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

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 1998 Oct 17

PMID 9774677

Citations 50

Authors

B He

Y H Meng

N F Mivechi

Affiliations

Soon will be listed here.

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.

Citing Articles

The dance of proteostasis and metabolism: Unveiling the caloristatic controlling switch.

Schroeder H, de Lemos Muller C, Heck T, Krause M, Homem de Bittencourt Jr P Cell Stress Chaperones. 2024; 29(1):175-200.

PMID: 38331164 PMC: 10939077. DOI: 10.1016/j.cstres.2024.02.002.

Heat shock response during the resolution of inflammation and its progressive suppression in chronic-degenerative inflammatory diseases.

Schroeder H, de Lemos Muller C, Heck T, Krause M, Homem de Bittencourt P Cell Stress Chaperones. 2024; 29(1):116-142.

PMID: 38244765 PMC: 10939074. DOI: 10.1016/j.cstres.2024.01.002.

Brassinosteroids promote thermotolerance through releasing BIN2-mediated phosphorylation and suppression of HsfA1 transcription factors in Arabidopsis.

Luo J, Jiang J, Sun S, Wang X Plant Commun. 2022; 3(6):100419.

PMID: 35927943 PMC: 9700127. DOI: 10.1016/j.xplc.2022.100419.

HSF-1: Guardian of the Proteome Through Integration of Longevity Signals to the Proteostatic Network.

Lazaro-Pena M, Ward Z, Yang S, Strohm A, Merrill A, Soto C Front Aging. 2022; 3:861686.

PMID: 35874276 PMC: 9304931. DOI: 10.3389/fragi.2022.861686.

AKT1 mediates multiple phosphorylation events that functionally promote HSF1 activation.

Lu W, Omari R, Ray H, Wang J, Williams I, Jacobs C FEBS J. 2022; 289(13):3876-3893.

PMID: 35080342 PMC: 9309721. DOI: 10.1111/febs.16375.

References

Morimoto R . Cells in stress: transcriptional activation of heat shock genes. Science. 1993; 259(5100):1409-10. DOI: 10.1126/science.8451637. View

Crespo P, Xu N, Simonds W, Gutkind J . Ras-dependent activation of MAP kinase pathway mediated by G-protein beta gamma subunits. Nature. 1994; 369(6479):418-20. DOI: 10.1038/369418a0. View

Boulton T, Nye S, Robbins D, Ip N, Radziejewska E, Morgenbesser S . ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell. 1991; 65(4):663-75. DOI: 10.1016/0092-8674(91)90098-j. View

Kyriakis J, Avruch J . Sounding the alarm: protein kinase cascades activated by stress and inflammation. J Biol Chem. 1996; 271(40):24313-6. DOI: 10.1074/jbc.271.40.24313. View

Newton E, Knauf U, Green M, Kingston R . The regulatory domain of human heat shock factor 1 is sufficient to sense heat stress. Mol Cell Biol. 1996; 16(3):839-46. PMC: 231064. DOI: 10.1128/MCB.16.3.839. View

Tung H, Reed L . Purification and characterization of protein phosphatase 1I activating kinase from bovine brain cytosolic and particulate fractions. J Biol Chem. 1989; 264(5):2985-90. View

Cotto J, Kline M, Morimoto R . Activation of heat shock factor 1 DNA binding precedes stress-induced serine phosphorylation. Evidence for a multistep pathway of regulation. J Biol Chem. 1996; 271(7):3355-8. DOI: 10.1074/jbc.271.7.3355. View

Yang S, Lee S, Chang H . Heat stress induces tyrosine phosphorylation/activation of kinase FA/GSK-3 alpha (a human carcinoma dedifferentiation modulator) in A431 cells. J Cell Biochem. 1997; 66(1):16-26. View

Cotto J, Fox S, Morimoto R . HSF1 granules: a novel stress-induced nuclear compartment of human cells. J Cell Sci. 1998; 110 ( Pt 23):2925-34. DOI: 10.1242/jcs.110.23.2925. View

10.

Yang D, Tournier C, Wysk M, Lu H, Xu J, Davis R . 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; 94(7):3004-9. PMC: 20312. DOI: 10.1073/pnas.94.7.3004. View

11.

Azpiazu I, Saltiel A, DePaoli-Roach A, Lawrence J . 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; 271(9):5033-9. DOI: 10.1074/jbc.271.9.5033. View

12.

Xia W, Guo Y, Vilaboa N, Zuo J, Voellmy R . Transcriptional activation of heat shock factor HSF1 probed by phosphopeptide analysis of factor 32P-labeled in vivo. J Biol Chem. 1998; 273(15):8749-55. DOI: 10.1074/jbc.273.15.8749. View

13.

Hemmings B, Resink T, Cohen P . Reconstitution of a Mg-ATP-dependent protein phosphatase and its activation through a phosphorylation mechanism. FEBS Lett. 1982; 150(2):319-24. DOI: 10.1016/0014-5793(82)80760-6. View

14.

Pullen N, Thomas G . The modular phosphorylation and activation of p70s6k. FEBS Lett. 1997; 410(1):78-82. DOI: 10.1016/s0014-5793(97)00323-2. View

15.

Shi Y, Mosser D, Morimoto R . Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev. 1998; 12(5):654-66. PMC: 316571. DOI: 10.1101/gad.12.5.654. View

16.

Sarge K, Murphy S, Morimoto R . 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; 13(3):1392-407. PMC: 359449. DOI: 10.1128/mcb.13.3.1392-1407.1993. View

17.

Konishi H, Matsuzaki H, Tanaka M, Ono Y, Tokunaga C, Kuroda S . 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; 93(15):7639-43. PMC: 38799. DOI: 10.1073/pnas.93.15.7639. View

18.

Jolly C, Mongelard F, Vourch C . Optimization of nuclear transcript detection by FISH and combination with fluorescence immunocytochemical detection of transcription factors. J Histochem Cytochem. 1998; 45(12):1585-92. DOI: 10.1177/002215549704501201. View

19.

Han J, Lee J, Bibbs L, Ulevitch R . A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science. 1994; 265(5173):808-11. DOI: 10.1126/science.7914033. View

20.

Wu J, Spiegel S, Sturgill T . Sphingosine 1-phosphate rapidly activates the mitogen-activated protein kinase pathway by a G protein-dependent mechanism. J Biol Chem. 1995; 270(19):11484-8. DOI: 10.1074/jbc.270.19.11484. View