Adaptive thermogenesis in hummingbirds
1 Department of Physiology, Biosciences Institute, University of São
Paulo, SP, Brazil
2 Thyroid Division, Department of Medicine, Brigham & Women's Hospital
and Harvard Medical School, Boston, MA 02115, USA
3 Division of Endocrinology, Department of Medicine, Beth Israel Deaconess
Medical Center and Harvard Medical School, Boston, MA 02115, USA
* Present address: Departmento de Fisiologia, Instituto de Biociências,
Universidade de São Paulo, 05508-900 São Paulo, SP, Brazil
(e-mail: jebicudo{at}usp.br )
Accepted 13 May 2002
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Summary |
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Key words: non-shivering thermogenesis, brown adipose tissue, Ca2+-ATPase, uncoupling protein, bird, hummingbird
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Introduction |
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Factors affecting adaptive thermogenesis |
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Cold-induced metabolic scope has been examined in a few studies and has
been shown to range from three to eight times SMR in birds
(Withers, 1977;
Prinzinger and Siedle, 1988
;
Brigham, 1992
;
Maddocks and Geiser, 1997
).
Metabolic scope during flight can range from five to ten times SMR, thus
exceeding the maximum metabolic rate elicited by cold exposure
(Brackenbury, 1984
;
Marsh and Dawson, 1989
). The
extraordinary demands of flight in birds have resulted in selection for muscle
fiber types with high rates of substrate utilization and may predispose the
use of these muscles in birds as thermogenic organs
(Block, 1994
).
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Non-shivering thermogenesis |
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Torpid and hibernating placental mammals rely mostly on NST in brown
adipose tissue for rewarming (Smith and
Horwitz, 1969). Brown adipose tissue is specialized for heat
production as a result of the expression of uncoupling protein 1 (UCP1), a
physiological mitochondrial uncoupler
(Klingenberg and Huang, 1999
).
This protein dissipates the H+ gradient formed across the inner
mitochondrial membrane, preventing both the passage of H+ through
the F1Fo-ATP synthase and the synthesis of ATP from ADP
and inorganic phosphate (Pi). As a result, oxidative metabolism is
activated, leading to an increase in the rate of heat production
(Nicholls and Locke, 1984
).
Shivering, however, has been considered to be the primary thermogenic
mechanism during rewarming in torpid birds or during cold stress
(West, 1965
;
Dawson, 1975
;
Block, 1994
). The capacity for
NST has been more carefully investigated in birds over the past few years, and
there is now good evidence that it occurs in this group, although it may be
limited to a few species. The literature reports data accumulated for a
relatively restricted group of birds, but this phenomenon might well be more
widespread than previously thought (Bicudo
et al., 2001
).
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Thermogenic mechanisms in birds |
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Ca2+-ATPase and ryanodine-receptor content increase in the
sarcoplasmic reticulum during cold acclimation in birds
(Dumonteil et al., 1995),
raising the possibility that Ca2+ cycling in bird skeletal muscle
could also contribute to adaptive thermogenesis, including NST. Within this
context, hummingbirds appear to be a good model system for investigating NST
among birds. They possess one of the highest mass-specific metabolic rates
recorded among vertebrates, requiring an abundant supply of oxygen and energy
substrates (Suarez et al.,
1986
). Their limited amount of adipose tissue impairs the
maintenance of euthermic metabolic rate under conditions of food deprivation.
To circumvent this, hummingbirds enter torpor on a daily basis to conserve
energy and survive throughout the night
(Pearson, 1950
;
Lasiewsky, 1963
;
Calder, 1994
;
Bicudo, 1996
).
The cellular and molecular mechanisms underlying the rewarming process in
hummingbirds are still not entirely understood. Occupying between 25 and 30 %
of body mass, the pectoral muscle of hummingbirds, with a mitochondrial volume
density of 25-30 %, is the natural candidate for heat generation in this avian
group. The same kind of argument might also hold for adult humans, which,
unlike rodents, do not have large, distinct depots of brown adipose tissue.
Skeletal muscle, in contrast, constitutes up to 40 % of total body mass in
humans and has a significant volume density of mitochondria, prompting several
investigators to assume that it is the logical tissue in which to study
adaptive thermogenesis. The mechanisms involved are not completely understood
but could include effects on mitochondrial function and uncoupling,
Ca2+ cycling or both (Lowell
and Spiegelman, 2000).
During Ca2+ transport, the chemical energy derived from ATP
hydrolysis is used by the Ca2+-ATPase to pump Ca2+ into
the sarcoplasmic reticulum, and chemical energy is converted into osmotic
energy during this process. After accumulation of Ca2+ within the
sarcoplasmic reticulum, the Ca2+ gradient formed across the
membrane promotes the reversal of the catalytic cycle of the enzyme. During
this reversal, some of the chemi-osmotic energy is either used to resynthesise
some of the ATP previously cleaved
(Makinose and Hasselbach,
1971) or dissipated into the surrounding medium as heat
(Block, 1994
). Ca2+
leaves the sarcoplasmic reticulum through the action of the
Ca2+-ATPase both during ATP synthesis from ADP and Pi
and during heat production (de Meis,
1998
).
An increase in the rate of Ca2+ uptake does not necessarily
indicate an augmentation of the Ca2+-ATPase activity. It simply
represents the net accumulation of Ca2+ in the lumen of the
sarcoplasmic reticulum: the product of a dynamic equilibrium between what is
released and taken up by the sarcoplasmic reticulum as a whole.
Ca2+-ATPase itself participates in the uptake of Ca2+ as
well as in its release, and in both processes the conversion of different
forms of energy into heat may occur. According to de Meis et al.
(1997), with the release of
Ca2+ mediated by the Ca2+-ATPase, the accumulated energy
derived from the Ca2+ electrochemical gradient may be converted
into heat, i.e. in this case, Ca2+ transport is uncoupled from ATP
synthesis.
During non-shivering thermogenesis, most of the heat is derived from
resting muscle, but the mechanism of heat production remains unclear. It has
been proposed that Ca2+ leaks from the sarcoplasmic reticulum, and
heat would therefore be derived from the hydrolysis of the extra ATP needed to
maintain a low myoplasmic Ca2+ concentration
(Block, 1994). In this
situation, it is assumed that the amount of heat produced during the
hydrolysis of an ATP molecule is always the same and is not modified by the
formation of the Ca2+ gradient, as if the energy released by the
ATP hydrolysis were divided into two independent packets, one to be converted
into heat and the other to be used for Ca2+ transport
(Landeria-Fernandez et al.,
2000
). More recently, microcalorimetric measurements of ATP
hydrolysis have shown that, in the presence of a Ca2+ gradient, the
heat produced during the hydrolysis of each ATP molecule is 2-3 times greater
than that measured in sarcoplasmic reticulum vesicles in the absence of a
Ca2+ gradient (de Meis,
1998
). These results indicate that the Ca2+-ATPase
isoform found in vertebrate skeletal muscle is able to convert osmotic energy
into heat.
Experiments using sarcoplasmic reticulum vesicles from hummingbird
(Eupetomena macroura) pectoral muscle have shown that the ratio
between rates of ATP hydrolysis and ATP synthesis, with the release of
Ca2+ mediated by the Ca2+-ATPase, is twice that in
rabbit skeletal muscle sarcoplasmic reticulum
(Vianna et al., 1999),
suggesting that, in the presence of a Ca2+ gradient, at least
theoretically, twice as much energy is being converted into heat in
hummingbird pectoral muscle as in rabbit skeletal muscle. Thus, during arousal
from torpor, rewarming of the hummingbird body could also take place through
NST, an alternative source of heat derived from the hydrolysis of ATP by the
sarcoplasmic reticulum Ca2+-ATPase of its pectoral muscle fibers.
This mechanism might contribute to some energy conservation during arousal,
particularly when energy storage is low before entering into torpor.
Uncoupling protein homologs
Although uncoupling protein 1 (UCP1) occurs exclusively in brown adipose
tissue, a large array of similar uncoupling proteins was recently found in
various tissues of mice; e.g. UCP2, which is expressed ubiquitously
(Fleury et al., 1997), and
UCP3, which is expressed primarily in skeletal muscle
(Boss et al., 1997
). When
expressed in yeast mitochondria or reconstituted into liposomes, both UCP2 and
UCP3 catalyze H+ flux (Jaburek
et al., 1999
). The physiological role of these newly described
uncoupling proteins is controversial and not yet defined, particularly because
they have been found in tissues whose primary function is not thermogenic,
e.g. spleen, kidney and brain. Given, however, the apparent widespread
distribution of uncoupling proteins among eukaryotes and the lack of brown
adipose tissue in birds, hummingbirds again become an interesting model system
in which to test the hypothesis that body heat might also be generated in
birds through the mediation of an uncoupling protein.
Raimbault et al. (2001)
have recently cloned an uncoupling protein homolog (avUCP) from chicken
(Gallus gallus) skeletal muscle, and they suggest that this avUCP may
be involved in facultative muscle thermogenesis. They claim, however, that it
was not possible to obtain functional data, and the uncoupling activity of
avUCP could not therefore be demonstrated. However, the unique expression of
this protein in skeletal muscle of chicken, and its upregulation after
cold-acclimation in ducklings or following treatment with glucagon, inducing
muscle NST or in association with diet-induced thermogenesis, support,
according to these authors, a role for avUCP in energy expenditure in
birds.
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Hummingbird uncoupling protein homolog |
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HmUCP was expressed in Saccharomyces cerevisiae and used in
functional studies. A pYES2 plasmid containing the 12CA5 epitope-tagged HmUCP
was used to transform yeast cells. The western blot revealed a single protein
of approximately 34kDa, compatible with the predicted molecular mass, in the
enriched mitochondria fraction. In these cells, transiently expressed HmUCP
decreased the 3',3-dihexyl-oxacarbocyanine iodide (DiOC6)
uptake as measured by flow cytometry by a similar degree as did rat UCP1,
demonstrating that HmUCP is capable of lowering the mitochondrial membrane
potential (Fig. 2). The
analysis of HmUCP mRNA expression in various tissues indicated a high level of
expression in the pectoral muscle. Heart and liver both show slightly lower
levels of expressions, followed by lung and kidneys. Brain was the only tissue
tested in which HmUCP mRNA was not detected
(Vianna et al., 2001).
|
Vianna et al. (2001) also
tested whether HmUCP mRNA levels change under various physiological
conditions. Hummingbirds were studied in conditions of euthermy, torpor and
rewarming. At each phase, various tissues were processed for northern
blotting. A typical profile of the rate of oxygen consumption by a E.
macroura for these phases is shown in
Fig. 3A.
|
Northern blot analysis indicated that, in pectoral muscle and heart, HmUCP
mRNA levels changed significantly during the torpor/rewarming process.
Accordingly, the heart of torpid animals showed an approximately 3.4-fold
increase in HmUCP mRNA levels compared with euthermic animals. During the
rewarming phase, the induction of the HmUCP mRNA levels was only 2.2-fold
compared with euthermic animals. In the pectoral muscle, a tissue that has
fivefold higher levels of HmUCP mRNA than heart, similar, although less
marked, changes were detected. It is interesting, however, that both heart and
pectoral muscle exhibited their highest levels of HmUCP during torpor. These
characteristics show remarkable similarity to the ground squirrel, a
hibernating mammal in which UCP2 and UCP3 mRNA levels are also maximal during
hibernation (Boyer et al.,
1998). Unique to the hummingbird, however, was the approximately
3.4-fold upregulation of HmUCP in the heart. The high level of expression of
HmUCP in the heart differs from placental mammals and, given the relatively
large size of the heart of hummingbirds (2.0-2.4% compared with approximately
0.6% of body mass in mammals), its presence might have physiological
relevance. Heart rates recorded for hummingbirds are of the order of 1250
beats min-1 (Lasiewski,
1964
), which is among the highest heart rates recorded for
endotherms. It is conceivable that the high workload and rate of ATP turnover
observed in the hummingbird's heart might be associated with elevated HmUCP
mRNA levels.
An additional feature that contrasts HmUCP with UCPs of placental mammals
is the high level of expression in liver, at levels similar to those in the
heart. In placental mammals, this is not the case. UCP2 expression is
restricted to Kupffer cells (Larrouy et
al., 1997) and occurs only in hepatocytes of mice with fatty liver
(Cortez-Pinto et al., 1999
).
Hummingbird hepatocytes contain approximately 20% fat compared with normal
mouse hepatocytes, which contain approximately 0.2%
(Bicudo, 1996
), and Vianna et
al. (2001
) speculate that
fat-induced UCP2 expression in placental mammals is similar to a mechanism
also present in birds, linking food availability and uncoupling of
H+ entry from ATP synthesis.
On the basis of the uncoupling activity of UCP2 and UCP3, it has been
proposed that, as with UCP1, they too could contribute to adaptive
thermogenesis. However, the physiological role of UCP2 and UCP3 is still
highly controversial, with several studies supporting or rejecting their
thermogenic role (Ricquier and Bouillaud,
2000; Nedergaard et al.,
2001
). Despite its proton conductance capacity, UCP3 expression in
skeletal muscle does not change in response to 48 h of cold exposure, a
condition known to increase UCP1 mRNA levels three- to fourfold. Furthermore,
UCP2 and UCP3 mRNA levels increase during starvation, a situation known to
decrease energy expenditure (Samec et al.,
1998
). However, the recent finding of increased thermogenesis in
transgenic mice overexpressing UCP3
(Clapham et al., 2000
)
strongly favors a role for UCP3 in adaptive thermogenesis.
Even if the primary role of UCP2 and UCP3 in placental mammals is not
adaptive thermogenesis, this might not necessarily be the case for HmUCP.
Placental mammals have brown adipose tissue whose temperature can rise 3-5
°C within minutes of adrenergic stimulation
(Branco et al., 1999).
However, unlike placental mammals, birds do not possess brown adipose tissue
or a similarly thermogenic tissue and seem to possess only one UCP1 homolog.
The presence of HmUCP mRNA in the pectoral muscle and heart and its
upregulation during torpor suggest a thermogenic role during rewarming. The
presence of HmUCP in the skeletal muscle may also be relevant for shivering
thermogenesis by decreasing the thermodynamic efficiency of mitochondrial ATP
synthesis. Shivering-induced ATP breakdown stimulates mitochondrial oxidation
and ADP phosphorylation which, in the presence of HmUCP, will dissipate
greater amounts of heat.
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Concluding remarks |
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Acknowledgments |
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References |
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