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PMID: 19864465 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A novel mouse HSF3 has the potential to activate nonclassical heat-shock genes during heat shock.

Molecular biology of the cell ·Vol. 21 ·No. 1 ·2010-01-01 ·Pages 106-16

Fujimoto M, Hayashida N, Katoh T, Oshima K, Shinkawa T, Prakasam R, Tan K, Inouye S, Takii R, Nakai A

Abstract

The heat-shock response is characterized by the expression of a set of classical heat-shock genes, and is regulated by heat-shock transcription factor 1 (HSF1) in mammals. However, comprehensive analyses of gene expression have revealed very large numbers of inducible genes in cells exposed to heat shock. It is believed that HSF1 is required for the heat-inducible expression of these genes although HSF2 and HSF4 modulate some of the gene expression. Here, we identified a novel mouse HSF3 (mHSF3) translocated into the nucleus during heat shock. However, mHSF3 did not activate classical heat-shock genes such as Hsp70. Remarkably, overexpression of mHSF3 restored the expression of nonclassical heat-shock genes such as PDZK3 and PROM2 in HSF1-null mouse embryonic fibroblasts (MEFs). Although down-regulation of mHSF3 expression had no effect on gene expression or cell survival in wild-type MEF cells, it abolished the moderate expression of PDZK3 mRNA and reduced cell survival in HSF1-null MEF cells during heat shock. We propose that mHSF3 represents a unique HSF that has the potential to activate only nonclassical heat-shock genes to protect cells from detrimental stresses.

MeSH Terms
Animals COS Cells Cell Nucleus/metabolism Chickens Chlorocebus aethiops Cytoprotection DNA/metabolism DNA Helicases/metabolism Gene Expression Regulation Genome/genetics HSP70 Heat-Shock Proteins/genetics,metabolism Heat-Shock Proteins/metabolism Heat-Shock Response/genetics Humans Mice Molecular Sequence Data Multigene Family/genetics Nuclear Proteins/metabolism Protein Binding Protein Transport Stress, Physiological Temperature Transcription Factors/metabolism
Chemicals
HSF3 protein, mouse HSP70 Heat-Shock Proteins Heat-Shock Proteins Nuclear Proteins Transcription Factors DNA Smarca4 protein, mouse DNA Helicases
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Fujimoto Mitsuaki
Department of Biochemistry, Yamaguchi University School of Medicine, Ube, Japan.
Hayashida Naoki
Katoh Takuma
Oshima Kouji
Shinkawa Toyohide
Prakasam Ramachandran
Tan Ke
Inouye Sachiye
Takii Ryosuke
Nakai Akira
References (79)
79 references, click to expand
  1. Heat shock factor 1 regulates lifespan as distinct from disease onset in prion disease.
    Proc Natl Acad Sci U S A. 2008 Sep 9;105(36):13626-31 PMID: 18757733
  2. Gene duplications and the origins of vertebrate development.
    Dev Suppl. 1994;:125-33 PMID: 7579513
  3. Heat shock transcription factor 1 is involved in quality-control mechanisms in male germ cells.
    Biol Reprod. 2004 Jan;70(1):18-24 PMID: 12954729
  4. Genomic analysis of heat-shock factor targets in Drosophila.
    Genome Biol. 2005;6(7):R63 PMID: 15998452
  5. Analysis of HSF4 binding regions reveals its necessity for gene regulation during development and heat shock response in mouse lenses.
    J Biol Chem. 2008 Oct 31;283(44):29961-70 PMID: 18755693
  6. Heat shock factor 2 (HSF2) contributes to inducible expression of hsp genes through interplay with HSF1.
    J Biol Chem. 2007 Mar 9;282(10):7077-86 PMID: 17213196
  7. Transcriptional activation domains of human heat shock factor 1 recruit human SWI/SNF.
    Mol Cell Biol. 2001 Sep;21(17):5826-37 PMID: 11486022
  8. Characterization of prominin-2, a new member of the prominin family of pentaspan membrane glycoproteins.
    J Biol Chem. 2003 Mar 7;278(10):8586-96 PMID: 12514187
  9. Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress.
    Mol Cell Biol. 1993 Mar;13(3):1392-407 PMID: 8441385
  10. Selection of new HSF1 and HSF2 DNA-binding sites reveals difference in trimer cooperativity.
    Mol Cell Biol. 1994 Nov;14(11):7592-603 PMID: 7935474
  11. Cell cycle transition under stress conditions controlled by vertebrate heat shock factors.
    EMBO J. 2001 Jun 1;20(11):2885-95 PMID: 11387221
  12. Consequences of genome duplication.
    Curr Opin Genet Dev. 2007 Dec;17(6):505-12 PMID: 18006297
  13. A nuclear localization signal is essential for stress-induced dimer-to-trimer transition of heat shock transcription factor 3.
    J Biol Chem. 2000 Nov 3;275(44):34665-71 PMID: 10942768
  14. Human heat shock factors 1 and 2 are differentially activated and can synergistically induce hsp70 gene transcription.
    Mol Cell Biol. 1994 Mar;14(3):2087-99 PMID: 8114740
  15. Brain abnormalities, defective meiotic chromosome synapsis and female subfertility in HSF2 null mice.
    EMBO J. 2002 Jun 3;21(11):2591-601 PMID: 12032072
  16. HSF4, a new member of the human heat shock factor family which lacks properties of a transcriptional activator.
    Mol Cell Biol. 1997 Jan;17(1):469-81 PMID: 8972228
  17. Enlarged ventricles, astrogliosis and neurodegeneration in heat shock factor 1 null mouse brain.
    Neuroscience. 2004;126(3):657-63 PMID: 15183515
  18. Active HSF1 significantly suppresses polyglutamine aggregate formation in cellular and mouse models.
    J Biol Chem. 2005 Oct 14;280(41):34908-16 PMID: 16051598
  19. Canonical heat shock element in the alpha B-crystallin gene shows tissue-specific and developmentally controlled interactions with heat shock factor.
    J Biol Chem. 2000 Jun 2;275(22):17154-9 PMID: 10747896
  20. Role of heat-shock factor 2 in cerebral cortex formation and as a regulator of p35 expression.
    Genes Dev. 2006 Apr 1;20(7):836-47 PMID: 16600913
  21. Roles of the heat shock transcription factors in regulation of the heat shock response and beyond.
    FASEB J. 2001 May;15(7):1118-31 PMID: 11344080
  22. HSF4 is required for normal cell growth and differentiation during mouse lens development.
    EMBO J. 2004 Oct 27;23(21):4297-306 PMID: 15483628
  23. Genome-wide analysis of human HSF1 signaling reveals a transcriptional program linked to cellular adaptation and survival.
    Mol Biosyst. 2006 Dec;2(12):627-39 PMID: 17216044
  24. Impaired IgG production in mice deficient for heat shock transcription factor 1.
    J Biol Chem. 2004 Sep 10;279(37):38701-9 PMID: 15226319
  25. Targeted disruption of the heat shock transcription factor (hsf)-2 gene results in increased embryonic lethality, neuronal defects, and reduced spermatogenesis.
    Genesis. 2003 May;36(1):48-61 PMID: 12748967
  26. Removal of Hsf4 leads to cataract development in mice through down-regulation of gamma S-crystallin and Bfsp expression.
    BMC Mol Biol. 2009 Feb 19;10:10 PMID: 19224648
  27. 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. 2003 Aug;23(16):5882-95 PMID: 12897157
  28. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution.
    Nature. 2004 Dec 9;432(7018):695-716 PMID: 15592404
  29. Genome-wide analysis of the biology of stress responses through heat shock transcription factor.
    Mol Cell Biol. 2004 Jun;24(12):5249-56 PMID: 15169889
  30. Human Alu RNA is a modular transacting repressor of mRNA transcription during heat shock.
    Mol Cell. 2008 Feb 29;29(4):499-509 PMID: 18313387
  31. Heat shock transcription factor 1 opens chromatin structure of interleukin-6 promoter to facilitate binding of an activator or a repressor.
    J Biol Chem. 2007 Nov 9;282(45):33210-7 PMID: 17766920
  32. The amphioxus genome and the evolution of the chordate karyotype.
    Nature. 2008 Jun 19;453(7198):1064-71 PMID: 18563158
  33. Molecular characterization of heat shock-like factor encoded on the human Y chromosome, and implications for male infertility.
    Biol Reprod. 2004 Jul;71(1):297-306 PMID: 15044259
  34. Characterization of HSFY, a novel AZFb gene on the Y chromosome with a possible role in human spermatogenesis.
    Mol Hum Reprod. 2004 Apr;10(4):253-8 PMID: 14985478
  35. Disruption of the HSF3 gene results in the severe reduction of heat shock gene expression and loss of thermotolerance.
    EMBO J. 1998 Mar 16;17(6):1750-8 PMID: 9501096
  36. Unique contribution of heat shock transcription factor 4 in ocular lens development and fiber cell differentiation.
    Genesis. 2004 Dec;40(4):205-17 PMID: 15593327
  37. Demyelination, astrogliosis, and accumulation of ubiquitinated proteins, hallmarks of CNS disease in hsf1-deficient mice.
    J Neurosci. 2007 Jul 25;27(30):7974-86 PMID: 17652588
  38. A heat shock-responsive domain of human HSF1 that regulates transcription activation domain function.
    Mol Cell Biol. 1995 Jun;15(6):3354-62 PMID: 7760831
  39. Targeted disruption of hsf1 leads to lack of thermotolerance and defines tissue-specific regulation for stress-inducible Hsp molecular chaperones.
    J Cell Biochem. 2002;86(2):376-93 PMID: 12112007
  40. Genomic organization and promoter analysis of the human heat shock factor 2 gene.
    Cell Stress Chaperones. 2001 Oct;6(4):377-85 PMID: 11795475
  41. Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones.
    Mol Biol Cell. 2004 Feb;15(2):657-64 PMID: 14668486
  42. Upregulation of heat shock transcription factor 1 plays a critical role in adaptive cardiac hypertrophy.
    Circ Res. 2006 Dec 8;99(12):1411-8 PMID: 17095722
  43. Opposing activities protect against age-onset proteotoxicity.
    Science. 2006 Sep 15;313(5793):1604-10 PMID: 16902091
  44. Cutting edge: cross-presentation of cell-associated antigens to MHC class I molecule is regulated by a major transcription factor for heat shock proteins.
    J Immunol. 2004 Nov 15;173(10):5929-33 PMID: 15528326
  45. Structural organization and promoter analysis of murine heat shock transcription factor-1 gene.
    J Biol Chem. 1998 Dec 4;273(49):32514-21 PMID: 9829985
  46. Arrest of spermatogenesis in mice expressing an active heat shock transcription factor 1.
    EMBO J. 2000 Apr 3;19(7):1545-54 PMID: 10747023
  47. Mutant DNA-binding domain of HSF4 is associated with autosomal dominant lamellar and Marner cataract.
    Nat Genet. 2002 Jul;31(3):276-8 PMID: 12089525
  48. Unwinding chromatin for development and growth: a few genes at a time.
    Trends Genet. 2007 Aug;23(8):403-12 PMID: 17566593
  49. Elevated expression of heat shock factor (HSF) 2A stimulates HSF1-induced transcription during stress.
    J Biol Chem. 2003 Sep 12;278(37):35465-75 PMID: 12813038
  50. Essential requirement for both hsf1 and hsf2 transcriptional activity in spermatogenesis and male fertility.
    Genesis. 2004 Feb;38(2):66-80 PMID: 14994269
  51. 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. 2000 Sep 22;275(38):29875-80 PMID: 10896674
  52. Skeletal muscle specification by myogenin and Mef2D via the SWI/SNF ATPase Brg1.
    EMBO J. 2006 Feb 8;25(3):490-501 PMID: 16424906
  53. The mammalian HSF4 gene generates both an activator and a repressor of heat shock genes by alternative splicing.
    J Biol Chem. 1999 Sep 24;274(39):27845-56 PMID: 10488131
  54. Hydrophobic coiled-coil domains regulate the subcellular localization of human heat shock factor 2.
    Genes Dev. 1993 Aug;7(8):1549-58 PMID: 8339932
  55. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators.
    Genes Dev. 1998 Dec 15;12(24):3788-96 PMID: 9869631
  56. A novel HSF1-mediated death pathway that is suppressed by heat shock proteins.
    EMBO J. 2006 Oct 18;25(20):4773-83 PMID: 17024176
  57. Initial sequencing and analysis of the human genome.
    Nature. 2001 Feb 15;409(6822):860-921 PMID: 11237011
  58. Heat shock transcription factors: structure and regulation.
    Annu Rev Cell Dev Biol. 1995;11:441-69 PMID: 8689565
  59. Localized recruitment of a chromatin-remodeling activity by an activator in vivo drives transcriptional elongation.
    Genes Dev. 2003 Jun 1;17(11):1392-401 PMID: 12782657
  60. Multiple layers of regulation of human heat shock transcription factor 1.
    Mol Cell Biol. 1995 Aug;15(8):4319-30 PMID: 7623826
  61. Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging.
    Genes Dev. 2008 Jun 1;22(11):1427-38 PMID: 18519635
  62. New aspects in the vertebrate heat shock factor system: Hsf3 and Hsf4.
    Cell Stress Chaperones. 1999 Jun;4(2):86-93 PMID: 10547058
  63. Characterization of a novel chicken heat shock transcription factor, heat shock factor 3, suggests a new regulatory pathway.
    Mol Cell Biol. 1993 Apr;13(4):1983-97 PMID: 8455593
  64. The role of heat shock transcription factor 1 in the genome-wide regulation of the mammalian heat shock response.
    Mol Biol Cell. 2004 Mar;15(3):1254-61 PMID: 14668476
  65. Targeted disruption of heat shock transcription factor 1 abolishes thermotolerance and protection against heat-inducible apoptosis.
    J Biol Chem. 1998 Mar 27;273(13):7523-8 PMID: 9516453
  66. Regulation of aging and age-related disease by DAF-16 and heat-shock factor.
    Science. 2003 May 16;300(5622):1142-5 PMID: 12750521
  67. Heterotrimerization of heat-shock factors 1 and 2 provides a transcriptional switch in response to distinct stimuli.
    Mol Biol Cell. 2009 Mar;20(5):1340-7 PMID: 19129477
  68. The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins.
    Annu Rev Genet. 1993;27:437-96 PMID: 8122909
  69. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  70. Formation of nuclear stress granules involves HSF2 and coincides with the nucleolar localization of Hsp70.
    J Cell Sci. 2003 Sep 1;116(Pt 17):3557-70 PMID: 12865437
  71. Heat shock transcription factor 1 is required for maintenance of ciliary beating in mice.
    J Biol Chem. 2007 Dec 21;282(51):37285-92 PMID: 17965413
  72. Activation of human heat shock genes is accompanied by oligomerization, modification, and rapid translocation of heat shock transcription factor HSF1.
    Mol Cell Biol. 1993 Apr;13(4):2486-96 PMID: 8455624
  73. Function of the C-terminal transactivation domain of human heat shock factor 2 is modulated by the adjacent negative regulatory segment.
    Nucleic Acids Res. 1998 Jun 1;26(11):2580-5 PMID: 9592140
  74. TreeView: an application to display phylogenetic trees on personal computers.
    Comput Appl Biosci. 1996 Aug;12(4):357-8 PMID: 8902363
  75. The DNA-binding properties of two heat shock factors, HSF1 and HSF3, are induced in the avian erythroblast cell line HD6.
    Mol Cell Biol. 1995 Oct;15(10):5268-78 PMID: 7565675
  76. The carboxyl-terminal transactivation domain of heat shock factor 1 is negatively regulated and stress responsive.
    Mol Cell Biol. 1995 Aug;15(8):4309-18 PMID: 7623825
  77. The impact of comparative genomics on our understanding of evolution.
    Cell. 2000 Jun 9;101(6):573-6 PMID: 10892642
  78. Genetic evidence for a protective role for heat shock factor 1 and heat shock protein 70 against colitis.
    J Biol Chem. 2007 Aug 10;282(32):23240-52 PMID: 17556362
  79. Initial sequencing and comparative analysis of the mouse genome.
    Nature. 2002 Dec 5;420(6915):520-62 PMID: 12466850
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1939-4586
Published
2010-01-01
Epub
2009-00-28
Pages
106-16
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC2801703
Subset
IM
Databases
GENBANK
AB510446, AB510447, AB510448
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