1 Biochimie Cellulaire, Centre National de la Recherche Scientifique Unité Propre de Recherche 9065, Collège de France, 75231 Paris Cedex 05; and 2 Hôpital Lariboisière, Institut National de la Santé et de la Recherche Médicale Unité 127, 75010 Paris, France
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ABSTRACT |
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During muscle development, an isozymic transition of the
glycolytic enzyme enolase occurs from the embryonic and ubiquitous -isoform to the muscle-specific
-isoform. Here, we
demonstrate a stimulatory role of thyroid hormones on these two enolase
genes during rat development in hindlimb muscles and an inhibitory
effect on the muscle-specific enolase gene in cardiac muscle. In
hindlimb muscles the ubiquitous
-transcript level is diminished by
hypothyroidism, starting at birth. On the contrary, the more abundant
muscle-specific
-transcript is insensitive to hypothyroidism before
establishment of the functional diversification of fibers and is
greatly decreased thereafter. Our data support the hypothesis of a role
of thyroid hormones in coordinating the expressions of contractile
proteins and metabolic enzymes during muscle development. The
subcellular localization of isoenolases, established here, is not
modified by hypothyroidism. Our results underline the specificity of
action of thyroid hormones, which modulate differentially two isozymes in the same muscle and regulate, in opposite directions, the expression of the same gene in two different muscles.
glycolysis; muscle specific; energy metabolism
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INTRODUCTION |
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MUSCLE PHYSIOLOGY is greatly influenced by thyroid status. Thyroid deficiency leads to muscular weakness and excessive fatigability, characterized by a fall in production of energetic compounds. In developing muscle, thyroid hormones control not only myosin isoform transitions but also the expression of several genes, such as those encoding the Ca2+-ATPase of the sarcoplasmic reticulum (41, 42, 45), the Na+-K+-ATPase pump (2, 12), and enzymes of the oxidative and glycolytic pathways (1, 22, 36, 43). Thus they modulate energy-consuming reactions (contraction and relaxation) as well as reactions of the energy-producing pathways. In a study of the metabolic specialization of individual fibers, in fast- and slow-twitch rat muscles, it has been suggested that thyroid hormones could be useful to optimally coordinate the expressions of contractile and metabolic proteins during development (36). Thus patterns of energy metabolism could adjust to specific energy requirements. Many studies dealing with the control of energy metabolism by thyroid hormones have been devoted to enzymes of the oxidative pathway; fewer studies have been devoted to glycolytic enzymes.
Enolase (2-phospho-D-glycerate
hydrolyase, EC 4.2.1.11) is a glycolytic enzyme that is active as a
dimer. In higher vertebrates it exhibits cell type-specific isoforms
constituted from the three subunits, ,
, and
, encoded by
different genes (7, 13, 38). The
-homodimer is predominant in all
embryonic tissues and remains expressed at various levels in most adult
tissues. During development, accumulation of specific isoforms
accompanies the differentiation of two tissues with high energy
demands:
and
in brain and
and
in striated
muscles (14, 24, 30, 31, 49). At the adult stage,
-enolase
transcript and subunit accumulate preferentially in fast-twitch fibers.
In skeletal muscle, total enolase activity is highest in fast-twitch
muscle, and this activity is almost entirely due to the muscle-specific homodimer
. In rat cardiac muscle, which exhibits a lower enolase activity, the three isozymes
,
, and
are almost
equally abundant (18, 23-25). In cardiac muscle the decrease of
total enolase activity observed during postnatal development results from a drop of
-enolase activity (23, 25).
Quantitative analyses of -enolase gene expression during development
of mouse hindlimb muscles have shown a biphasic accumulation of
-enolase transcripts (30). A prenatal increase accompanies the
establishment of innervation, and a postnatal rise is temporally correlated with the increase in thyroid hormone levels in serum (9, 32)
and with the accumulation of the transcripts of the rapid adult form of
myosin, myosin heavy chain (MHC) IIB, known to be dependent on these
hormones (8, 9, 40).
The influence of thyroid hormones on enolase gene expressions has not
been studied. Here, we present the effects of rat thyroid status on the
- and
-isoform gene expressions during development in two types
of muscle: hindlimb muscles, which are mostly glycolytic and fast
twitch, and heart, which is oxidative.
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EXPERIMENTAL PROCEDURES |
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Animals. Wistar rats (IFFA-CRÉDO, L'Arbresle, France) were kept under controlled housing conditions. Animals in three different thyroid statuses were used. Control rats were euthyroid. Hypothyroidism was induced in pregnant rats by feeding a diet containing 0.1% methylthiouracil (MTU) from 16 days of gestation and suppressing iodine throughout the experiment. In the third group, young MTU-treated rats were injected daily, from birth, with 3,5,3'-triiodo-L-thyronine (Sigma Chemical, l'Isle d'Abeau Chesnes, France, T3, 30 ng/10 g body wt ip). Litters were maintained at seven pups per dam.
The rats were used at birth and at 4, 8, 13, 15, 21, and 28 days after birth. Muscles were dissected and immediately frozen in liquid nitrogen for protein and mRNA extraction.Northern blot analysis. Total RNA was prepared according to the RNA-Plus manufacturer's protocol (Bioprobe, Montreuil, France).
Northern blots and hybridization procedures were carried out as previously described (30).Probes.
The probe for -enolase mRNA corresponds to the 3'-untranslated
region of the murine
-enolase mRNA (European Molecular Biology Laboratories/GenBank Data Library ACX57747). The specific
-enolase probe corresponds to the 3'-untranslated region of the mouse
-enolase mRNA (European Molecular Biology Laboratories/GenBank Data
Library ACX52379). Probe for MHC IIB mRNA was provided by Shin'ichi
Takeda and corresponds to the 5'-noncoding region of the mouse
mRNA (44). A 30mer oligonucleotide probe corresponding to the 18S
ribosomal rat RNA (6) was used to normalize the results to the same
amount of total RNA (30).
Enolase enzyme activity. Enolase activity was measured at 30°C. Activity was measured spectrophotometrically at 240 nm as the conversion of sodium 2-phospho-D-glycerate to phosphoenolpyruvate and expressed in international units, as previously described (26).
Protein concentration was determined by using the Bio-Rad (Bradford) protein assay and BSA as a standard.Western blot analysis.
Protein extraction and Western blot analysis, and then two-dimensional
gel electrophoresis were performed according to a
standardized protocol (33). Briefly, the blots were kept dry until
immunologic treatments were applied, according to the protocol
indicated by Amersham (Les Ulis, France) for the enhanced
chemiluminescence Western blotting detection system. The anti-- and
anti-
-enolase rabbit sera were diluted 1:5,000 and 1:50,000,
respectively. The peroxidase-coupled secondary antibody was anti-rabbit
IgG (Biosys, Compiègne, France).
Immunocytochemistry. After rapid removal, the muscles were dissected and immersed in 2% paraformaldehyde in PBS for 3 h at 4°C. They were then treated as previously described (25). After overnight incubations at 4°C with the primary antibodies, cryostat sections were washed and incubated for 1 h at room temperature with the appropriate secondary antibodies. Muscle sections were then mounted in Imunofluor (New England Nuclear) and observed by confocal microscopy. Control preparations were obtained using the second antibody alone or rabbit preimmune serum. No fluorescent staining was visible in these conditions (data unshown).
Production of specific antibodies directed against the rabbitStatistical analysis. Data were statistically analyzed using the STATVIEW program, by ANOVA or Student's t-test. P < 0.05 was considered significant.
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RESULTS |
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Thyroid status.
Three series of neonatal rat pups were analyzed: controls (C), which
were euthyroid; rats treated with MTU, an antithyroid drug that induces
hypothyroidism; and MTU-treated rats that received a daily injection of
T3 from birth (MTU + T; see
EXPERIMENTAL PROCEDURES). The body
weight of control rats increased more rapidly than that of hypothyroid
rats (Fig.
1A).
At 21 days, body weights and heart weights of MTU-treated rats were
only 40% of those of the controls.
T3 treatment (30 ng/10 g) of
hypothyroid rats did not significantly modify the developmental profile
of body weight (Fig. 1A) or heart
weight (Fig. 1B). Thus the dose of
T3 used in this protocol did not
induce the cardiac hypertrophy known to be produced by hyperthyroidism.
It is known that induction of the rapid adult form of MHC, MHC IIB, is
dependent on thyroid hormones. We have measured the levels of MHC IIB
mRNA in extracts from hindlimb muscles (Fig.
1C). MHC IIB mRNA level started to increase in muscle extracts of control rats after 8 postnatal days. In
MTU-treated rats, MHC IIB mRNA level remained undetectable by Northern
blot analysis throughout the experiment. In MTU + T rats, the
developmental profile of MHC IIB mRNA was comparable to that of
controls, indicating the effectiveness of
T3 treatment.
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Differential regulation of - and
-enolase gene expressions by thyroid hormones in rat
hindlimb muscles.
We have compared the developmental profiles of
- and
-enolase
transcripts in hindlimb muscles from control and hypothyroid rats (Fig.
2, A and
C). During normal muscle
development, the level of
-enolase transcripts did not vary
significantly (Fig. 2C). At all the
examined times, except at birth, this level was significantly reduced
in hypothyroid animals. At 21 and 28 days the
-enolase level in
muscles of hypothyroid rats corresponded to 35% of the control levels.
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Total enolase activity is decreased by hypothyroidism in hindlimb
muscles.
Total enolase activity was measured in hindlimb muscle extracts of
control and hypothyroid rats. This activity increased linearly during
the postnatal muscle maturation in both groups of animals, but the
slope of the line was significantly lower in hypothyroid rats than in
controls (Fig.
3A).
During the same period, an increase in the muscle-specific enolase
transcript level, , was observed (Fig.
2A). Statistical analysis indicated
a positive linear relationship between total enolase activity and
-enolase transcript level, independently of the animal group (Fig.
3B).
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Microheterogeneity of - but not
-enolase subunit is influenced by the thyroid status in
developing hindlimb muscle.
Biochemical analyses of
- and
-enolase subunits have shown a
microheterogeneity of these proteins that is modulated during mouse
hindlimb muscle maturation (33). We have now examined whether similar
developmental changes occur in rats. Hindlimb muscle extracts were
analyzed by two-dimensional gel electrophoresis and then by Western
blot from embryonic day 18 (E18) to
postnatal day 21 (P21). To visualize
both subunits, the blots were sequentially reacted with the
anti-
-enolase and with the anti-
-enolase serum. In the less
mature muscles (E18), a large amount of the ubiquitous
-subunit and
a small amount of
-enolase subunit were each expressed as one major
basic spot (Fig. 4, control). A large
increase in the concentration of
-enolase subunit occurred between
E18 and postnatal day 15 (P15).
Between postnatal day 8 (P8) and P15
there was a transition in the expression of
-enolase variants, with the acidic spot becoming predominant. At P15 and later,
- and
-enolase subunits exhibited two electrophoretic variants differing in their isoelectric points.
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Localization of - and
-enolase in
hindlimb muscle fibers by indirect immunofluorescence labeling and
confocal microscopy.
Taking advantage of antibodies produced in different species, we have
compared the fiber localization of
- and
-enolase subunits in
double-labeling experiments. As shown on gastrocnemius muscle sections
of 15-day-old rats (Fig. 5,
a and
b), some fibers expressed both
subunits (1), some expressed
- but not
-subunits (2), and some
expressed
- and not
-subunits (3). Other double-labeling
experiments were performed using monoclonal antibodies specific for
slow- or fast-type MHCs and the polyclonal antibodies specific for each
enolase isoform. The results shown here on gastrocnemius sections of
28-day-old rats demonstrated that the muscle-specific enolase subunit
was expressed in all fast-twitch and not in slow-twitch fibers (Fig. 5,
c and
d). Similar results were obtained
when the immunocytochemical analysis was conducted with muscles of
hypothyroid animals: the
-subunit was never detected in slow-twitch
fibers (Fig. 5, g and
h), in contrast to the
-subunit
(Fig. 5, e and f).
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Hypothyroidism increases -enolase gene expression in
the heart.
It is assessed that the adult heart relies on oxidative metabolism.
Hypothyroidism did not modify significantly the
-enolase transcript
level in developing cardiac muscle (Fig.
7A) but
increased the transcript level of the muscle-specific isoform after 8 days (Fig. 7B). At 13-15 days,
the
-enolase transcript levels are significantly higher in
hypothyroid than in control rats, but values obtained at 21-28
days are more dispersed, and in this case the differences are not
statistically significant. Interestingly, an increase in the
-subunit level compared with control level was visible in
hypothyroid rats at 21 and 28 days (Fig.
8).
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DISCUSSION |
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Among glycolytic enzymes, enolase is unique for the strict cell type
specificity of its muscle isoforms, and
. Our previous results suggested a role of thyroid hormones in the postnatal rise of
-enolase gene expression (30). Thus the enolase isozymic system has
allowed us to study the effect of these hormones simultaneously on the
ubiquitous (
) and the muscle-specific (
) genes, both expressed
throughout development.
Differential regulation of - and
-enolase genes by thyroid hormones during hindlimb
muscle development.
We demonstrate here, for the first time, an important role of thyroid
hormones on
- and
-enolase gene expressions during rat muscle
maturation. Data obtained from hypothyroid rats show that
- and
-enolase gene expressions are responsive to thyroid hormones, but in
different ways. Starting at birth, the ubiquitous enolase transcript
level is diminished by hypothyroidism. Thus, throughout the period
studied,
-enolase gene expression appears sensitive to thyroid
hormones, even to the low levels of these hormones already present in
the circulation of neonates. On the contrary, the muscle-specific
enolase gene expression is insensitive to the thyroid status of the
rats before the establishment of the functional diversification of
fibers, indicated in our experiments by the MHC IIB transcript
accumulation. The fraction of
-enolase expression responding to
thyroid hormones thereafter is less important than that of
-enolase.
However, because of the major abundance of the
-isoform in
postnatal skeletal muscles (23, 25, 30), the decreased expression of
the
-enolase gene should be the determinant for the modulation of
total enolase activity. Indeed, we have established that there is a
linear relationship between
-enolase transcript level and total
enolase activity during normal or hypothyroid postnatal development.
Cellular and subcellular localization of muscle enolase isoforms is
independent of thyroid status.
The immunocytochemical analyses have shown that, after the
establishment of functional fiber diversity in control rats, the muscle-specific enolase subunit, , is specifically expressed in
fast-twitch fibers. Although neonatal MHC persists in many myofibers of
hypothyroid rats (5, 16),
-enolase immunoreactivity still presents a
nonuniform myofiber distribution and is absent from slow-twitch fibers,
demonstrating that this heterogeneous distribution is not under thyroid
hormone control. In this study we have observed, for the first time,
that the ubiquitous subunit of enolase,
, is expressed not only in
nonmuscle cells (see labeled vessel cells in Figs. 5 and
6) but also in skeletal muscle fibers. No fiber
type-related distribution of this isoform is evident. Hypothyroidism
induces an important decrease of
-enolase gene expression (at P21,
-enolase transcript level is 40% of control), and at least part of
this drop probably takes place within myofibers.
Mechanisms of action of thyroid hormones on enolase gene
expressions.
The effects of thyroid hormones on - and
-enolase expressions can
be direct or indirect. Direct effects are mediated via T3 receptors bound to a thyroid
hormone response element on the gene. Sequence analysis of the
-enolase gene did not reveal the canonical motif composed of two
half-sites, which are usually separated by four nucleotides, and we
were able to characterize half-sites only. Such a sequence analysis
cannot be done for the rat
-enolase gene, which has not yet been cloned.
Thyroid hormone sensitivity of enolase genes is muscle type specific. In heart, in contrast to hindlimb muscles, enolase gene expressions are not depressed by hypothyroidism. On the contrary, thyroid hormone withdrawal results in an increase in the muscle-specific form of enolase gene expression.
It had been proposed that hypothyroidism induces mitochondrial metabolism impairment, and this could lead to an abnormal recruitment of several metabolic pathways, such as glycolysis (21). The effects of thyroid hormones on the enzymes of the respiratory chain are also developmentally modulated and are specific to the tissue examined. These differences may be a consequence of the different energy requirements of tissues such as heart and skeletal muscle during development (37, 43). The interdependency of these two energy-producing pathways, oxidative and glycolytic, should be considered to interpret the resulting effect of thyroid hormones on energy production during skeletal and cardiac muscle development. From our results, we can establish some correlation between the expression of the ![]() |
ACKNOWLEDGEMENTS |
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We thank J. P. Martin for the photographic art work of Western blots. We are indebted to Beatrice Desvergne for stimulating discussions and helpful suggestions.
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FOOTNOTES |
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This work was supported by grants from the Association Française contre les Myopathies to M. Lazar. T. Merkulova was a recipient of support from Fondation pour la Recherche Médicale.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: M. Lucas, Biochimie Cellulaire, CNRS UPR 9065, Collège de France, 11, Place Marcelin Berthelot, 75231 Paris Cedex 05, France (E-mail: mlucas{at}ext.jussieu.fr).
Received 2 April 1999; accepted in final form 1 October 1999.
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