Abstract
Phosphorylation is one of the mechanisms controlling the activity of heat-shock transcription factors in yeast and mammalian cells. Here we describe partial purification, identification, and characterization of a protein kinase that phosphorylates the Arabidopsis heat-shock factor AtHSF1 at multiple serine residues. The HSF1 kinase forms a stable complex with AtHSF1, which can be detected by kinase pull-down assays using a histidine-tagged AtHSF1 substrate. The HSF1 kinase interacts with the cell-cycle control protein Suc1p and is immunoprecipitated by an antibody specific for the Arabidopsis cyclin-dependent CDC2a kinase. Phosphorylation by CDC2a in vitro inhibits DNA binding of AtHSF1 to the cognate heat-shock elements, suggesting a possible regulatory interaction between heat-shock response and cell-cycle control in plants.
Full Text
The Full Text of this article is available as a PDF (2.4 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Abravaya K., Myers M. P., Murphy S. P., Morimoto R. I. The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev. 1992 Jul;6(7):1153–1164. doi: 10.1101/gad.6.7.1153. [DOI] [PubMed] [Google Scholar]
- Adler V., Schaffer A., Kim J., Dolan L., Ronai Z. UV irradiation and heat shock mediate JNK activation via alternate pathways. J Biol Chem. 1995 Nov 3;270(44):26071–26077. doi: 10.1074/jbc.270.44.26071. [DOI] [PubMed] [Google Scholar]
- Anderson R. L., Van Kersen I., Kraft P. E., Hahn G. M. Biochemical analysis of heat-resistant mouse tumor cell strains: a new member of the HSP70 family. Mol Cell Biol. 1989 Aug;9(8):3509–3516. doi: 10.1128/mcb.9.8.3509. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baler R., Dahl G., Voellmy R. 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):2486–2496. doi: 10.1128/mcb.13.4.2486. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baler R., Welch W. J., Voellmy R. Heat shock gene regulation by nascent polypeptides and denatured proteins: hsp70 as a potential autoregulatory factor. J Cell Biol. 1992 Jun;117(6):1151–1159. doi: 10.1083/jcb.117.6.1151. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bourne Y., Watson M. H., Hickey M. J., Holmes W., Rocque W., Reed S. I., Tainer J. A. Crystal structure and mutational analysis of the human CDK2 kinase complex with cell cycle-regulatory protein CksHs1. Cell. 1996 Mar 22;84(6):863–874. doi: 10.1016/s0092-8674(00)81065-x. [DOI] [PubMed] [Google Scholar]
- Cotto J. J., Kline M., Morimoto R. I. 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):3355–3358. doi: 10.1074/jbc.271.7.3355. [DOI] [PubMed] [Google Scholar]
- Craig E. A., Gross C. A. Is hsp70 the cellular thermometer? Trends Biochem Sci. 1991 Apr;16(4):135–140. doi: 10.1016/0968-0004(91)90055-z. [DOI] [PubMed] [Google Scholar]
- Ferreira P. C., Hemerly A. S., Villarroel R., Van Montagu M., Inzé D. The Arabidopsis functional homolog of the p34cdc2 protein kinase. Plant Cell. 1991 May;3(5):531–540. doi: 10.1105/tpc.3.5.531. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Høj A., Jakobsen B. K. A short element required for turning off heat shock transcription factor: evidence that phosphorylation enhances deactivation. EMBO J. 1994 Jun 1;13(11):2617–2624. doi: 10.1002/j.1460-2075.1994.tb06552.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hübel A., Lee J. H., Wu C., Schöffl F. Arabidopsis heat shock factor is constitutively active in Drosophila and human cells. Mol Gen Genet. 1995 Jul 28;248(2):136–141. doi: 10.1007/BF02190794. [DOI] [PubMed] [Google Scholar]
- Hübel A., Schöffl F. Arabidopsis heat shock factor: isolation and characterization of the gene and the recombinant protein. Plant Mol Biol. 1994 Oct;26(1):353–362. doi: 10.1007/BF00039545. [DOI] [PubMed] [Google Scholar]
- Imajuku Y., Hirayama T., Endoh H., Oka A. Exon-intron organization of the Arabidopsis thaliana protein kinase genes CDC2a and CDC2b. FEBS Lett. 1992 Jun 8;304(1):73–77. doi: 10.1016/0014-5793(92)80592-5. [DOI] [PubMed] [Google Scholar]
- Jackson S. P. The recognition of DNA damage. Curr Opin Genet Dev. 1996 Feb;6(1):19–25. doi: 10.1016/s0959-437x(96)90005-2. [DOI] [PubMed] [Google Scholar]
- Jakobsen B. K., Pelham H. R. Constitutive binding of yeast heat shock factor to DNA in vivo. Mol Cell Biol. 1988 Nov;8(11):5040–5042. doi: 10.1128/mcb.8.11.5040. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jerry D. J. Monitoring coupling of peptides to carrier proteins using biotinylated peptide. Biotechniques. 1993 Mar;14(3):464–469. [PubMed] [Google Scholar]
- Larson J. S., Schuetz T. J., Kingston R. E. In vitro activation of purified human heat shock factor by heat. Biochemistry. 1995 Feb 14;34(6):1902–1911. doi: 10.1021/bi00006a011. [DOI] [PubMed] [Google Scholar]
- Lee J. H., Hübel A., Schöffl F. Derepression of the activity of genetically engineered heat shock factor causes constitutive synthesis of heat shock proteins and increased thermotolerance in transgenic Arabidopsis. Plant J. 1995 Oct;8(4):603–612. doi: 10.1046/j.1365-313x.1995.8040603.x. [DOI] [PubMed] [Google Scholar]
- Lee J. H., Schöffl F. An Hsp70 antisense gene affects the expression of HSP70/HSC70, the regulation of HSF, and the acquisition of thermotolerance in transgenic Arabidopsis thaliana. Mol Gen Genet. 1996 Aug 27;252(1-2):11–19. doi: 10.1007/s004389670002. [DOI] [PubMed] [Google Scholar]
- Li G. C., Yang S. H., Kim D., Nussenzweig A., Ouyang H., Wei J., Burgman P., Li L. Suppression of heat-induced hsp70 expression by the 70-kDa subunit of the human Ku autoantigen. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4512–4516. doi: 10.1073/pnas.92.10.4512. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McConnell K., Dynan W. S. The DNA-dependent protein kinase: a matter of life and (cell) death. Curr Opin Cell Biol. 1996 Jun;8(3):325–330. doi: 10.1016/s0955-0674(96)80005-6. [DOI] [PubMed] [Google Scholar]
- Meijer L., Arion D., Golsteyn R., Pines J., Brizuela L., Hunt T., Beach D. Cyclin is a component of the sea urchin egg M-phase specific histone H1 kinase. EMBO J. 1989 Aug;8(8):2275–2282. doi: 10.1002/j.1460-2075.1989.tb08353.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mizoguchi T., Yamaguchi-Shinozaki K., Hayashida N., Kamada H., Shinozaki K. Cloning and characterization of two cDNAs encoding casein kinase II catalytic subunits in Arabidopsis thaliana. Plant Mol Biol. 1993 Jan;21(2):279–289. doi: 10.1007/BF00019944. [DOI] [PubMed] [Google Scholar]
- Mosser D. D., Duchaine J., Massie B. The DNA-binding activity of the human heat shock transcription factor is regulated in vivo by hsp70. Mol Cell Biol. 1993 Sep;13(9):5427–5438. doi: 10.1128/mcb.13.9.5427. [DOI] [PMC free article] [PubMed] [Google Scholar]
- O'Brien T., Hardin S., Greenleaf A., Lis J. T. Phosphorylation of RNA polymerase II C-terminal domain and transcriptional elongation. Nature. 1994 Jul 7;370(6484):75–77. doi: 10.1038/370075a0. [DOI] [PubMed] [Google Scholar]
- Parsell D. A., Lindquist S. The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet. 1993;27:437–496. doi: 10.1146/annurev.ge.27.120193.002253. [DOI] [PubMed] [Google Scholar]
- Peterson S. R., Jesch S. A., Chamberlin T. N., Dvir A., Rabindran S. K., Wu C., Dynan W. S. Stimulation of the DNA-dependent protein kinase by RNA polymerase II transcriptional activator proteins. J Biol Chem. 1995 Jan 20;270(3):1449–1454. doi: 10.1074/jbc.270.3.1449. [DOI] [PubMed] [Google Scholar]
- Scharf K. D., Rose S., Zott W., Schöffl F., Nover L., Schöff F. Three tomato genes code for heat stress transcription factors with a region of remarkable homology to the DNA-binding domain of the yeast HSF. EMBO J. 1990 Dec;9(13):4495–4501. doi: 10.1002/j.1460-2075.1990.tb07900.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sorger P. K., Lewis M. J., Pelham H. R. Heat shock factor is regulated differently in yeast and HeLa cells. Nature. 1987 Sep 3;329(6134):81–84. doi: 10.1038/329081a0. [DOI] [PubMed] [Google Scholar]
- Sorger P. K., Pelham H. R. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell. 1988 Sep 9;54(6):855–864. doi: 10.1016/s0092-8674(88)91219-6. [DOI] [PubMed] [Google Scholar]
- Stewart E., Enoch T. S-phase and DNA-damage checkpoints: a tale of two yeasts. Curr Opin Cell Biol. 1996 Dec;8(6):781–787. doi: 10.1016/s0955-0674(96)80078-0. [DOI] [PubMed] [Google Scholar]
- Westwood J. T., Wu C. Activation of Drosophila heat shock factor: conformational change associated with a monomer-to-trimer transition. Mol Cell Biol. 1993 Jun;13(6):3481–3486. doi: 10.1128/mcb.13.6.3481. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wu C. Heat shock transcription factors: structure and regulation. Annu Rev Cell Dev Biol. 1995;11:441–469. doi: 10.1146/annurev.cb.11.110195.002301. [DOI] [PubMed] [Google Scholar]