MINIREVIEW
Novel aspects of heat shock factors: DNA recognition,
chromatin modulation and gene expression
Hiroshi Sakurai and Yasuaki Enoki
Department of Clinical Laboratory Science, Kanazawa University Graduate School of Medical Science, Ishikawa, Japan
Background
The heat shock factor (HSF) in eukaryotes is involved
not only in heat shock protein (HSP) gene expression
and stress resistance, but also in the expression of
genes with roles in cell maintenance and differentia-
tion, as well as in developmental processes. HSF forms
a homotrimer that binds to gene promoters containing
a heat shock element (HSE), which is composed of
multiple inverted repeats of the pentanucleotide motif
nGAAn. Functional conservation of HSFs among
eukaryotes has been revealed by the finding that HSFs
from various organisms, including insects, mammals
and plants, can substitute for yeast HSF in Saccharo-
myces [1–4].
HSF proteins contain two evolutionarily conserved
functional modules: the DNA-binding domain (DBD)
at the amino-terminus and the oligomerization domain
in the central region of the protein [1,4]. The HSF
DBD belongs to the ‘winged’ helix-turn-helix family of
DNA-binding proteins and contains a three-helix bun-
dle capped by a four-stranded antiparallel b-sheet, and
a flexible loop or ‘wing’ with a less ordered structure
(Fig. 1) [5,6]. The second and third a-helices comprise
the helix-turn-helix motif. The oligomerization domain
consists of arrays of hydrophobic heptad repeats
(HRs), characteristic of helical coiled-coil structures

processes. Mammalian cells have four HSF family members involved in dif-
ferent, but in some cases similar, biological functions, including stress resis-
tance, cell differentiation and development. Mammalian HSF family
members exhibit differential specificity for different types of heat shock ele-
ments, which, together with cell type-specific expression of HSFs is impor-
tant in determining the target genes of each HSF. This minireview focuses
on the molecular mechanisms of DNA recognition, chromatin modulation
and gene expression by yeast and mammalian HSFs.
Abbreviations
3P, three perfect repeats; DBD, DNA-binding domain; HDAC1, ; HDAC2, ; HR, hydrophobic heptad repeat; HSE, heat shock element; HSF,
heat shock factor; HSP, heat shock protein; ncRNA, noncoding RNA; PARP, poly(ADP)-ribose polymerase; Pol II, RNA polymerase II;
SAGA, Spt-Ada-Gcn5 acetyltransferase; TFIIA, general transcription factor IIA.
4140 FEBS Journal 277 (2010) 4140–4149 ª 2010 The Authors Journal compilation ª 2010 FEBS
Trimerization of HSF polypeptides is a prerequisite
for binding to the HSE. Under physiological condi-
tions, stress-inducible HSFs, such as Drosophila HSF
and mammalian HSF1, are found in an inactive mono-
meric form. In vitro analysis has shown that inactive
monomeric HSF directly senses heat and oxidative
stress, and becomes able to trimerize and bind to the
HSE [8,9]. Drosophila HSF and mammalian HSF1
have a third HR, HR-C, adjacent to the carboxy-ter-
minus of the protein [10]. The HR-C maintains HSFs
in a monomeric form by suppressing trimerization
through intramolecular coiled-coil interactions with the
HR-A ⁄ B. Under stress conditions, the HR-A ⁄ B–HR-C
interaction is disrupted, thereby leading to intermolec-
ular coiled-coil interactions of the HR-A ⁄ B, although
the detailed molecular mechanisms are unknown
[10–12]. In addition, protein–protein interactions with

cal axis of the DNA. The evolutionarily conserved
arginine residue in this recognition helix makes two
hydrogen bonds with G
2
of the pentanucleotide
n
1
G
2
A
3
A
4
n
5
(Fig. 1). Additional direct contacts
include van der Waals bonds between the arginine and
a conserved serine residue and the thymine comple-
mentary to the third A
3
. The remaining contacts with
the DNA are to the phosphate backbone. Consistent
with the structural data, in vitro-binding assays have
shown that the order of importance of the bases in the
nGAAn repeat is G
2
>A
3
>A
4

Disulfide bond formation in mammalian HSF1
S1
PHFLTKLWILVDDAVLDHVIRWGKDGHSFQIVNEETFAREVLPKYFKHNKITSFIRQLNMYGSRKVFALQTEKTSQENKISIEFQHPLFKR
Mm3
Fig. 1. Amino acid sequences of HSF DBDs. The DBD contains three a-helices (H1, H2 and H3), four b-sheets (S1, S2, S3 and S4), a ‘turn’
of the helix-turn-helix motif and a disordered loop referred to as a ‘wing’. The linker region connects between the DBD and the HR-A ⁄ B
motifs. The amino acid sequences of the DBDs from Kluyveromyces HSF (Kl), Saccharomyces HSF (Sc), Drosophila HSF (Dm), human HSF1
(Hs1), HSF2 (Hs2) and HSF4 (Hs4), and mouse HSF3 (Mm3) are shown. Residues making contacts with DNA are shown in red, residues
that have aromatic–aromatic interactions are shown in blue, cysteine residues that form a disulfide bond are shown in green and conserved
residues are shown in black.
H. Sakurai and Y. Enoki HSF–HSE interaction
FEBS Journal 277 (2010) 4140–4149 ª 2010 The Authors Journal compilation ª 2010 FEBS 4141
(possibly one from each trimer) not making contact
with the DNA (Fig. 2A, B) [14,20,21]. The dissociation
constant of Drosophila HSF for an HSE containing six
or more units (2 · 10
)15
m at 25 °C) is significantly
lower than that for an HSE containing three perfect
repeats (3P) (4 · 10
)12
m at 25 °C) [19]. Multiple
inverted repeats of nGAAn found at the promoter
regions of many HSP genes provide high affinity-bind-
ing sites for HSF.
The DBD–DBD interaction is important in the
HSF–HSF and HSF–HSE interactions. In HSF DBD–
HSE co-crystals, the protein–protein interface consists
of the helix 2 amino-terminus, the turn and the wing
[15]. Unlike other winged helix-turn-helix proteins, the

[27,28]. Heat shock and oxidative stress lead to
enhanced binding of HSF to HSEs in yeast [27,29].
However, whether the trimerization status and ⁄ or
the affinity of each DBD for nGAAn changes under
stress conditions is not known. The activation
domains at the amino- and carboxy-termini are
required for the transient and sustained heat shock
responses, respectively [30]. Phosphorylation of HSF,
regulated by heat and oxidative stress, is involved in
the activation and inactivation of the transactivating
ability [26]. Interestingly, Saccharomyces HSF is unu-
sual among transcriptional activators because it can
bypass a need for critical general transcription factors
and co-activators, including general transcription fac-
tor IIA (TFIIA) [31], Kin28 (a C-terminal-domain
kinase of TFIIH) [32], the Taf9 subunit of TFIID
and Spt-Ada-Gcn5 acetyltransferase (SAGA) [33,34],
and the Med17 and Med22 subunits of Mediator [32].
Although the archetypical HSE is a sequence of con-
tinuous perfect inverted repeats of nGAAn (perfect-
type), the Saccharomyces HSF tolerates the presence of
gaps between the units [28,35]. The gap-type HSE con-
sists of two inverted nGAAn units followed by another
unit after a gap of 5 bp, and the step-type HSE con-
sists of three direct units, each interrupted by 5 bp
(Fig. 2A). In the discontinuous gap- and step-type
Two trimers on 4P-type HSE
One trimer on step-type HSE
One trimer on gap-type HSE
One trimer on 3P-type HSE

uous HSEs, the HSF trimer dissociates from two units
and quickly rebinds to another two units, thereby sta-
bilizing the protein–DNA complex (Fig. 2B). Gap-type
HSEs are involved in moderate stress-induced tran-
scription, whereas step-type HSEs are involved in basal
constitutive transcription and in low-level activation
[28,36]. These discontinuous HSEs are widely used as
HSF-binding sequences, at least in the Saccharomyces
genome, because approximately half of the HSF target
genes contain these types of HSE [37].
The number of HSF trimers bound to an HSE
affects the subsequent acquisition of the transactivat-
ing capacity. In HSF, a C-terminal modulator
domain is necessary for stress-induced hyperphosph-
orylation of the protein and for transcriptional activa-
tion of a gene by a single trimer bound to HSEs with
three nGAAn units (3P-, gap-, or step-type). How-
ever, the C-terminal modulator, and thereby hyper-
phosphorylation, are not necessary for transcriptional
activation by trimers cooperatively bound to HSEs
containing four or more repeat units [20,29]. The
HR-A ⁄ B is indispensable for binding of a single tri-
mer to three-unit HSEs and for HSF hyperphosph-
orylation, but HR-A ⁄ B is not required for binding
HSEs with four or more units or for transactivation
at these HSEs. These results indicate that trimer–tri-
mer interactions are implicated not only in the coop-
erative binding of HSF to the DNA, but also in
transcriptional activation [36]. Although the role of
hyperphosphorylation in transcriptional activation is

and transactivating abilities upon stress, a little HSF1
trimer is present constitutively in cells and binds to
and regulates the expression of genes without any
apparent stress intervention [1,3].
HSF2 and HSF4 may not be directly involved in the
stress response, but rather in cell differentiation and
development [3]. In addition to covalent modifications,
including phosphorylation, SUMOylation and ubiquiti-
nation, the regulatory roles of HSF2 and HSF4 are
dependent on their cellular concentrations [2]. The
non-DNA-binding form of HSF2 exists primarily in
the cytoplasm as a dimer, which has been suggested to
require an interaction between HR-A⁄ B and HR-C.
Although the signals responsible for activation of
HSF2 remain enigmatic, activated HSF2 trimerizes
and binds to HSEs [39]. HSF2 possesses an activation
domain at the carboxy-terminus, but the activity is sig-
nificantly lower than the activation domain of HSF1
[2]. During development, HSF2 is important for neural
specification and spermatogenesis [3]. HSF4 lacks the
HR-C, and trimeric HSF4 is able to constitutively bind
to the HSEs of target genes [40]. Alternative splicing
of the HSF4 transcript results in the production of
two isoforms, HSF4a and HSF4b. HSF4b has the
potential to activate transcription, whereas HSF4a
does not [2]. HSF4 is required for ocular lens develop-
ment and fibre cell differentiation [3].
The HSF3 gene was recently identified in mouse as
an orthologue of the chicken HSF3 gene; however,
the human HSF3 gene is a pseudogene [41]. Mouse

continuous HSEs. When HSF1, HSF2 and HSF4 are
expressed in yeast cells, transcription of various genes
is differentially regulated by the three HSFs and corre-
lated with the type of HSE, namely perfect, gap, or
step [21,45]. These observations indicate that the con-
figuration of the nGAAn unit is an important determi-
nant of HSF–HSE interactions. This is consistent with
the notion that although DNA-binding transcription
factors of the same family bind the same highest-affin-
ity sites, they prefer different lower-affinity sites, and
that low-affinity sites do contribute to factor binding
and gene expression [46].
Differences in the HSE-binding specificity are in part
explained by the oligomerization of HSFs. When an
amino acid substitution is made in the HR-A⁄ Bof
HSF4, the protein exhibits a reduced ability to trimerize
and is unable to bind to discontinuous gap- and step-type
HSEs, but binding to the continuous 3P-type HSE is not
affected [21]. In contrast, an amino acid substitution in
the HR-C of HSF1 enables HSF1 to constitutively form
trimers that bind to discontinuous HSEs [45]. Similar
results have been obtained by introducing oligomeriza-
tion-prone mutations into the HSF1 DBD [45]. On
discontinuous HSEs, in which two pairs of two nGAAn
units provide a platform for binding two DBDs of a
single HSF trimer, stable oligomerization inhibits disso-
ciation and ⁄ or stimulates rebinding of HSF (Fig. 2B).
Interestingly, HSF1 and HSF2 form heterotrimers
via the HR-A ⁄ B regions [47–49]. When HSF1 and
HSF2 bind as a complex to satellite III DNA in

and RSC) and histone chaperones (Asf1, Spt6 and
Spt16), are involved in histone acetylation and eviction
[52–55]. Stress-inducible or constitutive binding of
HSF to a promoter is dependent on the structure of
the HSE. The HSP12 promoter possesses a low-affinity
HSE and a binding site for the general stress response
transcription factors Msn2 and Msn4 (Msn2 ⁄ 4).
However, HSF and Msn2 ⁄ 4 are not preloaded on this
promoter. Heat-induced binding of HSF to the pro-
moter in nucleosomes is assisted by Msn2 ⁄ 4 and the
chromatin remodelling complexes SWI ⁄ SNF, ISW1
and RSC [56,57]. These remodellers play partially
overlapping, but not redundant, function [57]. In con-
trast, the HSP82 promoter possesses a high-affinity
HSE, which constitutively binds HSF. The promoter
contains remodelled nucleosomes exhibiting DNase I
hypersensitivity, and the gene is transcribed at low
levels under physiological conditions [58,59]. Binding
of HSF to the HSP82 promoter has been suggested to
occur soon after DNA replication and before nucleo-
somes have assembled, in the S ⁄ G
2
phase of the cell
cycle [59], depending on ISW1 and RSC activities [57].
In response to heat shock, HSF occupancy at HSE-
containing promoters increases, the SAGA and
HSF–HSE interaction H. Sakurai and Y. Enoki
4144 FEBS Journal 277 (2010) 4140–4149 ª 2010 The Authors Journal compilation ª 2010 FEBS
SWI ⁄ SNF complexes are recruited to both the pro-
moter and coding regions, and histones are acetylated

gered by HSF-mediated recruitment of positive tran-
scription elongation factor-b (P-TEFb), which
phosphorylates the polymerase [62–64]. Concomitant
nucleosome loss at hsp70 requires poly(ADP)-ribose
polymerase (PARP), which is capable of binding nucleo-
somes and is important for puff formation [60]. The
possible roles of PARP in nucleosome loss are as fol-
lows, (a) PARP prebound to nucleosomes is released
from chromatin to reverse any repressive effects of the
chromatin structure, (b) PARP ADP-ribosylates
histones and thus destabilizes nucleosomes or (c)
ADP-ribose polymers generated by PARP, which look
much like a nucleic acid, bind to histones, facilitating
nucleosome dissociation [60].
In mammals
Similarly to Drosophila, the promoter region of mam-
malian HSP70 is hypersensitive to DNase I and
contains paused polymerase [62–64]. Although GAGA
factor-like DNA-binding activity has been reported,
the involvement of a mammalian GAGA factor-like
protein in polymerase pausing has not been docu-
mented [65]. Instead, the HSP70 promoter is bound by
HSF2 in mitotic cells, which prevents compaction at
the site by condensin and maintains the gene in a tran-
scription-competent state, thereby enabling robust acti-
vation by HSF1 if cells in the early G
1
phase are
exposed to a stressor [66]. The bookmarking function
of HSF2 is achieved by recruitment of protein phos-

sical heat shock genes (including HSP70), does not
bind SWI ⁄ SNF, suggesting the importance of the chro-
matin remodeller in HSF member-specific transcription
[41]. Histone acetylation at the HSP70 promoter
occurs under treatment with heat and arsenite; how-
ever, phosphorylation of histone H3 occurs as a result
of treatment with arsenite [72]. The arsenite-induced
phosphorylation of H3 and HSP70 transcription is
dependent on p38 mitogen-activated protein kinase
activation. However, it remains to be explored how
phosphorylation of H3 is involved in arsenite-induced,
but not in heat-induced, transcription by HSF1.
H. Sakurai and Y. Enoki HSF–HSE interaction
FEBS Journal 277 (2010) 4140–4149 ª 2010 The Authors Journal compilation ª 2010 FEBS 4145
During attenuation of RNA synthesis, the chaperone
HSP70 behaves as a corepressor of HSF1 in a nega-
tive-feedback loop and interacts with CoREST, a com-
ponent of a histone deacetylase complex containing
HDAC1 and HDAC2 [73]. CoREST binds to the
HSP70 promoter at low levels under physiological
conditions and suppresses basal expression.
Global transcriptional changes and
histone modifications in heat-shocked
mammalian cells
When cells are subjected to heat shock, transcription
of many mRNA genes is rapidly repressed. In contrast,
the levels of the noncoding RNAs (ncRNAs) – B2
RNA and Alu RNA – which are transcribed from
short interspersed elements (SINEs) by RNA polymer-
ase III, increase in mouse and human cells, respec-

is recruited to the promoters of estrogen-responsive
genes and participates in the repression of transcrip-
tion, an effect linked to metastasis [78]. Therefore,
HSF1 is a potent regulator of global histone acetyla-
tion ⁄ deacetylation in stressed and unstressed cells.
Conclusion
In the HSF trimer, binding of each DBD to a 5-bp
unit (nGAAn) is necessary to achieve a stable protein–
DNA interaction, because monomeric HSF binds to
the repeat unit with significantly less affinity than does
the trimer. In addition to the continuous repeat units,
three discontinuous units in the gap- and step-type
HSEs can be bound by HSFs. Efficient trimerization
of HSFs is important to establish interactions with the
gap- and step-type HSEs. The different types of HSEs
result in the induction, by yeast HSFs, of different lev-
els of gene expression and probably in distinguishing
target genes by mammalian HSFs. In response to
stress, yeast HSF bound to an HSE recruits the gen-
eral transcription factors and Pol II to the promoter,
while the target promoters of mammalian HSF1 con-
tain paused polymerase that switches to productive
elongation in response to activated HSF1. Chromatin
regulators that disrupt the nucleosome structure facili-
tate the binding of HSF, general transcription factors
and Pol II to the promoters, and subsequent RNA
synthesis by polymerase. In mammalian cells, HSF1
target promoters are also bound by HSF2 and HSF4
under physiological conditions, suggesting that these
factors play a positive role in the opening of the chro-

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H. Sakurai and Y. Enoki HSF–HSE interaction
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