Plasticity of muscle fibre number in seawater stages of Atlantic salmon in response to photoperiod manipulation
1 Gatty Marine Laboratory, School of Biology, University of St Andrews, St
Andrews, Fife, KY16 8LB, UK,
2 Marine Harvest Scotland Ltd, Craigcrook Castle, Edinburgh, EH4 3TU,
UK,
3 BioMar Ltd, North Shore Road, Grangemouth Docks, Grangemouth, FK3 8UL,
UK
4 Roche Vitamins Ltd, Heanor, Derbyshire, DE75 7SG, UK
* Author for correspondence (e-mail: iaj{at}st-andrews.ac.uk)
Accepted 2 July 2003
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Summary |
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Key words: Atlantic salmon, Salmo salar, skeletal muscle, myogenesis, growth, photoperiod, myogenic precursor cell, phenotypic plasticity
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Introduction |
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Growth of the skeletal muscle involves the recruitment and subsequent
hypertrophy of muscle fibres (Weatherley
et al., 1988). The major mechanism for expansion of muscle bulk in
postembryonic stages is mosaic hyperplasia
(Rowlerson and Veggetti, 2001
)
involving a population(s) of proliferating myogenic progenitor cells that are
scattered throughout the myotome (Johnston
et al., 1995
; Rowlerson et
al., 1995
). New myotubes form on the scaffold of existing fibres
to produce a mosaic of muscle fibre diameters. Around 80% of the myogenic
cells in the sub-Antarctic fish Harpagifer bispinis were readily
labelled with bromo-deoxyuridine, indicating that they were actively dividing
(Brodeur et al., 2003a
). The
myogenic progenitor cells are thought to undergo a limited number of divisions
before exiting the cell cycle and expressing genes associated with terminal
differentiation, such as myogenin
(Johnston et al., 2000b
) and
desmin (Koumans, 1992
).
Myoblasts either fuse to form myotubes or are absorbed into maturing fibres as
they expand in diameter (Koumans and
Akster, 1995
; Johnston,
2001
). The embryological origin and the stage at which myoblasts
become committed to particular fates is uncertain
(Koumans and Akster, 1995
;
Stoiber and Sänger,
1996
). In Atlantic salmon, mosaic hyperplasia begins around first
feeding and continues throughout freshwater
(Higgins and Thorpe, 1990
;
Johnston and McLay, 1997
) and
during the first part of seawater life
(Johnston et al., 2000a
).
Significant genetic variation has been demonstrated in the duration of fibre
recruitment and in the maximum number of muscle fibres
(FNmax; Johnston et
al., 2000a
). FNmax and the density of myogenic
progenitor cells also show developmental plasticity with respect to the
thermal regime during the freshwater stages of the life cycle (Johnston et
al., 2000b
,
2003a
). However, the
consequence of photoperiod regime for the growth of the skeletal muscle has
not previously been investigated.
The endocrine control of growth is complex and the role of hormones and
growth factors regulating myogenesis such as insulin-like growth factor-I
(IGF-I), myostatin (MSTN), scatter factor/hepatocyte growth factor (HGF) and
the fibroblast growth factor (FGF) gene family is poorly understood
(Mommsen and Moon, 2001;
Johnston et al., 2003a
). HGF
stimulates myogenic cell proliferation
(Tatsumi et al., 1998
), and
its receptor, c-met, is a useful marker of myogenic cells
(Cornelison and Wold, 1997
;
Johnston et al., 1999
; Brodeur
et al.,
2003a
,2003b
).
Myogenic cells possess IGF-I (Castillo et
al., 2002
) and FGF receptors
(Thisse et al., 1995
), and IGF
has been reported to stimulate both cell proliferation and muscle-specific
gene expression and differentiation under certain cell culture conditions
(Florini et al., 1991
).
Feeding is associated with an increase in IGF-I and FGF2 mRNA levels
(Chauvigné et al., 2003
)
and an increase in the number of proliferating myogenic progenitor cells
(Brodeur et al., 2003b
). Growth
hormone is thought to act synergistically with IGF-1 produced in the liver and
locally in the skeletal muscle to stimulate muscle growth
(Björnsson, 1997
;
Mommsen and Moon, 2001
). Thus,
hormones and growth factors that change in concentration in response to
changing day length also influence the behaviour of myogenic cells.
In the present study, the growth of fast myotomal muscle was investigated in 1-SW Atlantic salmon subject to either natural photoperiod or continuous light from 1 November to 18 June. The aim was to test the hypothesis that enhancement of growth by continuous light treatment results from the plasticity of muscle fibre recruitment and is linked to an increase in the production of myogenic progenitor cells.
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Materials and methods |
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The sea cages were also stocked with Goldsinney wrasse (Ctenolabrus rupestris; 1 per 50 salmon) to control sea lice infestations. Additional treatments with Excis® [cypermethrin at 1% (m/v); Novartis Animal Health, Litlington, UK] for 1 h were performed on three occasions. In all treatments, the net pens were raised to a depth of 1 m and enclosed in a tarpaulin, with oxygen provided to ensure that a minimum level of 7 p.p.m. was maintained.
Random samples of fish (103-145 per cage) were repeatedly weighed at approximately 6-week intervals to assess growth performance (Table 1). Fork length (FL) and body mass (Mb) were recorded, and the condition factor (CF) of the fish was calculated according to the formula: CF=[(Mb/FL3)x100]. A random sub-sample of the fish was sampled for analysis of muscle structure on the dates shown in Table 2. In all cases, fish were identified by brand and cross-referenced against PIT-tag number.
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Fish that were clearly maturing as grilse were identified and removed from the cages during the weighing procedures on 17 July 2001. This enabled the percentage maturing as grilse to be determined for each cage and treatment.
Analysis of muscle cellularity
The fish were sacrificed with a sharp blow to the head, and muscle blocks
prepared immediately. A 0.7 cm-thick steak was prepared at the level of the
first dorsal fin ray using a sharp knife. The steak cross-section was traced
onto an acetate sheet in triplicate using a fine pen to identify slow and fast
myotomal muscle, the fin muscles and non-muscle components. The fast myotomal
muscle component of the steak from one side of the body was divided into a
series of evenly spaced blocks ranging from three per individual in the
smallest fish to 12 per individual in the largest fish. Blocks were mounted on
cork sheets and frozen in 2-methyl butane cooled to near its freezing point
(-159°C) in liquid nitrogen. The blocks were wrapped in tin foil and
stored in a liquid nitrogen refrigerator until they could be processed. The
blocks were equilibrated to -20°C, and 7 µm frozen sections cut,
mounted on poly-L-lysine-coated slides, air dried and either
stained with Mayer's haematoxylin or used for immunohistochemistry. The
outlines of 100-300 muscle fibres per block were digitised using an image
analysis system (SigmaScan software, SPSS Inc., Chicago, IL, USA), and the
mean fibre diameter was calculated. A minimum of 800 and a mean of 1000 muscle
fibres were measured per fish and the fibre number estimated from the total
cross-sectional area (Johnston et al.,
1999).
Immunohistochemistry
Frozen sections (18 mm thick) were fixed in acetone for 10 min and then air
dried for 10 min. Myogenic cells were identified using a c-met primary
antibody (Santa Cruz Biotechnology Ltd, Santa Cruz, CA, USA) and an
extravidin-Cy3 conjugated secondary antibody (Sigma, Poole, UK) as described
previously (Johnston et al.,
1999,
2003b
). Sections were
counterstained in Sytox green® (Molecular Probes Inc., Leiden, The
Netherlands) to visualise all the nuclei and then mounted in a fluorescent
medium (DAKO Corp., Carpinteria, CA, USA). The sections were viewed with a
laser confocal microscope (BioRad Radiance 2000). The density of myonuclei
(stained green with Sytox green) and c-met+ve cells (stained
yellow) were quantified using a sequential scanning mode in five or six fields
of 0.4 mm2 tissue section per fish using LaserPix vs. 4.0 software
(BioRad, Hemel Hempstead, UK). Nuclear counts were corrected for section
thickness and the mean diameter of nuclei
(Abercrombie, 1946
) using data
previously determined from electron micrographs
(Johnston et al., 2000a
).
Nuclear content of isolated muscle fibres
Small bundles of fast muscle fibres were isolated from the dorsal myotome
posterior to the region sampled for histology. Fibre bundles were pinned at
their resting length on strips of Sylgard (RS Ltd, Corby, UK) and fixed for
6-10 h in 4% (m/v) paraformaldehyde in phosphate-buffered saline (PBS). Single
muscle fibres freed from connective tissue were isolated in PBS solution using
a binocular microscope fitted with dark-field illumination. Fibres were
suspended in 1% (m/v) saponin in PBS for 3 h, washed three times in PBS and
treated with 2 µg ml-1 units RNase (Sigma). Following further
washes in PBS, the nuclei were stained with 30 µmol l-1 Sytox
green in PBS for 5 min in the dark. Fibres were mounted on glass slides using
fluorescent mounting medium (DAKO Corp.) and viewed with a laser confocal
microscope (BioRad Radiance 2000). The density of fluorescent myonuclei was
quantified in fibre segments 0.3-0.6 mm long using a z-series of 1
µm optical thick sections and LaserPix vs. 4.0 software.
Statistical analysis
The effects of growth performance [Mb, FL and
CF] and muscle cellularity [fibre number and fibre density (fibre
number/muscle cross-sectional area)] were investigated with a General Linear
Model analysis of co-variance (ANCOVA) with a normal error structure using
sequential sums of squares (MinitabTM statistical software; Minitab
Inc., State College, USA). Post-hoc testing was by Tukey's multiple
comparison tests. Plots of residuals versus fitted values, the normal
probability of residuals and histograms of residuals were routinely examined
to ensure the data fulfilled the assumptions of the ANOVA.
Nonparametric statistical techniques were used to fit smoothed probability
density functions (pdfs) to the measured diameters using a kernel function as
described in Bowman and Azzalini
(1997). The application of
these methods to the analysis of muscle fibre diameters has been described in
detail previously (Johnston et al.,
1999
). Values for the smoothing parameter h
(Bowman and Azzalini, 1997
)
were in the range 0.084 to 0.209, with no systematic variation between samples
and/or treatments. Bootstrap techniques were used to distinguish underlying
structure in the distributions from random variation
(Bowman and Azzalini, 1997
;
Davison and Hinkley, 1997
;
Johnston et al., 1999
). The
Kolmogorov-Smirnov two-sample test statistic was used to test the null
hypothesis that the probability density functions of groups were equal over
all diameters. To supplement this test, density curves for each treatment were
compared graphically by constructing a variability band around the density
estimate for the combined populations estimated by pooling fish over the
age-class and using the mean smoothing parameter. Any region where the
individual pdfs fell outside of this `reference' band provided evidence for a
major difference between the densities.
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Results |
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Fork length (not illustrated) demonstrated a similar response to body mass, with significant effects of treatment (F1,2514=46.35; P=0.02), treatment x GP (F1,2524=98.40; P<0.001) and cage nested within treatment (F2,2514=4.76; P<0.01). Condition factor demonstrated the largest cage effect of the parameters investigated, and this was particularly marked for the ambient photoperiod cages (Fig. 1B). All the fixed factors tested were significant for condition factor; treatment (F1,2514=20.49; P<0.05), treatment x GP (F1,2514=97.96; P<0.001) and cage nested within treatment (F2,2514=8.72; P<0.01). Combining the data for replicate cages, condition factor was significantly higher in the continuous light than in the ambient photoperiod cages for weighings 8-10 (P<0.01; Tukey's test).
Maturity
The percentage identified as maturing as grilse was 42% and 33% for the
ambient photoperiod cages and 41% and 31% for the cages subjected to
continuous light over the winter.
Muscle cellularity
Changes in the number of fast muscle fibres per myotomal cross-section with
growth and following photoperiod manipulation are illustrated in
Fig. 2. This figure also
illustrates how temperature and natural day length varied throughout the
experiment. The effect of photoperiod regime on muscle fibre number was
analysed using two ANOVA models for the sample points shown in
Table 3. For Model A, with
growth period as covariate, there were significant effects of treatment and a
significant treatment x growth period interaction but no significant
cage effect on fibre number (Table
3). On 2 November, 24-30 h after the lights were switched on,
there were 637x103 fibres in the ambient fish and
621x103 fibres in the photoperiod-manipulated fish sampled
(Fig. 2). At the next sample on
10 January, 40 days after the start of the experiment, fibre number had
increased 28.5% in the fish subject to continuous lighting
(799x103) (P<0.01; Tukey's test) but was
unchanged in the fish on ambient photoperiod (
644x103).
The appropriate reference for muscle growth is the total cross-sectional area
of the fibres (TCA) (Fig. 3A).
For Model B, with fibre number as dependent variable and TCA as covariate,
there were significant effects of treatment, with a significant treatment
x TCA interaction term but no significant cage effect
(Table 3). TCA was rather
similar between treatments until the final sample in August 2001
(Fig. 3A). TCA for the final
sample, 70 days after the lights were switched off, was 12.4% greater (10 952
mm2 of muscle) in the continuous light than in the ambient
photoperiod groups (9743 mm2 of muscle) (P<0.05;
Tukey's test). An examination of the distributions of muscle fibre diameters
in the June and August 2001 samples indicated that fibre recruitment had
ceased. There were
1% of fibres in the range 5-10 µm in June and no
fibres less than 10 µm diameter in the August sample. These samples were
therefore combined to provide an estimate of the maximum number of fibres
(FNmax). FNmax was 22.9% higher in the
continuous light (mean ± S.E.M.,
881x103±32x103; N=19) than
in the ambient photoperiod
(717x103±15x103; N=20)
groups (one-way ANOVA, F1, 37=22.0;
P<0.001).
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Fibre density is a composite parameter reflecting changes in fibre number and size. The density of fast muscle fibres declined with growth in seawater as the expansion of muscle fibres outpaced the recruitment of new muscle fibres (Fig. 3B). An ANOVA revealed a significant treatment effect (F1,127=21.73; P<0.05), whereas a treatment x growth period interaction term and cage nested within treatment were not significant. In the sample 70 days after the lights were switched on, the fibre density was 28% higher in the continuous light than in the ambient treatment groups (P<0.05; Tukey's test), reflecting the higher rate of fibre recruitment. There was a tendency for the fibre density to become more similar between groups as the experiment progressed, and in the final sample 70 days after the lights were switched off the treatment effect was no longer significant (Tukey's test).
The smooth distributions of muscle fibre diameter were calculated for all
the sample points. In November, the peak probability density (PD) of
fibre diameter comprised a broad peak with a plateau at 50-100 µm for both
treatments (not shown). For the ambient photoperiod group, the peak
PD of fibre diameter had increased to 110 µm by June 2001 (solid
line in Fig. 4) and reached
140-150 µm in August (not shown). In the June sample, the left-hand tail of
the distribution of fibre diameters had higher values of PD in fish
subject to continuous light (dashed line) than in the fish at ambient
photoperiod (solid line), reflecting the higher fibre number
(Fig. 4). One hundred bootstrap
estimates of the combined population of fibres from both treatments were
calculated. For the January, March (not shown) and June
(Fig. 4) samples, portions of
the left-hand and right-hand tail of the PD were shifted to
respectively higher and lower values in the lit than ambient groups, and
significant differences were found between the groups in nonparametric
Kolmogorov-Smirnov tests (P<0.01). These differences in fibre size
were most pronounced for the June sample
(Fig. 4). By contrast, in the
final sample, the overall distributions of fibre diameter were not
significantly different between treatments (not shown). The maximum fibre size
was 220 µm diameter in both treatments.
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The mean fibre diameter and scaled plots of fibre diameter distribution reflect a combination of fibre recruitment and hypertrophy, which tend to decrease and increase fibre size, respectively. We therefore used the mean values of fibre number per group to estimate the numbers of fibres recruited between successive sample points. The 800-1000 fibres measured at each sample were ranked by diameter, and then the estimated proportion of fibres recruited since the last sample was subtracted and the mean diameter of the remaining samples were calculated. The mean rate of fibre hypertrophy over each growth period showed no consistent difference with treatment (Fig. 5).
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Myonuclei content of isolated fibres
The myonuclear content of isolated single fibre segments was determined for
the June 2001 sample (Fig. 6).
AnANOVA with treatment as a fixed factor and fibre diameter as covariate
revealed a significant difference between treatments
(F1,390=318.1; P<0.001). First-order linear
regression equations were fitted to the data. r2 values
were significantly lower for the continuous lit (0.34) than for the ambient
photoperiod (0.80) groups (Fig.
6). For fibres of 150-µm diameter, the mean myonuclear content
was 27% higher in the photoperiod-manipulated (3118) than ambient (2448)
groups.
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Myogenic cell density
The effect of photoperiod manipulation on the density of c-met
immuno-positive cells is shown in Fig.
7. An ANOVA with fixed factors of treatment and treatment x
GP, and GP as covariate, revealed a significant effect of
photoperiod on the density of c-met+ve cells
(F1,75=50.63; P<0.001). In fish sampled 24-30
h after the lights were switched on, the density of myogenic cells was 12%
higher in fish exposed to continuous light than ambient photoperiod
(P<0.01), rising to a peak of 72% higher after 40 days
(P<0.0001; Tukey's tests; Fig.
7).
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Discussion |
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In the present study, continuous light treatment was shown to produce a marked increase in fibre number within 40 days of the lights being switched on, equivalent to an average recruitment of 4400 fibres day-1 per myotomal cross-section. The corresponding rate of fibre recruitment was less than 200 fibres day-1 per myotomal cross-section in fish exposed to natural daylight. By contrast, over the next 53 days, 900-1000 fibres day-1 per myotomal cross-section were added in both treatments, and recruitment had ceased entirely by June in both cases (Fig. 2). Thus, photoperiod manipulation of fibre number only occurred in a relatively narrow window, which corresponded to the period of decreasing day length (Fig. 2). It is therefore possible that an earlier onset of continuous light would produce a greater effect on fibre recruitment and vice versa. The results are consistent with the view that distinct genetic mechanisms control the duration of fibre recruitment on one hand and its intensity on the other. Once fibre recruitment had ceased, growth occurred entirely via the hypertrophy of fibres formed at earlier stages of ontogeny.
In the present study, the density of c-met-expressing cells was
significantly higher in fish under continuous light than natural day length,
and this was associated with an increase in both myotube formation and the
myonuclei content of muscle fibres (Fig.
7). The myogenic precursors expressing c-met are thought to
represent a relatively rare muscle stem cell population and their progeny at
various stages towards terminal differentiation
(Hawke and Garry, 2001;
Zammit and Beauchamp, 2001
).
Wada et al. (2002
) reported
that, in the mouse, single undifferentiated muscle progenitor cells derived
from a single satellite cell were multipotent and able to differentiate into
myotubes, adipocytes or osteoblasts depending on the culture conditions.
Perhaps the simplest model for muscle growth in fish would be a single
population of myogenic precursors in each muscle type with the fate of the
cells destined to form myotubes determined by local signalling, thereby
ensuring that fibres were added in the correct places as the myotomal cones
expand in volume (Johnston et al.,
2003b
).
The major increase in myogenic progenitor cells was transient and coincident with the increase in myotube formation that accompanied the onset of continuous light treatment (Fig. 7). The relatively low correlation coefficient (0.34) for the relationship between fibre myonuclei content and fibre diameter in the continuous light treatment suggests that not all the fibres absorbed additional nuclei (Fig. 7). Our working hypothesis to explain these results is that the continuous light treatment affected cell cycle duration and/or the number of times the myogenic progenitor cells divided prior to exiting the cell cycle and differentiating (illustrated diagrammatically in Fig. 8).
|
The cellular mechanisms underlying developmental plasticity of fibre
recruitment (Johnston et al.,
2000b,
2003b
) and the phenotypic
plasticity observed with continuous light treatment
(Fig. 2) are almost certainly
different. Salmon reared at different temperatures during the freshwater
stages showed differences in FNmax of up to 22%
(Johnston et al., 2003b
). In
this case, temperature probably influenced the number of myogenic stem cells
but not their subsequent behaviour, since the different
freshwater-temperature-treated fish were reared under identical conditions
during the seawater stages.
The minimum time required for myogenic progenitors to respond to the onset
of continuous light will be limited by their cell cycle duration, which is
known to vary with temperature, growth rate and feeding status
(Brodeur et al., 2003a). The
cell cycle time of myogenic progenitors was estimated at 32 h in rat skeletal
muscle (Schultz, 1996
) and at
81 h in adult stages of the sub-Antarctic fish H. bispinis at
10°C under conditions of zero growth
(Brodeur et al., 2003a
).
Interestingly, in the present study, a significant increase in
c-met+ve cells was observed 24-30 h after the lights were switched
on. A key factor regulating myocycte cell cycle exit and viability is the
cyclin-dependent kinase inhibitor p21. Gene targeting experiments in mice have
shown that myostatin-I (MSTN-I), a member of the TGF-B superfamily of secreted
growth and differentiation factors, is a powerful negative regulator of muscle
fibre number and size (McPherron et al.,
1997
). The overexpression of MSTN-I in C2C12 myoblasts resulted in
a decrease in their proliferation and an increase in their resistance to
apoptosis (Ríos et al.,
2001
). Based on the analysis of cell cycle control proteins, it
has been suggested that MSTN signalling upregulates p21, inhibiting
cyclin-E-Cdk2 activity, causing the hypophosphorylation of retinoblastoma
protein and arrest at the G1 gap phase of the cell cycle
(Thomas et al., 2000
). Thus,
MSTN is a potential candidate for mediating the control of muscle fibre
recruitment by photoperiod, possibly in conjunction with growth hormone and
IGF-I (Björnsson,
1997
).
There was no evidence that the rate of fibre hypertrophy was affected by
light treatment, suggesting that the genetic mechanisms controlling this
process are distinct from those regulating myotube formation and myonuclei
production. Short days appear to inhibit the proliferation of myogenic
progenitors and hence muscle growth. The delayed increase in body mass
observed in the continuous light treatment probably reflects the time required
for hypertrophy of the muscle fibres produced once the inhibitory effects of
short day length are removed. A similar delay in the growth-stimulating
effects of continuous light treatment has been observed previously
(Oppedal et al., 1997). It has
been suggested that the ratio between day/night light intensity is important
with respect to the timing and increase in growth rate observed
(Steffansson et al.,
1991
).
While there were effects of the extended day length in winter on growth and
muscle fibre recruitment, the expected reduction in the percentage of fish
sexually maturing (Hansen et al.,
1992; Porter et al.,
1999
) was not found. Endal et al.
(2000
) also reported that
holding fish on long days from November to July failed to reduce maturity;
indeed, in their study maturity was significantly enhanced. The relationships
between the light intensity of the extended photoperiod, growth rate and
maturity may be more complex than previously considered
(Oppedal et al., 1997
).
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Acknowledgments |
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