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PMID: 9774677 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Glycogen synthase kinase 3beta and extracellular signal-regulated kinase inactivate heat shock transcription factor 1 by facilitating the disappearance of transcriptionally active granules after heat shock.

Molecular and cellular biology ·Vol. 18 ·No. 11 ·1998-11-00 ·Pages 6624-33

He B, Meng YH, Mivechi NF

Abstract

Heat shock transcription factor 1 (HSF-1) activates the transcription of heat shock genes in eukaryotes. Under normal physiological growth conditions, HSF-1 is a monomer. Its transcriptional activity is repressed by constitutive phosphorylation. Upon activation, HSF-1 forms trimers, acquires DNA binding activity, increases transcriptional activity, and appears as punctate granules in the nucleus. In this study, using bromouridine incorporation and confocal laser microscopy, we demonstrated that newly synthesized pre-mRNAs colocalize to the HSF-1 punctate granules after heat shock, suggesting that these granules are sites of transcription. We further present evidence that glycogen synthase kinase 3beta (GSK-3beta) and extracellular signal-regulated kinase mitogen-activated protein kinase (ERK MAPK) participate in the down regulation of HSF-1 transcriptional activity. Transient increases in the expression of GSK-3beta facilitate the disappearance of HSF-1 punctate granules and reduce hsp-70 transcription after heat shock. We have also shown that ERK is the priming kinase for GSK-3beta. Taken together, these results indicate that GSK-3beta and ERK MAPK facilitate the inactivation of activated HSF-1 after heat shock by dispersing HSF-1 from the sites of transcription.

MeSH Terms
Calcium-Calmodulin-Dependent Protein Kinases/physiology DNA-Binding Proteins/metabolism Down-Regulation/physiology Fluorescent Antibody Technique Glycogen Synthase Kinase 3 Glycogen Synthase Kinases HSP70 Heat-Shock Proteins/metabolism HeLa Cells Heat Shock Transcription Factors Humans Microscopy, Fluorescence Nuclear Proteins/metabolism Phosphorylation Protein Conformation RNA Precursors/metabolism RNA, Messenger/metabolism Signal Transduction/physiology Temperature Transcription Factors Transcription, Genetic/genetics Transfection/genetics
Chemicals
DNA-Binding Proteins HSF1 protein, human HSP70 Heat-Shock Proteins Heat Shock Transcription Factors Nuclear Proteins RNA Precursors RNA, Messenger Transcription Factors Glycogen Synthase Kinases Calcium-Calmodulin-Dependent Protein Kinases Glycogen Synthase Kinase 3
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
He B
Institute of Molecular Medicine and Genetics, Department of Radiology, Medical College of Georgia, Augusta, Georgia 30912, USA.
Meng Y H
Mivechi N F
References (71)
71 references, click to expand
  1. Sounding the alarm: protein kinase cascades activated by stress and inflammation.
    J Biol Chem. 1996 Oct 4;271(40):24313-6 PMID: 8798679
  2. Selective response of ternary complex factor Sap1a to different mitogen-activated protein kinase subgroups.
    Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11563-8 PMID: 8876175
  3. Stable overexpression of human HSF-1 in murine cells suggests activation rather than expression of HSF-1 to be the key regulatory step in the heat shock gene expression.
    J Cell Biochem. 1995 Oct;59(2):266-80 PMID: 8904320
  4. Isolation of the active form of RAC-protein kinase (PKB/Akt) from transfected COS-7 cells treated with heat shock stress and effects of phosphatidylinositol 3,4,5-trisphosphate and phosphatidylinositol 4,5-bisphosphate on its enzyme activity.
    FEBS Lett. 1996 Nov 4;396(2-3):305-8 PMID: 8915008
  5. Sequential phosphorylation by mitogen-activated protein kinase and glycogen synthase kinase 3 represses transcriptional activation by heat shock factor-1.
    J Biol Chem. 1996 Nov 29;271(48):30847-57 PMID: 8940068
  6. Repression of human heat shock factor 1 activity at control temperature by phosphorylation.
    Genes Dev. 1996 Nov 1;10(21):2782-93 PMID: 8946918
  7. The p38 and ERK MAP kinase pathways cooperate to activate Ternary Complex Factors and c-fos transcription in response to UV light.
    EMBO J. 1996 Dec 2;15(23):6552-63 PMID: 8978682
  8. The mechanism by which epidermal growth factor inhibits glycogen synthase kinase 3 in A431 cells.
    Biochem J. 1994 Oct 1;303 ( Pt 1):27-31 PMID: 7945252
  9. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis.
    Nature. 1994 Dec 22-29;372(6508):739-46 PMID: 7997261
  10. Repression of the heat shock factor 1 transcriptional activation domain is modulated by constitutive phosphorylation.
    Mol Cell Biol. 1997 Apr;17(4):2107-15 PMID: 9121459
  11. Activation of the transcription factor MEF2C by the MAP kinase p38 in inflammation.
    Nature. 1997 Mar 20;386(6622):296-9 PMID: 9069290
  12. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3.
    Science. 1997 Mar 28;275(5308):1930-4 PMID: 9072970
  13. Targeted disruption of the MKK4 gene causes embryonic death, inhibition of c-Jun NH2-terminal kinase activation, and defects in AP-1 transcriptional activity.
    Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3004-9 PMID: 9096336
  14. MNK1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates.
    EMBO J. 1997 Apr 15;16(8):1921-33 PMID: 9155018
  15. Heat stress induces tyrosine phosphorylation/activation of kinase FA/GSK-3 alpha (a human carcinoma dedifferentiation modulator) in A431 cells.
    J Cell Biochem. 1997 Jul 1;66(1):16-26 PMID: 9215524
  16. The modular phosphorylation and activation of p70s6k.
    FEBS Lett. 1997 Jun 23;410(1):78-82 PMID: 9247127
  17. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo.
    J Biol Chem. 1995 Nov 17;270(46):27489-94 PMID: 7499206
  18. Reconstitution of a Mg-ATP-dependent protein phosphatase and its activation through a phosphorylation mechanism.
    FEBS Lett. 1982 Dec 27;150(2):319-24 PMID: 6297978
  19. 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
  20. The heat-shock response.
    Annu Rev Biochem. 1986;55:1151-91 PMID: 2427013
  21. 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
  22. Analysis of the phosphorylation of human heat shock transcription factor-1 by MAP kinase family members.
    J Cell Biochem. 1997 Oct 1;67(1):43-54 PMID: 9328838
  23. HSF1 granules: a novel stress-induced nuclear compartment of human cells.
    J Cell Sci. 1997 Dec;110 ( Pt 23):2925-34 PMID: 9359875
  24. Nuclear accumulation of NFAT4 opposed by the JNK signal transduction pathway.
    Science. 1997 Nov 28;278(5343):1638-41 PMID: 9374467
  25. Optimization of nuclear transcript detection by FISH and combination with fluorescence immunocytochemical detection of transcription factors.
    J Histochem Cytochem. 1997 Dec;45(12):1585-92 PMID: 9389761
  26. Molecular chaperones as HSF1-specific transcriptional repressors.
    Genes Dev. 1998 Mar 1;12(5):654-66 PMID: 9499401
  27. Transcriptional activation of heat shock factor HSF1 probed by phosphopeptide analysis of factor 32P-labeled in vivo.
    J Biol Chem. 1998 Apr 10;273(15):8749-55 PMID: 9535852
  28. Formation of protein kinase recognition sites by covalent modification of the substrate. Molecular mechanism for the synergistic action of casein kinase II and glycogen synthase kinase 3.
    J Biol Chem. 1987 Oct 15;262(29):14042-8 PMID: 2820993
  29. Purification and characterization of a heat-shock element binding protein from yeast.
    EMBO J. 1987 Oct;6(10):3035-41 PMID: 3319580
  30. Activation in vitro of sequence-specific DNA binding by a human regulatory factor.
    Nature. 1988 Sep 22;335(6188):372-5 PMID: 3419505
  31. Purification and characterization of protein phosphatase 1I activating kinase from bovine brain cytosolic and particulate fractions.
    J Biol Chem. 1989 Feb 15;264(5):2985-90 PMID: 2914940
  32. ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF.
    Cell. 1991 May 17;65(4):663-75 PMID: 2032290
  33. Attenuation of the heat shock response in HeLa cells is mediated by the release of bound heat shock transcription factor and is modulated by changes in growth and in heat shock temperatures.
    Genes Dev. 1991 Nov;5(11):2117-27 PMID: 1936996
  34. Activation of protein kinase C increases phosphorylation of the L-myc trans-activator domain at a GSK-3 target site.
    Oncogene. 1992 Feb;7(2):347-53 PMID: 1312697
  35. Glycogen synthase kinase-3: functions in oncogenesis and development.
    Biochim Biophys Acta. 1992 Dec 16;1114(2-3):147-62 PMID: 1333807
  36. Lower heat shock factor activation and binding and faster rate of HSP-70A messenger RNA turnover in heat sensitive human leukemias.
    Cancer Res. 1992 Dec 15;52(24):6815-22 PMID: 1458470
  37. Regulation of heat shock factor trimer formation: role of a conserved leucine zipper.
    Science. 1993 Jan 8;259(5092):230-4 PMID: 8421783
  38. 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
  39. Cells in stress: transcriptional activation of heat shock genes.
    Science. 1993 Mar 5;259(5100):1409-10 PMID: 8451637
  40. 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
  41. 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
  42. The mitogen-activated protein kinase signal transduction pathway.
    J Biol Chem. 1993 Jul 15;268(20):14553-6 PMID: 8325833
  43. Hydrophobic coiled-coil domains regulate the subcellular localization of human heat shock factor 2.
    Genes Dev. 1993 Aug;7(8):1549-58 PMID: 8339932
  44. Inactivation of glycogen synthase kinase-3 beta by phosphorylation: new kinase connections in insulin and growth-factor signalling.
    Biochem J. 1993 Nov 15;296 ( Pt 1):15-9 PMID: 8250835
  45. The alpha-isoform of glycogen synthase kinase-3 from rabbit skeletal muscle is inactivated by p70 S6 kinase or MAP kinase-activated protein kinase-1 in vitro.
    FEBS Lett. 1994 Jan 24;338(1):37-42 PMID: 8307153
  46. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain.
    Cell. 1994 Mar 25;76(6):1025-37 PMID: 8137421
  47. Inhibitors of tyrosine and Ser/Thr phosphatases modulate the heat shock response.
    J Cell Biochem. 1994 Feb;54(2):186-97 PMID: 8175893
  48. The stress-activated protein kinase subfamily of c-Jun kinases.
    Nature. 1994 May 12;369(6476):156-60 PMID: 8177321
  49. Ras-dependent activation of MAP kinase pathway mediated by G-protein beta gamma subunits.
    Nature. 1994 Jun 2;369(6479):418-20 PMID: 8196770
  50. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells.
    Science. 1994 Aug 5;265(5173):808-11 PMID: 7914033
  51. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins.
    Cell. 1994 Sep 23;78(6):1027-37 PMID: 7923353
  52. Translation. Turned on by insulin.
    Nature. 1994 Oct 27;371(6500):747-8 PMID: 7935831
  53. A secondary phosphorylation of CREB341 at Ser129 is required for the cAMP-mediated control of gene expression. A role for glycogen synthase kinase-3 in the control of gene expression.
    J Biol Chem. 1994 Dec 23;269(51):32187-93 PMID: 7798217
  54. Transcription factor ATF2 regulation by the JNK signal transduction pathway.
    Science. 1995 Jan 20;267(5196):389-93 PMID: 7824938
  55. Inactivation of glycogen synthase kinase-3 by epidermal growth factor is mediated by mitogen-activated protein kinase/p90 ribosomal protein S6 kinase signaling pathway in NIH/3T3 cells.
    J Biol Chem. 1995 Jan 20;270(3):987-90 PMID: 7836418
  56. Activation of mitogen-activated protein kinase by arachidonic acid in rat liver epithelial WB cells by a protein kinase C-dependent mechanism.
    J Biol Chem. 1995 Mar 3;270(9):4201-4 PMID: 7876176
  57. Sphingosine 1-phosphate rapidly activates the mitogen-activated protein kinase pathway by a G protein-dependent mechanism.
    J Biol Chem. 1995 May 12;270(19):11484-8 PMID: 7744787
  58. The MAPK signaling cascade.
    FASEB J. 1995 Jun;9(9):726-35 PMID: 7601337
  59. Distinct pathways of Gi- and Gq-mediated mitogen-activated protein kinase activation.
    J Biol Chem. 1995 Jul 21;270(29):17148-53 PMID: 7615510
  60. Angiotensin II stimulates calcium-dependent activation of c-Jun N-terminal kinase.
    Mol Cell Biol. 1995 Nov;15(11):6160-8 PMID: 7565768
  61. Mitogen-activated protein kinase acts as a negative regulator of the heat shock response in NIH3T3 cells.
    Cancer Res. 1995 Dec 1;55(23):5512-9 PMID: 7585624
  62. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B.
    Nature. 1995 Dec 21-28;378(6559):785-9 PMID: 8524413
  63. Evidence for a role of MEK and MAPK during signal transduction by protein kinase C zeta.
    EMBO J. 1995 Dec 15;14(24):6157-63 PMID: 8557035
  64. The regulatory domain of human heat shock factor 1 is sufficient to sense heat stress.
    Mol Cell Biol. 1996 Mar;16(3):839-46 PMID: 8622685
  65. Regulation of both glycogen synthase and PHAS-I by insulin in rat skeletal muscle involves mitogen-activated protein kinase-independent and rapamycin-sensitive pathways.
    J Biol Chem. 1996 Mar 1;271(9):5033-9 PMID: 8617780
  66. 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
  67. Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP Kinase.
    Science. 1996 May 31;272(5266):1347-9 PMID: 8650547
  68. Heat shock transcription factors: structure and regulation.
    Annu Rev Cell Dev Biol. 1995;11:441-69 PMID: 8689565
  69. Characterization of the structure and function of a new mitogen-activated protein kinase (p38beta).
    J Biol Chem. 1996 Jul 26;271(30):17920-6 PMID: 8663524
  70. Localization of human T-cell leukemia virus type 1 tax to subnuclear compartments that overlap with interchromatin speckles.
    J Virol. 1996 Sep;70(9):6347-57 PMID: 8709263
  71. Activation of RAC-protein kinase by heat shock and hyperosmolarity stress through a pathway independent of phosphatidylinositol 3-kinase.
    Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7639-43 PMID: 8755528
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1998-11-00
Pages
6624-33
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC109247
Subset
IM
Grants
NCI NIH HHS · CA62130 · United States
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