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PMID: 8943357 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Regulation of Drosophila heat shock factor trimerization: global sequence requirements and independence of nuclear localization.

Molecular and cellular biology ·Vol. 16 ·No. 12 ·1996-12-00 ·Pages 7018-30

Orosz A, Wisniewski J, Wu C

Abstract

Heat shock transcription factor (HSF) is a multidomain protein that exists as a monomer under normal conditions and is reversibly induced upon heat shock to a trimeric state that binds to DNA with high affinity. The maintenance of the monomeric state is dependent on hydrophobic heptad repeats located at the amino- and carboxy-terminal regions which have been proposed to form an intramolecular coiled-coil structure. In a systematic deletion analysis to identify other regions of HSF that may be required to regulate its oligomeric state, we have found that local sequences encompassing the carboxy-terminal end of the DNA binding domain and a broad region of HSF between the heptad repeats also contribute to this regulation. Immunocytochemical analysis of mutant HSF proteins revealed a canonical motif required for nuclear localization. HSF proteins lacking the nuclear localization signal remain in the cytoplasm, but these HSFs nonetheless exhibit reversible heat stress-inducible trimerization. The results indicate that the signals that regulate HSF trimerization operate in both the nuclear and cytoplasmic compartments of the cell.

MeSH Terms
Animals Biological Transport Cell Nucleus/genetics Drosophila/genetics Heat-Shock Proteins/genetics Mutation Signal Transduction/genetics
Chemicals
Heat-Shock Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Orosz A
Laboratory of Molecular Cell Biology, National Cancer Institute, Bethesda, Maryland 20892-4255, USA.
Wisniewski J
Wu C
References (57)
57 references, click to expand
  1. Heat-inducible human factor that binds to a human hsp70 promoter.
    Mol Cell Biol. 1987 Apr;7(4):1530-4 PMID: 3600634
  2. Transcriptional regulation of SSA3, an HSP70 gene from Saccharomyces cerevisiae.
    Mol Cell Biol. 1990 Jun;10(6):3262-7 PMID: 2188113
  3. Heat shock factor is regulated differently in yeast and HeLa cells.
    Nature. 1987 Sep 3-9;329(6134):81-4 PMID: 3306402
  4. Characterization and use of the Drosophila metallothionein promoter in cultured Drosophila melanogaster cells.
    Nucleic Acids Res. 1988 Feb 11;16(3):1043-61 PMID: 3125519
  5. Germline transformation used to define key features of heat-shock response elements.
    Science. 1988 Mar 4;239(4844):1139-42 PMID: 3125608
  6. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation.
    Cell. 1988 Sep 9;54(6):855-64 PMID: 3044613
  7. Activation in vitro of sequence-specific DNA binding by a human regulatory factor.
    Nature. 1988 Sep 22;335(6188):372-5 PMID: 3419505
  8. Constitutive binding of yeast heat shock factor to DNA in vivo.
    Mol Cell Biol. 1988 Nov;8(11):5040-2 PMID: 3062378
  9. Key features of heat shock regulatory elements.
    Mol Cell Biol. 1988 Sep;8(9):3761-9 PMID: 3146692
  10. The heat-shock proteins.
    Annu Rev Genet. 1988;22:631-77 PMID: 2853609
  11. Stable binding of Drosophila heat shock factor to head-to-head and tail-to-tail repeats of a conserved 5 bp recognition unit.
    Cell. 1989 Dec 1;59(5):797-806 PMID: 2590940
  12. Antibody-mediated activation of Drosophila heat shock factor in vitro.
    Science. 1990 Aug 3;249(4968):546-9 PMID: 2200124
  13. The yeast heat shock transcription factor contains a transcriptional activation domain whose activity is repressed under nonshock conditions.
    Cell. 1990 Aug 24;62(4):807-17 PMID: 2201453
  14. Molecular cloning and expression of a hexameric Drosophila heat shock factor subject to negative regulation.
    Cell. 1990 Nov 30;63(5):1085-97 PMID: 2257625
  15. Genomic footprinting of the yeast HSP82 promoter reveals marked distortion of the DNA helix and constitutive occupancy of heat shock and TATA elements.
    J Mol Biol. 1990 Dec 5;216(3):611-31 PMID: 2175361
  16. A conserved heptapeptide restrains the activity of the yeast heat shock transcription factor.
    EMBO J. 1991 Feb;10(2):369-75 PMID: 1899375
  17. Nuclear protein localization.
    Biochim Biophys Acta. 1991 Mar 7;1071(1):83-101 PMID: 2004116
  18. Heat shock factor and the heat shock response.
    Cell. 1991 May 3;65(3):363-6 PMID: 2018972
  19. Molecular cloning and expression of a human heat shock factor, HSF1.
    Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):6906-10 PMID: 1871105
  20. Cloning and characterization of two mouse heat shock factors with distinct inducible and constitutive DNA-binding ability.
    Genes Dev. 1991 Oct;5(10):1902-11 PMID: 1717345
  21. Stress-induced oligomerization and chromosomal relocalization of heat-shock factor.
    Nature. 1991 Oct 31;353(6347):822-7 PMID: 1944557
  22. Temperature-dependent regulation of a heterologous transcriptional activation domain fused to yeast heat shock transcription factor.
    Mol Cell Biol. 1992 Mar;12(3):1021-30 PMID: 1545786
  23. Effect of sodium salicylate on the human heat shock response.
    Science. 1992 Mar 6;255(5049):1243-5 PMID: 1546322
  24. Enzymatic inverse PCR: a restriction site independent, single-fragment method for high-efficiency, site-directed mutagenesis.
    Biotechniques. 1992 Aug;13(2):214-20 PMID: 1327007
  25. Trimerization of the heat shock transcription factor by a triple-stranded alpha-helical coiled-coil.
    Biochemistry. 1992 Dec 8;31(48):12272-6 PMID: 1457424
  26. Regulation of heat shock factor trimer formation: role of a conserved leucine zipper.
    Science. 1993 Jan 8;259(5092):230-4 PMID: 8421783
  27. 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
  28. 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
  29. Activation of Drosophila heat shock factor: conformational change associated with a monomer-to-trimer transition.
    Mol Cell Biol. 1993 Jun;13(6):3481-6 PMID: 8497263
  30. Induction temperature of human heat shock factor is reprogrammed in a Drosophila cell environment.
    Nature. 1993 Jul 15;364(6434):252-5 PMID: 8321322
  31. Protein traffic on the heat shock promoter: parking, stalling, and trucking along.
    Cell. 1993 Jul 16;74(1):1-4 PMID: 8334697
  32. Hydrophobic coiled-coil domains regulate the subcellular localization of human heat shock factor 2.
    Genes Dev. 1993 Aug;7(8):1549-58 PMID: 8339932
  33. Promoter specificity and deletion analysis of three heat stress transcription factors of tomato.
    Mol Gen Genet. 1993 Jul;240(1):113-25 PMID: 8341257
  34. 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
  35. Fine structure analyses of the Drosophila and Saccharomyces heat shock factor--heat shock element interactions.
    Nucleic Acids Res. 1994 Jan 25;22(2):167-73 PMID: 8121800
  36. A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene.
    Cell. 1982 Sep;30(2):517-28 PMID: 6814763
  37. Two protein-binding sites in chromatin implicated in the activation of heat-shock genes.
    Nature. 1984 May 17-23;309(5965):229-34 PMID: 6325944
  38. Activating protein factor binds in vitro to upstream control sequences in heat shock gene chromatin.
    Nature. 1984 Sep 6-11;311(5981):81-4 PMID: 6472466
  39. The heat-shock response.
    Annu Rev Biochem. 1986;55:1151-91 PMID: 2427013
  40. Yeast heat shock transcription factor contains a flexible linker between the DNA-binding and trimerization domains. Implications for DNA binding by trimeric proteins.
    J Biol Chem. 1994 Apr 29;269(17):12475-81 PMID: 8175654
  41. Putative nuclear localization signals (NLS) in protein transcription factors.
    J Cell Biochem. 1994 May;55(1):32-58 PMID: 8083298
  42. Interaction of the DNA-binding domain of Drosophila heat shock factor with its cognate DNA site: a thermodynamic analysis using analytical ultracentrifugation.
    Protein Sci. 1994 Jul;3(7):1040-51 PMID: 7920249
  43. Interaction between heat shock factor and hsp70 is insufficient to suppress induction of DNA-binding activity in vivo.
    Mol Cell Biol. 1994 Oct;14(10):6552-60 PMID: 7935376
  44. Activation of the DNA-binding ability of human heat shock transcription factor 1 may involve the transition from an intramolecular to an intermolecular triple-stranded coiled-coil structure.
    Mol Cell Biol. 1994 Nov;14(11):7557-68 PMID: 7935471
  45. Dynamic protein-DNA architecture of a yeast heat shock promoter.
    Mol Cell Biol. 1995 May;15(5):2737-44 PMID: 7739554
  46. 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
  47. 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
  48. Multiple layers of regulation of human heat shock transcription factor 1.
    Mol Cell Biol. 1995 Aug;15(8):4319-30 PMID: 7623826
  49. Solution structure of the DNA-binding domain of Drosophila heat shock transcription factor.
    Nat Struct Biol. 1994 Sep;1(9):605-14 PMID: 7634100
  50. The C-terminal region of Drosophila heat shock factor (HSF) contains a constitutively functional transactivation domain.
    Nucleic Acids Res. 1996 Jan 15;24(2):367-74 PMID: 8628664
  51. Activation of heat shock factor 1 DNA binding precedes stress-induced serine phosphorylation. Evidence for a multistep pathway of regulation.
    J Biol Chem. 1996 Feb 16;271(7):3355-8 PMID: 8631933
  52. Heat shock transcription factors: structure and regulation.
    Annu Rev Cell Dev Biol. 1995;11:441-69 PMID: 8689565
  53. Trimerization of a yeast transcriptional activator via a coiled-coil motif.
    Cell. 1989 Dec 1;59(5):807-13 PMID: 2686840
  54. Complex modes of heat shock factor activation.
    Mol Cell Biol. 1990 Feb;10(2):752-9 PMID: 2405254
  55. DNA binding of heat shock factor to the heat shock element is insufficient for transcriptional activation in murine erythroleukemia cells.
    Mol Cell Biol. 1990 Apr;10(4):1600-8 PMID: 2320006
  56. In vitro activation of heat shock transcription factor DNA-binding by calcium and biochemical conditions that affect protein conformation.
    Proc Natl Acad Sci U S A. 1990 May;87(10):3748-52 PMID: 2339118
  57. Induction of sequence-specific binding of Drosophila heat shock activator protein without protein synthesis.
    Nature. 1987 Jun 25-Jul 1;327(6124):727-30 PMID: 3600771
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
DOI
10.1128/MCB.16.12.7018
Published
1996-12-00
Pages
7018-30
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC231705
Subset
IM
External Links
PubMed source DOI: 10.1128/MCB.16.12.7018 PMC Full Text View journal details
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