19: 1545-1554
44. Neef DW, Turski ML, Thiele DJ (2010) Modulation of heat shock transcription factor 1 as a therapeutic target for small molecule intervention in neurodegenerative disease. PLoS Biol 8: e1000291
45. Nollen EA, Garcia SM, van Haaften G, Kim S, Chavez A, Morimoto RI, Plasterk RH (2004) Genome-wide RNA interference screen identifies previously undescribed regulators of polyglutamine aggregation. Proc Natl Acad Sci USA 101 : 6403-6408
46. Ohno H, Hirabayashi S, Iizuka T, Ohnishi H, Fujita T, Hata Y (2002) Localization of p0071-interacting proteins, plakophilin-related armadillo-repeat protein-interacting protein (PAPIN) and ERBIN, in epithelial cells. Oncogene 21: 7042-7049
47. 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
48. Powers ET, Morimoto RI, Dillin A, Kelly JW, Balch WE (2009) Biological and chemical approaches to diseases of proteostasis deficiency. Annu Rev Biochem 78: 959-991
49. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519-529
50. Steele AD, Hutter G, Jackson WS, Heppner FL, Borkowski AW, King OD, Raymond GJ, Aguzzi A, Lindquist S (2008) Heat shock factor 1 regulates lifespan as distinct from disease onset in prion disease. Proc Natl Acad Sci USA 105: 13626-13631
51. Takii R, Inouye S, Fujimoto M, Nakamura T, Shinkawa T, Prakasam R, Tan K, Hayashida N, Ichikawa H, Hai T, Nakai A (2010) Heat shock transcription factor 1 inhibits induction of IL-6 through inducing activation transcription factor 3. J Immunol 184: 1041-1048
52. Tanabe M, Kawazoe Y, Takeda S, Morimoto RI, Nagata K, Nakai A (1998) Disruption of the HSF3 gene results in the severe reduction of heat shock gene expression and loss of thermotolerance. EMBO J 17: 1750-1758
53. Tanaka T, Grusby MJ, Kaisho T (2007) PDLIM2-mediated termination of transcription factor NF-kappaB activation by intranuclear sequestration and degradation of the p65 subunit. Nat Immunol 8: 584-591
54. Trinklein ND, Murray JI, Hartman SJ, Botstein D, Myers RM (2004) The role of heat shock transcription factor 1 in the Genome-wide regulation of the mammalian heat shock response. Mol Biol Cell 15: 1254-1261
55. Vihma H, Pruunsild P, Timmusk T (2008) Alternative splicing and expression of human and mouse NFAT genes. Genomics 92: 279-291
56. Wacker JL, Huang SY, Steele AD, Aron R, Lotz GP, Nguyen Q, Giorgini F, Roberson ED, Lindquist S, Masliah E, Muchowski PJ (2009) Loss of Hsp70 exacerbates pathogenesis but not levels of fibrillar aggregates in a mouse model of Huntington's disease. J Neurosci 29: 9104-9114
57. Westerheide SD, Bosman JD, Mbadugha BN, Kawahara TL, Matsumoto G, Kim S, Gu W, Devlin JP, Silverman RB, Morimoto RI (2004) Celastrols as inducers of the heat shock response and cytoprotection. J Biol Chem 279: 56053-56060
58. Williams AJ, Paulson HL (2008) Polyglutamine neurodegeneration: protein misfolding revisited. Trends Neurosci 31 : 521-528
59. Willingham S, Outeiro TF, DeVit MJ, Lindquist SL, Muchowski PJ (2003) Yeast genes that enhance the toxicity of a mutant huntingtin fragment or alpha-synuclein. Science 302: 1769-1772
60. Wu C (1995) Heat shock transcription factors: structure and regulation. Annu Rev Cell Dev Biol 11 : 441-469
61. Yeung ML, Tam TS, Tsang AC, Yao KM (2003) Proteolytic cleavage of PDZD2 generates a secreted peptide containing two PDZ domains. EMBO Rep 4: 412-418
62. Zourlidou A, Gidalevitz T, Kristiansen M, Landles C, Woodman B, Wells DJ, Latchman DS, de Belleroche J, Tabrizi SJ, Morimoto RI, Bates GP (2007) Hsp27 overexpression in the R6/2 mouse model of Huntington's disease: chronic neurodegeneration does not induce Hsp27 activation. Hum Mol Genet 16: 1078-1090