Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1995 Feb 11;23(3):467–474. doi: 10.1093/nar/23.3.467

Complex expression of murine heat shock transcription factors.

M T Fiorenza 1, T Farkas 1, M Dissing 1, D Kolding 1, V Zimarino 1
PMCID: PMC306699  PMID: 7885843

Abstract

A central step in the transcriptional activation of heat shock genes is the binding of the heat shock factor (HSF) to upstream heat shock elements (HSEs). In vertebrates, HSF1 mediates the ubiquitous response to stress stimuli, while the role of a second HSE-binding factor, HSF2, is still unclear. In this work we show that both factors are expressed in a wide range of murine tissues and each exists as two splicing isoforms. Although HSFs are virtually ubiquitous proteins, their abundance is predominant in testis and variable among other tissues, indicating specific regulations of their expression. A low level of DNA-binding activity of HSF1, detected in many tissues, is probably physiological and is not explained by an anomalous regulation of one of the two isoforms. Our observations suggest that these regulatory proteins may all have roles in fully developed tissues. This possibility is not mutually exclusive of a role of HSF2 during cellular differentiation and tissue development [L. Sistonen, K. D. Sarge and R. I. Morimoto (1994), Mol. Cell. Biol., 14, 2087-2099].

Full text

PDF
467

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. 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]
  2. Blake M. J., Gershon D., Fargnoli J., Holbrook N. J. Discordant expression of heat shock protein mRNAs in tissues of heat-stressed rats. J Biol Chem. 1990 Sep 5;265(25):15275–15279. [PubMed] [Google Scholar]
  3. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  4. Clos J., Westwood J. T., Becker P. B., Wilson S., Lambert K., Wu C. Molecular cloning and expression of a hexameric Drosophila heat shock factor subject to negative regulation. Cell. 1990 Nov 30;63(5):1085–1097. doi: 10.1016/0092-8674(90)90511-c. [DOI] [PubMed] [Google Scholar]
  5. Foulkes N. S., Sassone-Corsi P. More is better: activators and repressors from the same gene. Cell. 1992 Feb 7;68(3):411–414. doi: 10.1016/0092-8674(92)90178-f. [DOI] [PubMed] [Google Scholar]
  6. Gallo G. J., Prentice H., Kingston R. E. Heat shock factor is required for growth at normal temperatures in the fission yeast Schizosaccharomyces pombe. Mol Cell Biol. 1993 Feb;13(2):749–761. doi: 10.1128/mcb.13.2.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gething M. J., Sambrook J. Protein folding in the cell. Nature. 1992 Jan 2;355(6355):33–45. doi: 10.1038/355033a0. [DOI] [PubMed] [Google Scholar]
  8. Harrison C. J., Bohm A. A., Nelson H. C. Crystal structure of the DNA binding domain of the heat shock transcription factor. Science. 1994 Jan 14;263(5144):224–227. doi: 10.1126/science.8284672. [DOI] [PubMed] [Google Scholar]
  9. Jakobsen B. K., Pelham H. R. A conserved heptapeptide restrains the activity of the yeast heat shock transcription factor. EMBO J. 1991 Feb;10(2):369–375. doi: 10.1002/j.1460-2075.1991.tb07958.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kothary R., Clapoff S., Darling S., Perry M. D., Moran L. A., Rossant J. Inducible expression of an hsp68-lacZ hybrid gene in transgenic mice. Development. 1989 Apr;105(4):707–714. doi: 10.1242/dev.105.4.707. [DOI] [PubMed] [Google Scholar]
  11. Krawczyk Z., Mali P., Parvinen M. Expression of a testis-specific hsp70 gene-related RNA in defined stages of rat seminiferous epithelium. J Cell Biol. 1988 Oct;107(4):1317–1323. doi: 10.1083/jcb.107.4.1317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Krawczyk Z., Szymik N., Wiśniewski J. Expression of hsp70-related gene in developing and degenerating rat testis. Mol Biol Rep. 1987;12(1):35–41. doi: 10.1007/BF00580648. [DOI] [PubMed] [Google Scholar]
  13. Kroeger P. E., Sarge K. D., Morimoto R. I. Mouse heat shock transcription factors 1 and 2 prefer a trimeric binding site but interact differently with the HSP70 heat shock element. Mol Cell Biol. 1993 Jun;13(6):3370–3383. doi: 10.1128/mcb.13.6.3370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Larson J. S., Schuetz T. J., Kingston R. E. Activation in vitro of sequence-specific DNA binding by a human regulatory factor. Nature. 1988 Sep 22;335(6188):372–375. doi: 10.1038/335372a0. [DOI] [PubMed] [Google Scholar]
  15. Lindquist S., Craig E. A. The heat-shock proteins. Annu Rev Genet. 1988;22:631–677. doi: 10.1146/annurev.ge.22.120188.003215. [DOI] [PubMed] [Google Scholar]
  16. Lis J., Wu C. Protein traffic on the heat shock promoter: parking, stalling, and trucking along. Cell. 1993 Jul 16;74(1):1–4. doi: 10.1016/0092-8674(93)90286-y. [DOI] [PubMed] [Google Scholar]
  17. Mezger V., Bensaude O., Morange M. Unusual levels of heat shock element-binding activity in embryonal carcinoma cells. Mol Cell Biol. 1989 Sep;9(9):3888–3896. doi: 10.1128/mcb.9.9.3888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Murphy S. P., Gorzowski J. J., Sarge K. D., Phillips B. Characterization of constitutive HSF2 DNA-binding activity in mouse embryonal carcinoma cells. Mol Cell Biol. 1994 Aug;14(8):5309–5317. doi: 10.1128/mcb.14.8.5309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nakai A., Morimoto R. I. 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):1983–1997. doi: 10.1128/mcb.13.4.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Peteranderl R., Nelson H. C. Trimerization of the heat shock transcription factor by a triple-stranded alpha-helical coiled-coil. Biochemistry. 1992 Dec 8;31(48):12272–12276. doi: 10.1021/bi00163a042. [DOI] [PubMed] [Google Scholar]
  21. Rabindran S. K., Giorgi G., Clos J., Wu C. Molecular cloning and expression of a human heat shock factor, HSF1. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):6906–6910. doi: 10.1073/pnas.88.16.6906. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rabindran S. K., Haroun R. I., Clos J., Wisniewski J., Wu C. Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science. 1993 Jan 8;259(5092):230–234. doi: 10.1126/science.8421783. [DOI] [PubMed] [Google Scholar]
  23. Rosario M. O., Perkins S. L., O'Brien D. A., Allen R. L., Eddy E. M. Identification of the gene for the developmentally expressed 70 kDa heat-shock protein (P70) of mouse spermatogenic cells. Dev Biol. 1992 Mar;150(1):1–11. doi: 10.1016/0012-1606(92)90002-x. [DOI] [PubMed] [Google Scholar]
  24. Sarge K. D., Murphy S. P., Morimoto R. I. 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):1392–1407. doi: 10.1128/mcb.13.3.1392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sarge K. D., Park-Sarge O. K., Kirby J. D., Mayo K. E., Morimoto R. I. Expression of heat shock factor 2 in mouse testis: potential role as a regulator of heat-shock protein gene expression during spermatogenesis. Biol Reprod. 1994 Jun;50(6):1334–1343. doi: 10.1095/biolreprod50.6.1334. [DOI] [PubMed] [Google Scholar]
  26. Sarge K. D., Zimarino V., Holm K., Wu C., Morimoto R. I. Cloning and characterization of two mouse heat shock factors with distinct inducible and constitutive DNA-binding ability. Genes Dev. 1991 Oct;5(10):1902–1911. doi: 10.1101/gad.5.10.1902. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Schuetz T. J., Gallo G. J., Sheldon L., Tempst P., Kingston R. E. Isolation of a cDNA for HSF2: evidence for two heat shock factor genes in humans. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):6911–6915. doi: 10.1073/pnas.88.16.6911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sheldon L. A., Kingston R. E. Hydrophobic coiled-coil domains regulate the subcellular localization of human heat shock factor 2. Genes Dev. 1993 Aug;7(8):1549–1558. doi: 10.1101/gad.7.8.1549. [DOI] [PubMed] [Google Scholar]
  30. Sistonen L., Sarge K. D., Morimoto R. I. Human heat shock factors 1 and 2 are differentially activated and can synergistically induce hsp70 gene transcription. Mol Cell Biol. 1994 Mar;14(3):2087–2099. doi: 10.1128/mcb.14.3.2087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sistonen L., Sarge K. D., Phillips B., Abravaya K., Morimoto R. I. Activation of heat shock factor 2 during hemin-induced differentiation of human erythroleukemia cells. Mol Cell Biol. 1992 Sep;12(9):4104–4111. doi: 10.1128/mcb.12.9.4104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Studier F. W., Moffatt B. A. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol. 1986 May 5;189(1):113–130. doi: 10.1016/0022-2836(86)90385-2. [DOI] [PubMed] [Google Scholar]
  34. Treuter E., Nover L., Ohme K., Scharf K. D. Promoter specificity and deletion analysis of three heat stress transcription factors of tomato. Mol Gen Genet. 1993 Jul;240(1):113–125. doi: 10.1007/BF00276890. [DOI] [PubMed] [Google Scholar]
  35. Vuister G. W., Kim S. J., Wu C., Bax A. NMR evidence for similarities between the DNA-binding regions of Drosophila melanogaster heat shock factor and the helix-turn-helix and HNF-3/forkhead families of transcription factors. Biochemistry. 1994 Jan 11;33(1):10–16. doi: 10.1021/bi00167a002. [DOI] [PubMed] [Google Scholar]
  36. Wagner M., Perry R. P. Characterization of the multigene family encoding the mouse S16 ribosomal protein: strategy for distinguishing an expressed gene from its processed pseudogene counterparts by an analysis of total genomic DNA. Mol Cell Biol. 1985 Dec;5(12):3560–3576. doi: 10.1128/mcb.5.12.3560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wiederrecht G., Seto D., Parker C. S. Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell. 1988 Sep 9;54(6):841–853. doi: 10.1016/s0092-8674(88)91197-x. [DOI] [PubMed] [Google Scholar]
  38. Zakeri Z. F., Wolgemuth D. J. Developmental-stage-specific expression of the hsp70 gene family during differentiation of the mammalian male germ line. Mol Cell Biol. 1987 May;7(5):1791–1796. doi: 10.1128/mcb.7.5.1791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zimarino V., Tsai C., Wu C. Complex modes of heat shock factor activation. Mol Cell Biol. 1990 Feb;10(2):752–759. doi: 10.1128/mcb.10.2.752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Zimarino V., Wilson S., Wu C. Antibody-mediated activation of Drosophila heat shock factor in vitro. Science. 1990 Aug 3;249(4968):546–549. doi: 10.1126/science.2200124. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES