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Vol. 20, Issue 5, 1340-1347, March 1, 2009

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Heterotrimerization of Heat-Shock Factors 1 and 2 Provides a Transcriptional Switch in Response to Distinct Stimuli

Anton Sandqvist^*,, Johanna K. Björk^*,, Malin Åkerfelt^*,, Zhanna Chitikova^*,, Alexei Grichine, Claire Vourc'h, Caroline Jolly, Tiina A. Salminen, Yvonne Nymalm, and Lea Sistonen^*,

*Turku Centre for Biotechnology, University of Turku, Åbo Akademi University, 20520 Turku, Finland; Departments of Biochemistry and Pharmacy and Biology, Åbo Akademi University, 20520 Turku, Finland; and Institut National de la Santé et de la Recherche Médicale, U823, Institut Albert Bonniot; Université Joseph Fourier, Institut Albert Bonniot, Grenoble 38700, France

Submitted August 22, 2008; Revised December 19, 2008; Accepted December 23, 2008
Monitoring Editor: M. Bishr Omary

Organisms respond to circumstances threatening the cellular protein homeostasis by activation of heat-shock transcription factors (HSFs), which play important roles in stress resistance, development, and longevity. Of the four HSFs in vertebrates (HSF1-4), HSF1 is activated by stress, whereas HSF2 lacks intrinsic stress responsiveness. The mechanism by which HSF2 is recruited to stress-inducible promoters and how HSF2 is activated is not known. However, changes in the HSF2 expression occur, coinciding with the functions of HSF2 in development. Here, we demonstrate that HSF1 and HSF2 form heterotrimers when bound to satellite III DNA in nuclear stress bodies, subnuclear structures in which HSF1 induces transcription. By depleting HSF2, we show that HSF1-HSF2 heterotrimerization is a mechanism regulating transcription. Upon stress, HSF2 DNA binding is HSF1 dependent. Intriguingly, when the elevated expression of HSF2 during development is mimicked, HSF2 binds to DNA and becomes transcriptionally competent. HSF2 activation leads to activation of also HSF1, revealing a functional interdependency that is mediated through the conserved trimerization domains of these factors. We propose that heterotrimerization of HSF1 and HSF2 integrates transcriptional activation in response to distinct stress and developmental stimuli.

Address correspondence to: Lea Sistonen (lea.sistonen{at}btk.fi)

Abbreviations used: HSF, heat-shock factor; Hsp, heat-shock protein; nSB, nuclear stress body; sat III, satellite III.

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