Ectothermy and endothermy: evolutionary perspectives of thermoprotection by HSPs
Department of Biology, Technion-Israel Institute of Technology, Haifa 32000, Israel
* Author for correspondence (e-mail: zarad{at}tx.technion.ac.il)
Accepted 23 May 2005
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: HSP, ectothermy, endothermy, thermotolerance, heat shock, Gallus gallus domesticus
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() |
---|
Induced thermotolerance is generally referred to as the state at which
whole organisms and cultured cells are transiently more resistant to killing
by heat and other stressors, due to a short pretreatment at moderately
elevated ambient temperatures. This thermotolerance is well correlated with
the synthesis of heat shock proteins (HSPs;
Parsell and Lindquist, 1994).
Indeed, overexpression of HSPs extends life span and increases resistance to
stresses in ectotherms (Morrow et al.,
2004
). HSPs are evolutionary conserved polypeptides that function
as molecular chaperones to prevent and repair deleterious damages caused to
proteins by environmental and physiological stresses
(Georgopoulos and Welch, 1993
;
Parsell and Lindquist, 1993
;
Craig et al., 1994
). The
expression of HSPs is primarily regulated at the level of transcription by a
family of heat shock transcription factors (HSFs)
(Morimoto, 1998
). Four members
of the HSF gene family (HSF14) have been isolated and characterized in
vertebrates, two of which, HSF1 and HSF3, act as stress-responsive
transcriptional activators (Nakai,
1999
). In the absence of stress, HSF1 and HSF3 are mostly located
in the cytoplasm in an inactive state
(Nakai et al., 1995
;
Wu, 1995
;
Morimoto, 1998
). To induce
transcriptional activity of heat shock genes, HSF1 and HSF3 must acquire
DNA-binding activity, preceded by oligomerization to a trimeric state and
nuclear localization (Tanabe et al.,
1997
). Compared with the mammalian HSF1, avian HSF1 has a lower
potency of activating heat shock genes in cells subjected to heat stress
(Inouye et al., 2003
). It is
becoming clearer, however, that, similar to the mammalian HSF1, avian HSF1
also possesses thermoprotective traits, independent of induction of heat shock
genes (Nakai and Ishikawa,
2001
; Inouye et al.,
2003
; Izu et al.,
2004
).
Different models have been suggested as to the identity of the cellular
thermal sensor that triggers the HSP response. According to the classical
model, the accumulation of denatured proteins in the cytoplasm triggers the
synthesis of HSPs (Ananthan et al.,
1986). Other models raise the options of thermal sensation by the
ribosome, at the level of translation (Van
Bogelen and Neidhardt, 1990
) or based on the autophosphorylative
trait of the HSP70 family members (McCarty
and Walker, 1991
). Most tempting to adopt, however, is the
suggestion that thermal sensation occurs at the membrane level
(Vígh et al.,
1998
).
Our present study focuses on the relationship between the organism's thermal buffer capacity (i.e. ectothermy vs endothermy) and its heat shock response at the cellular and peripheral (non-cellular) levels. The peripheral level is the sum of physiological responses that involve feedback circuits that are involved in the control of body temperature.
We hypothesized that ectotherms and endotherms would differ in their heat shock responses as they possess different buffer capacities to deal with extreme ambient temperatures. We used ontogenetic development as an experimental model for the transition from ectothermy to endothermy and revealed the relationship between Tb regulation and the HSP response. We also compared, in real time, the in vivo heat shock response of genetically heat-resistant (desert strain), phenotypically heat-resistant (long-term induction of thermoresistance) and heat-sensitive fowls. We present a novel phenomenon of long-term induced thermotolerance. This embryonic induction of thermotolerance is expressed as increased HSP levels in the adult but does not confer improved survival upon heat stress. Finally, we metabolically labelled in vivo chicken embryos and postnatals (chicks) to reveal other cellular components that differentially participate in the heat shock response.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() |
---|
Two sets of postnatal heat shock experiments were carried out. In the first set, 1-day-old postnatals (N=3, in two independent experiments) of three chicken strains that differ in resistance to heat at maturity (Lohmann<Hy Line<Bedouin) were exposed to 42°C or 43°C for 28 h. In the second set, 16-day-old Leghorn postnatals (N=24) were exposed to 24 h at 40°C (see Long-term improvement of survival phenotypic thermoresistance). In each of the experiments, tissues were sampled for analyzing the expression of HSPs.
Protein extraction
For the purpose of protein extraction, dissected tissues (brain and liver)
were homogenized in ice-cold buffer containing 0.1 mol l1
NaCl, 20 mmol l1 Tris pH 7.4, 0.2 mmol l1
EDTA, 20% glycerol (v/v), 0.5 mmol l1 dithiothreitol (DTT),
15 µg ml1 leupeptin and 1 mmol l1
phenylmethylsulfonylfluoride (PMSF). Samples were centrifuged for 30 min
(4°C, 17 210 g; Sorvall RC-5B; rotor ss-34), and
supernatants were collected, frozen in liquid nitrogen and stored at
70°C. To extract protein from blood cells, blood samples were
washed once with ice-cold phosphate-buffered saline and centrifuged for 2 min
(4°C, 270 g; Sorvall RC-5B; rotor ss-34). The cells were
resuspended in ice-cold TMP buffer (containing 10 mmol l1
Tris pH 7.4, 1 mmol l1 EDTA, 5 mmol l1
MgCl2, 0.5 mmol l1 DTT, 15 µg
ml1 leupeptin and 1 mmol l1 PMSF) and were
frozen (liquid nitrogen) and thawed (37°C) in four cycles. Samples were
centrifuged for 30 min (4°C, 17 210 g; Sorvall RC-5B;
rotor ss-34), and supernatants were collected, frozen in liquid nitrogen and
stored at 70°C. Blood cell nuclear proteins were extracted as
previously described by Dyer and Herzog
(1995).
In vivo metabolic labelling
Protein labelling in chicken embryos was performed as described elsewhere
(Banerji et al., 1987), with
slight modifications. Briefly, three embryonated eggs (in two independent
experiments) were transferred on day 18 of incubation from 37°C to
42°C or 43°C for up to 8 h. At 2 h intervals, embryos were directly
injected subcutaneously with 200 µCi (7.4 MBq) of
[35S]methionine in 20 µl of PBS via a hole drilled
through the shell, using a syringe equipped with a 25 G bent needle. The hole
was then sealed with wax, and the eggs were incubated for 2.5 h at 37°C.
Control embryos were maintained at 37°C. One-day-old postnatals
(N=3, in two independent experiments) were transferred from 28°C
to 42°C or 43°C for up to 8 h in a controlled climate chamber. At 2 h
intervals, they were subcutaneously injected with 200 µCi (7.4 MBq) of
[35S]methionine in 20 µl of PBS, using a syringe adapted to a 25
G bent needle, then transferred back to 28°C for 2.5 h. Control postnatals
were maintained at 28°C. Labelled tissues of embryos and postnatals were
isolated, washed in PBS, homogenized, and the proteins separated by 10%
acrylamide gels. Gels were subjected to fluorography and exposed for
416 h.
Long-term induction of thermotolerance
Long-term induction of thermotolerance was achieved by exposing 6-day-old
Leghorn embryos (N=19) to a single thermal event, 6 h at 42°C
[relative humidity (RH)=50±5%], within a temperature-controlled room
(±0.3°C). We tested the induction of thermotolerance at maturity by
exposing adult chickens (5 months of age) to 40°C for 8 h during two
consecutive days.
Long-term improvement of survival phenotypic thermoresistance
Improvement of survival at maturity (phenotypic thermoresistance) was
achieved by exposing 16-day-old Leghorn postnatals (N=24) to a single
thermal event, 24 h at 40°C (RH=50±5%), within a
temperature-controlled room (±0.3°C). Phenotypic thermoresistance
was tested at maturity (5 months of age) by exposure for 8 h to 40°C
during two consecutive days.
Real-time, in vivo measurements of the heat shock response
Three different groups of mature chickens (N=3 in each group) that
differ in their resistance to heat were examined. The groups included
individuals of the genetic heat-sensitive Leghorn strain, the phenotypic
thermoresistant Leghorn strain (group 16d; see the previous section) and the
genetic heat-resistant Bedouin strain. Twenty hours prior to each experiment,
a polyethylene cannula (PE-50) was implanted in a wing vein of mature fowl
under local anaesthesia (2% Lidocaine HCl), and a 5 cm-long, custom-made
polyethylene cannula (PE-160) was implanted dorsal to the rectum and fastened
to the skin. Experiments were carried out within a temperature-controlled room
(±0.3°C). The birds had free access to food and water and could
freely move in their individual cages. Each experiment started at
08.0009.00 h at an ambient temperature of 24°C (RH=50±5%). A
copperconstantan thermocouple was introduced into the rectal cannula,
locked at a pre-determined depth of 5 cm andconnected to a digital thermometer
(±0.1°C). After 10 min, Tb stabilized
around 41°C, after which blood was remotely sampled through an extended
PE-50 tubing. Ta was then elevated to 38°C
(RH=50±5%). It took
20 min to reach this temperature. Body
temperature was monitored continuously and blood samples were taken at each
1°C increase in Tb up to 45°C (heating phase). At
this time, Ta was lowered back to 24°C and blood
samples taken at each 1°C decrease in Tb down to
41°C (recovery phase). After each blood sample, the cannula was flushed
with heparinized saline.
Fatty acid synthase identification mass spectrometry analysis
Protein extracts of brain and liver tissues of control and heat-exposed
embryos (N=3) and postnatals (N=3) were run on a 7%
acrylamide gel and stained with Coomassie blue. The stained protein bands, at
a molecular mass of 270 kDa, were cut from the gel with a clean razor
blade and the proteins were reduced with 10 mmol l1 DTT and
modified with 100 mmol l1 iodoacetamide in 10 mmol
l1 ammonium bicarbonate. The gel pieces were treated with
50% acetonitrile in 10 mmol l1 ammonium bicarbonate to
remove the stain, followed by drying the gel pieces. The dried gel pieces were
rehydrated with 10% acetonitrile in 10 mmol l1 ammonium
bicarbonate containing 0.005 µg µl1 trypsin, and then
incubated overnight at 37°C. The resulting peptides were recovered with
60% acetonitrile with 0.1% trifluoroacetate. The tryptic peptides were
resolved by reverse-phase high-performance liquid chromatography on
0.1x300-mm fused silica capillaries (J&W, Folsom, CA, USA; 100 µm
i.d.) home-filled with porous R2 (Persepective, Framingham, MA, USA). The
peptides were eluted using an 80-min linear gradient of 595%
acetonitrile with 0.1% acetic acid in water at a flow rate of
1 µl
min1. The liquid from the column was electrosprayed into an
ion-trap mass spectrometer (LCQ; Finnigan, San Jose, CA, USA). Mass
spectrometry was performed in the positive ion mode using repetitively full MS
scan followed by collision induced dissociation (CID) of the most dominant ion
selected from the first MS scan. The mass spectrometry data were compared to
simulated proteolysis and CID of the proteins in the NR-NCBI database using
the Sequest software (J. Eng and J. Yates, University of Washington and
Finnigan, San Jose, CA, USA). The amino terminal of the protein was sequenced
on a Peptide Sequencer 494A [Perkin Elmer, (Applied Biosystems), Foster City,
CA, USA] according to the manufacturer's instructions.
SDSPAGE and western blot
Whole-cell and tissue lysates were boiled in sample application buffer
containing 2-mercaptoethanol. Proteins were separated by
SDSpolyacrylamide gel (10%) and transferred onto nitrocellulose
membrane (Schleicher & Schuell Gmbh, Dassel, Germany). The membranes were
probed with monoclonal anti-actin, anti-HSP70 (recognizing the constitutive
and the inducible forms of the protein; Sigma H5147) and anti-HSP90 (Sigma
H1775) antibodies or polyclonal anti-HSF1 and anti-HSF3 (a generous gift from
Dr A. Nakai), followed by appropriate secondary antibodies. The proteins were
visualized by enhanced chemiluminescence.
RNA isolation and northern blot
Total RNA was isolated from blood cells by TRI REAGENT-BD (MRC, Cincinnati,
OH, USA) according to the manufacturer's instructions. RNA (5 µg) was
separated in formaldehydeagarose gel and transferred onto nylon
membrane (Zeta-Probe; Bio-Rad, Hercules, CA, USA). Chicken HSP70 cDNA (a kind
gift from Dr R. Morimoto) was labelled by the extension priming method using
[-32P]dATP. Membrane was hybridized for 16 h at 55°C,
washed with 0.1% SDS in 1x SSC at 45°C, 50°C and 55°C and
exposed to X-ray film (Kodak BioMax MS) at 70°C in the presence of
an intensifying screen.
Electromobility shift assay (EMSA)
Electromobility shift assay was performed as previously described
(Mosser et al., 1988).
Briefly, equal amounts of cellular proteins (20 µg for brain extraction and
5 µg for blood nuclei proteins) were incubated with a
32P-labelled double-stranded oligonucleotide
(5'-CTAGAAGCTTCTAGAAGCTTCTAG-3'). The protein-bound and free
oligonucleotides were electrophoretically separated by 4% native
polyacrylamide gels. The gels were dried and autoradiographed.
Statistical analysis
Differences between means (survival time of control and experimental groups
in the case of long-term induction of thermotolerance) as well as densitometry
of bands were verified by unpaired t-test. The other parameters
(hatchability of embryos from different strains) were subjected to Tukey's
post-hoc analysis of variance (ANOVA). A value of P<0.05
was accepted as significant.
![]() |
Results and discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
|
Remarkably, the peaks of thermosensitivity and thermoresistance during
ontogeny were only 34 days apart; indeed, postnatals proved to be the
most heat-resistant stage in the chicken's life cycle and, even after a 24 h
exposure to 4243°C, manifested only a small, though significant,
increase in Tb, safely below the hyperthermal zone (data
not shown). This slight increase in Tb was not accompanied
by an HSP response. Nevertheless, the unique constitutive DNA-binding state of
HSF (as seen in controls) was released at the end of the heat shock period
(Fig. 3A). The heat shock
response in avian cells is mediated by two transcription factors, HSF1 and
HSF3, interacting with the heat shock consensus element (HSE) at the promoter
of the heat shock genes (Nakai et al.,
1995). The release of the HSE-bound HSF in the heat-shocked
postnatals, however, did not result from decreased levels of either HSF
[P=0.11 and P=0.4 (ns) for HSF1 and HSF3, respectively;
Fig. 3B]. It has been suggested
that, upon heat exposure, HSF also regulates the activity of non-heat shock
genes (Westwood et al., 1991
).
Most striking, activated HSF1 negatively regulates the expression of febrile
response mediators (Housby et al.,
1999
; Xiao et al.,
1999
). Logically, the products of such genes should be
downregulated in heat-exposed organisms. We therefore suggest that part of the
overall physiological mechanism of thermoregulation under elevated
temperatures in postnatals is attained, at the cellular level, through a
switch from positively regulating heat shock genes by HSF to a positive and
negative mode of regulation of other genes. This switch may consequently
explain the unchanged protein levels of HSP70 and HSP90 [P=0.32 and
P=0.25 (ns), for HSP70 and HSP90, respectively] in response to heat
exposure (Fig. 3C), which held
for up to 25 days of age. Metabolic labelling of 1-day-old postnatals
confirmed that there was no net increase of newly synthesized HSPs during 8 h
of heat exposure (Fig. 3D).
Therefore, these results strongly support our suggestion that, under identical
heat shock conditions, the HSP system in postnatals, in contrast to embryos,
may play only a minor role in thermoprotection.
|
Acquired thermotolerance and survival in endotherms are not linked
Adaptation to elevated ambient temperatures may be divided into
thermotolerance and heat acclimatization. Whereas thermotolerance refers to
cellular adaptation via a prerequisite accumulation of HSPs,
acclimatization is determined by the organism's ability to maintain thermal
equilibrium in the heat (Moseley,
1997). Acquired thermotolerance has been implicated in increased
resistance to killing caused by extreme heat exposure in many ectotherms and
in cell cultures of endothermic organisms
(Feder and Hofmann, 1999
).
Here, we address the relationship between HSP accumulation and survival in
endotherms, at the whole organism level. We approached this issue by a
long-term induction of thermotolerance through embryonic conditioning and by a
long-term improvement of survival through postnatal conditioning. Our findings
show that embryonically conditioned individuals can acquire thermotolerance at
maturity, as expressed by improvement of their HSP response (unpaired
t-test, P<0.05; Fig.
4). Since survival time did not differ significantly among control
and embryonically conditioned groups (unpaired t-test,
P=0.34; Fig. 4,
bottom), this acquired thermotolerance is not correlated with improvement of
survival. Alternatively, survival of mature individuals from a heat-sensitive
strain was significantly improved as a result of a single postnatal heat
exposure (16-day-old Leghorn group). This type of `phenotypic adaptation'
(acclimatization) is characterized by a delayed HSP response
(Fig. 5BD) and is
distinct from the typical acquired thermotolerance because of its different
time course and duration (more than 5 months, compared with a few hours or
days for typical acquired thermotolerance). Altogether, these findings
indicate that, at least in endothermic birds, at the whole organism level,
survival does not depend on a prerequisite accumulation of HSPs.
|
|
Thermoresistance in endotherms is characterized by improvement of Tb regulation and by a delayed HSP response
How is the heat shock response reflected in various states of
thermoresistance in endothermy, and what accounts for improved
thermoresistance of endotherms if not HSPs? To gain insight into these issues,
we monitored in real time the in vivo heat shock response within the
same individuals of mature fowl of various thermal histories: control Leghorns
(heat sensitive), 16-day-old Leghorns (phenotypically adapted) and the Bedouin
fowl (genetically resistant). Within the Leghorn line, the two groups
represent identical genotypes but different states of phenotypic
thermoresistance. The intraspecific variation (Leghorn vs Bedouin)
represents a genetic difference. Our previous comparisons of the commercial
egg-layer Leghorn chicken and the desert-origin, genetically heat-resistant
Bedouin fowl identified various thermoregulatory mechanisms that contribute to
the superiority of the Bedouin fowl with respect to heat resistance
(Arad, 1983;
Arad and Marder, 1982
;
Marder et al., 1974
). Thus, we
hypothesized that the cellular heat shock response would also differ among
nonresistant, phenotypically and genetically heat-resistant fowl. A distinct
pattern of Tb regulation and HSP response was revealed for
each group. In general, the Bedouin fowl was superior to the heat-sensitive
Leghorn in its lower heating rate and in its higher cooling rate
(Fig. 5A) and was characterized
by a considerably delayed HSP response, both in relation to time scale and to
Tb level (Fig.
5BD). The 16-day-old Leghorn group revealed intermediate,
significantly different patterns (Fig.
5AD). These novel findings are of evolutionary
significance, since they suggest that fowl's HSP responses, unlike in
ectotherms (Krebs and Feder,
1997
; Michalak et al.,
2001
; Ul'masov et al.,
1992
), do not contribute to the genetic variations of heat shock
tolerance, but rather it is the effectiveness of the homeostatic mechanisms
for Tb regulation.
Fatty acid synthase is upregulated in postnatals in response to heat shock
In search of a cellular component other than HSPs that may participate in
the thermoprotective process in endotherms, we performed in vivo
metabolic labelling followed by mass spectrometry analysis of heat-shocked
embryos and postnatals. A dramatic increase (P<0.05) in the
expression of fatty acid synthase (FAS) was revealed in postnatals, but not in
embryos, in response to heat shock (Fig.
6). Abrupt elevation of temperature affects the cell membrane
physical state by increasing its fluidity
(Dynlacht and Fox, 1992; Mejia
et al., 1995; Vígh et al.,
1998
). However, cells may compensate for thermal disturbances
through physiological and biochemical mechanisms that allow them to maintain
homeostatic equilibrium. One such mechanism, termed homeoviscous adaptation,
allows cells to regulate membrane fluidity by adjustment of its lipid
composition (Carratù et al.,
1996
; Vígh et al.,
1998
). Upon exposure to low temperature, a reduction in the
membrane fluidity triggers an increase in the expression of desA, a desaturase
that subsequently leads to the desaturation of membrane lipids
(Vígh et al., 1993
). At
high temperature, it has been demonstrated that HSP17 transcription was
strongly regulated by subtle changes in membrane physical order
(Horváth et al., 1998
;
Lee et al., 2000
). HSP17 has
been further shown to have a dual role as a `membrane stabilizing factor' and
as a member of a multi-chaperon protein folding network
(Török et al.,
2001
). However, no causal link has been proposed, upon exposure to
elevated temperature, between compensative factors regulating membrane
fluidity, cellular thermoprotection and the expression of HSPs. The current
study suggests that FAS may play a role in this regulation as it catalyses the
synthesis of saturated long-chain fatty acids from acetyl CoA, malonyl CoA and
NADPH. Based on our findings, and supported by the findings of Horváth
et al. (1998
), who reported a
causal relationship between the membrane physical state and the threshold
temperature for activation of heat shock genes, we suggest a possible role for
FAS in modulating the cellular heat shock response in endotherms. Accordingly,
increasing levels of this enzyme in response to elevated temperatures may
contribute to rigidifying the membrane and thereby raising the threshold
temperature for synthesis of HSPs. This suggestion may serve as a foundation
for future studies.
|
Conclusions
Our study shows that, despite the likely contribution of HSPs to the
expansion of the cellular thermal safety margins in endothermic birds, HSPs do
not improve their thermal resistance and thus do not constitute a first-line
thermal defense mechanism. The ectothermic state, however, is strikingly
different. Here, the increased levels of HSPs precede and buffer the
deleterious effect of heat on embryo hatchability, suggesting a tight
correlation between HSPs and survival. This ectothermy-to-endothermy
transition concept is supported by findings that ectothermic species that live
in widely fluctuating thermal habitats possess a stronger HSP protective trait
compared with ectotherms that inhabit stable thermal niches and lack or have a
weaker HSP response (Bosch et al.,
1988; Hofmann et al.,
2000
; Sanders et al.,
1991
).
The distinct evolutionary adaptations of the Bedouin fowl
(Arad, 1983;
Arad and Marder, 1982
;
Marder et al., 1974
) were
clearly revealed in the kinetics of the heat shock response in the present
study, even after 9 years of maintenance in captivity under non-desert
conditions. At the cellular level, these genetically inherited traits could
result from the establishment of different thresholds for induction of HSPs:
slightly different biochemical properties of HSF
(Feder and Hofmann, 1999
),
different cellular environments (Clos et
al., 1993
), autoregulatory processes
(Morimoto, 1998
), variations
in thermal stability of cellular proteins
(Somero, 1995
) and different
membrane characteristics (Vígh et
al., 1998
; present study). At the peripheral level, the different
time course of the heat shock response
(Fig. 5A) could reflect
distinct capacities of the homeostatic mechanisms
(Arad, 1983
).
Based on our findings, such intraspecific variations are likely to occur also upon ontogenetic transition from ectothermy to endothermy. We thus suggest that the ontogenetic and the intraspecific evolutionary pathways of thermoresistance in fowl may have followed two, apparently non-related, parallel routes: first, a cellular route, in which the acquisition of thermoresistance is not HSP-dependent and could result from altered mechanisms of thermal sensation; second, a peripheral route, characterized by altered homeostatic mechanisms that lead to differential patterns of Tb regulation.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() |
---|
Ananthan, J., Goldberg, A. L. and Voellmy, R. (1986). Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science 232,522 -524.[Medline]
Arad, Z. (1983). Thermoregulation and acid-base
status in the panting dehydrated fowl. J. Appl.
Physiol. 54,234
-243.
Arad, Z. and Marder, J. (1982). Strain differences in heat resistance to acute heat stress between the Bedouin desert fowl, the White Leghorn and their crossbreeds. Comp. Biochem. Physiol. A 72,191 -193.[CrossRef]
Banerji, S. S., Laing, K. and Morimoto, R. I. (1987). Erythroyid lineage-specific expression and inducibility of the major heat shock protein HSP70 during avian embryogenesis. Genes Dev. 1,946 -953.[Abstract]
Bosch, T. C. G., Krylow, S. M., Bode, H. R. and Steele, R.
E. (1988). Thermotolerance and synthesis of heat shock
proteins: these responses are present in Hydra attenuata but absent
in Hydra oligactis. Proc. Natl. Acad. Sci. USA
85,7927
-7931.
Carratù, L., Franceschelli, S., Pardini, C. L.,
Kobayashi, G. S., Horváth, I., Vígh, L. and Maresca,
B. (1996). Membrane lipid perturbation modifies the set point
of the temperature of heat shock response in yeast. Proc. Natl.
Acad. Sci. USA 93,3870
-3875.
Clos, J., Rabindran, S., Wisniewski, J. and Wu, C. (1993). Induction temperature of human heat shock factor is reprogrammed in a Drosophila cell environment. Nature 364,252 -255.[CrossRef][Medline]
Craig, E. A., Weissman, J. S. and Horwich, A. L. (1994). Heat shock proteins and molecular chaperones: mediators of protein conformation and turnover in the cell. Cell 78,365 -372.[CrossRef][Medline]
Dyer, R. B. and Herzog, N. K. (1995). Isolation of intact nuclei for nuclear extract preparation from a fragile B-lymphocyte cell line. Biotechniques 19,192 -195.[Medline]
Dynlacht, J. R. and Fox, M. H. (1992). The effect of 45 degrees C hyperthermia on the membrane fluidity of cells of several lines. Radiat. Res. 130, 55-60.[Medline]
Feder, M. E. and Hofmann, G. E. (1999). Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61,243 -282.[CrossRef][Medline]
Georgopoulos, C. and Welch, W. J. (1993). Role of the major heat shock proteins as molecular chaperones. Annu. Rev. Cell. Biol. 9,601 -634.[CrossRef][Medline]
Hofmann, G. E., Buckley, B. A., Airaksinen, S., Keen, J. E. and
Somero, G. N. (2000). Heat shock protein expression is
absent in the Antarctic fish Trematomus bernacchii (Family
Nototheniidae). J. Exp. Biol.
203,2331
-2339.
Hohtola, E. and Visser, G. H. (1998). Development of locomotion and endothermy in altricial and precocial birds. In Avian Growth and Development, Evolution within the Altricial-Precocial Spectrum (ed. J. M. Strack and R. E. Ricklefs), pp. 157-173. Oxford: Oxford University Press.
Horváth, I., Glatz, A., Varvasovszki, V.,
Török, Z., Páli, T., Balogh, G., Kovács, E.,
Nádasdi, L., Benkö, S., Joó, F. et al.
(1998). Membrane physical state controls the signaling mechanism
of the heat shock response in Synechocystis PCC 6803, identification of
hsp17 as a "fluidity gene". Proc. Natl. Acad. Sci.
USA 95,3513
-3518.
Housby, J. N., Cahill, C. M., Chu, B., Prevelige, R., Bickford, K., Stevenson, M. A. and Calderwood, S. K. (1999). Non-steroidal anti-inflammatory drugs inhibit the expression of cytokines and induce HSP70 in human monocytes. Cytokine 11,347 -358.[CrossRef][Medline]
Huey, R. B., Carlson, M., Crozier, L., Frazier, M., Hamilton, H., Harley, C., Hoang, A. and Kingsolver, J. G. (2002). Plants versus animals: do they deal with stress in different ways? Integ. Comp. Biol. 42,415 -423.
Inouye, S., Katsuki, K., Izu, H., Fujimoto, M., Sugahara, K.,
Yamada, S., Shinkai, Y., Oka, Y., Katoh, Y. and Nakai, A.
(2003). Activation of heat shock genes is not necessary for
protection by heat shock transcription factor 1 against cell death due to a
single exposure to high temperatures. Mol. Cell Biol.
23,5882
-5895.
Izu, H., Inouye, S., Fujimoto, M., Shiraishi, K., Naito, K. and
Nakai, A. (2004). Heat shock transcription factor 1 is
involved in quality-control mechanisms in male germ cells. Biol.
Reprod. 70,18
-24.
Krebs, R. A. and Feder, M. E. (1997). Natural variation in the expression of the heat shock protein HSP70 in a population of Drosophila melanogaster, and its correlation with tolerance of ecologically relevant thermal stress. Evolution 51,173 -179.
Lee, S., Owen, H. A., Prochaska, D. J. and Barnum, S. R. (2000). HSP16.6 is involved in the development of thermotolerance and thylakoid stability in the unicellular cyanobacterium, Synechocystis sp. PCC 6803. Curr. Microbiol. 40,283 -287.[CrossRef][Medline]
Marder, J., Arad, Z. and Gafni, M. (1974). The effect of high ambient temperatures on acid-base balance of the panting Bedouin fowl (Gallus domesticus). Physiol. Zool. 47,180 -189.
McCarty, J. S. and Walker, G. C. (1991). DnaK
as a thermometer: threonine-199 is site of autophosphorylation and is critical
for ATPase activity. Proc. Natl. Acad. Sci. USA
88,9513
-9517.
Mejia, R., Gomez-Eichelmann, M. C. and Fernandez, M. S. (1992). Membrane fluidity of Escherichia coli during heat-shock. Biochim. Biophys. Acta. 1239,195 -200.
Michalak, P., Minkov, I., Helin, A., Lerman, D. N., Bettencourt, B. R., Feder, M. E., Korol, A. B. and Nevo, E. (2001). Genetic evidence for adaptation-driven incipient speciation of Drosophila melanogaster along a microclimatic contrast in "Evolution Canyon", Israel. Proc. Natl. Acad. Sci. USA 23,13195 -13200.[CrossRef]
Morimoto, R. I. (1998). Regulation of the heat
shock transcriptional response: cross talk between a family of heat shock
factors, molecular chaperones, and negative regulators. Genes
Dev. 12,3788
-3796.
Morimoto, R. I., Tissiers, A. and Georgopoulos, C. (1990). The stress response, function of the proteins and perspectives. In Stress Proteins in Biology and Medicine (ed. R. I. Morimoto, A. Tissieres and C. Georgopoulos), pp. 1-36. New York: Cold Spring Harbor Laboratory Press.
Morrow, G., Samson, M., Michaud, S. and Tanguay, R. M.
(2004). Overexpression of the small mitochondrial Hsp22 extends
Drosophila life span and increases resistance to oxidative stress.
FASEB J. 18,598
-599.
Moseley, P. L. (1997). Heat shock proteins and
heat adaptation of the whole organism. J. Appl.
Physiol. 83,1413
-1417.
Mosser, D. D., Theodorakis, N. G. and Morimoto, R. I. (1988). Coordinate changes in heat shock element-binding activity and HSP70 gene transcription rates in human cells. Mol. Cell. Biol. 8,4736 -4744.[Medline]
Nakai, A. (1999). New aspects in the vertebrate heat shock factor system: HSF3 and HSF4. Cell Stress Chaperones 4,86 -93.[CrossRef][Medline]
Nakai, A and Ishikawa, T. (2001). Cell cycle
transition under stress conditions controlled by vertebrate heat shock
factors. EMBO J. 20,2885
-2895.
Nakai, A., Kawazoe, Y., Tanabe, M. and Morimoto, R. I. (1995). The DNA-binding properties of two heat shock factors, HSF1 and HSF3, are induced in the avian erythroblast cell line HD6. Mol. Cell. Biol. 15,5268 -5278.[Abstract]
Parsell, D. A. and Lindquist, S. (1993). The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu. Rev. Genet. 27,437 -496.[CrossRef][Medline]
Parsell, D. A. and Lindquist, S. (1994). Heat shock proteins and stress tolerance. In The Biology of Heat Shock Proteins and Molecular Chaperone (ed. R. I. Morimoto, A. Tissieres and C. Georgopoulos), pp. 457-494. New York: Cold Spring Harbor Laboratory Press.
Sanders, B. M., Hope, C., Pascoe, V. M. and Martin, L. S. (1991). Characterization of the stress protein response in two species of Collisell limpets with different temperature tolerances. Physiol. Zool. 64,1471 -1489.
Somero, G. N. (1995). Proteins and temperature. Annu. Rev. Physiol. 57,43 -68.[CrossRef][Medline]
Tanabe, M., Nakai, A., Kawazoe, Y. and Nagata, K.
(1997). Different thresholds in the responses of two heat shock
transcription factors, HSF1 and HSF3. J. Biol. Chem.
272,15389
-15395.
Török, Z., Goloubinoff, P., Horváth, I.,
Tsvetkova, N. M., Glatz, A., Balogh, G., Varvasovszki, V., Los, D. A.,
Vierling, E. Crowe, J. H. et al. (2001).
Synechocystis HSP17 is an amphitropic protein that stabilizes
heat-stressed membranes and binds denatured proteins for subsequent
chaperone-mediated refolding. Proc. Natl. Acad. Sci.
USA 98,3098
-3103.
Ul'masov, K. A., Shammakov, S., Karaev, K. and Evgen'ev, M.
B. (1992). Heat shock proteins and thermoresistance in
lizards. Proc. Natl. Acad. Sci. USA
89,1666
-1670.
Van Bogelen, R. A. and Neidhardt, F. C. (1990).
Ribosomes as sensors of heat and cold shock in Escherichia coli.Proc. Natl. Acad. Sci. USA
87,5589
-5593.
Vígh, L., Los, D. A., Horváth, I. and Murata,
N. (1993). The primary signal in the biological perception of
temperature: Pd-catalyzed hydrogenation of membrane lipids stimulated the
expression of the desA gene in Synechocystis PCC6803.
Proc. Natl. Acad. Sci. USA
90,9090
-9094.
Vígh, L., Maresca, B. and Harwood, J. L. (1998). Does the membrane's physical state control the expression of heat shock and other genes? Trends Biochem. Sci. 23,369 -374.[CrossRef][Medline]
Westwood, J. T., Clos, J. and Wu, C. (1991). Stress-induced oligomerization and chromosomal relocalization of heat-shock factor. Nature 353,822 -827.[CrossRef][Medline]
Wu, C. (1995). Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 11,441 -469.[CrossRef][Medline]
Xiao, X. Z., Zuo, X. X., Davis, A. A., McMillan, D. R., Curry,
B. B., Richardson, J. A. and Benjamin, I. J. (1999).
HSF1 is required for extra-embryonic development, postnatal growth and
protection during inflammatory responses in mice. EMBO
J. 18,5943
-5952.