Proliferation of myogenic progenitor cells following feeding in the sub-antarctic notothenioid fish Harpagifer bispinis
1
Gatty Marine Laboratory, School of Biology, Division of Environmental and
Evolutionary Biology, University of St Andrews, St Andrews KY16 8LB,
Scotland
2
Centro Austral de Investigaciones Científicas (CADIC), Consejo
Nacional de Investigaciones Científicas y Técnicas (CONICET),
CC92, Ushuaia, 9410, Tierra del Fuego, Argentina
* Author for correspondence at present address: Toxicology and Environmental Research and Consulting Laboratory, The Dow Chemical Company, 1803N Building, Midland, MI 48674, USA (e-mail: jcbrodeur{at}dow.com)
Accepted 26 September 2002
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Summary |
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Key words: myogenic progenitor cell, notothenioid fish, Harpagifer bispinis, temperature, photoperiod, satellite cells, specific dynamic action, oxygen consumption
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Introduction |
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Since the myotomal muscle constitutes the largest fraction of tissues in
most fish species (Bone, 1978),
plasticity of fish organismic growth implies a corresponding responsiveness in
the growth dynamics of the muscle (Valente
et al., 1999
). Postlarval muscle growth in fish results from both
an increase in diameter of already existing fibres (hypertrophy) and the
recruitment of new fibres (hyperplasia)
(Weatherley et al., 1988
;
Rowlerson and Veggeti, 2001
).
The skeletal muscle is a differentiated tissue and post-embryonic growth
depends on the proliferation of a population of myogenic progenitor cells to
provide a source of nuclei for both fibre recruitment and hypertrophy
(Koumans and Akster, 1995
).
These progenitor cells are equivalent to the satellite cells described in
mammals (Mauro, 1961
) and can
be identified by their expression of c-met, the receptor for hepatocyte growth
factor (Cornelison and Wold,
1997
), which is believed to be involved in their activation
(Tatsumi et al., 1998
).
Proliferation and differentiation of the myogenic progenitor cells is
critically dependent on a family of four closely related muscle regulatory
factors (MRFs) that share a common DNA-binding and dimerization motif referred
to as the basic helixloophelix domain
(Edmonston and Olson, 1993).
This family consists of MyoD, myogenin, myf5 and MRF4
(Watabe, 2001
;
Rescan, 2001
). The primary
MRFs, MyoD and myf5, are required for myogenic determination, whereas the
secondary MRFs, myogenin and MRF4, are required later to initiate and
stabilize the differentiation program
(Megeney and Rudnicki, 1995
;
Rudnicki and Jaenisch,
1995
).
Although food intake is a major limiting factor of growth rate in fish
(Brett, 1979;
Wootton, 1998
), the influence
of individual feeding events on muscle growth dynamics remains largely
unknown. In all animals, feeding produces an increase in metabolic rate, which
is referred to as the specific dynamic action (SDA)
(Jobling, 1994
). This
phenomenon is believed to result in large part from a stimulation of protein
synthesis induced by the elevation of free amino acid concentrations (Brown
and Cameron, 1991a
,
b
;
Houlihan et al., 1995
). In
marine ectotherms, the rate of oxygen consumption typically increases by 2-4
times pre-feeding levels within a few hours
(Peck, 1998
). The duration of
the SDA, however, varies enormously with temperature and with the size and
composition of the meal (Muir and Niimi,
1972
; Jobling and Davies,
1980
; Johnston and Battram,
1993
).
Post-prandial elevations of free amino acid concentrations and protein
synthesis have been previously noted in fish muscle
(Lyndon et al., 1992;
Carter et al., 2000
),
suggesting a stimulation of muscle tissue synthesis and turnover by feeding.
In agreement with these observations, two recent studies also provided
evidence that feeding status influences the cellular dynamics of muscle
growth. In rainbow trout Oncorhynchus mykiss, primary myogenic cell
lines isolated from fed animals were found to differ extensively in terms of
their size, morphology and proliferation rate to those isolated from fasted
animals (Fauconneau and Paboeuf,
2000
). MyoD expression was also shown to increase significantly
after a meal in the skeletal muscle of the Antarctic notothenioid fish
Notothenia coriiceps, although observations were not continued long
enough to determine whether this phenomenon was associated with a net increase
in the number of myogenic cells (Brodeur et
al., 2002
).
The majority of Notothenioid fish, including Harpagifer species,
have a low number of myotomal muscle fibres for their body size such that
growth after the post-larval stages occurs entirely via fibre
hypertrophy (Battram and Johnston,
1991; Fernandez et al.,
2000
; Johnston et al., in press). Such species therefore represent
a simple model for studying fibre hypertrophy independently of fibre
recruitment. Harpagifer bispinis is a demersal sit-and-wait predator
that is relatively common in the inter-tidal zone of the Beagle Channel,
Tierra del Fuego. It is subjected to large annual variations in temperature
and day length and would be expected to exhibit highly seasonal growth
patterns.
The aim of the present study was to investigate the influence of food intake on the activation and proliferation of myogenic progenitor cells by monitoring MRFs expression and total myogenic cell numbers following a single meal in H. bispinis acclimatized to either simulated summer (10°C; 18 h:6 h light:dark) or simulated winter (5°C; 6 h:18 h light:dark) conditions. We wished to test the hypothesis that feeding stimulated a net increase in myogenic progenitor cells and that the response was influenced by temperature and photoperiod, reflecting the seasonality of growth patterns. Preliminary experiments established the time-course of the SDA to provide an indirect estimate of the period over which a satiating meal stimulated protein synthesis and, potentially, muscle growth.
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Materials and methods |
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Oxygen consumption
Oxygen consumption of the summer fish was measured in 300 ml respirometers
(lengthxheightxwidth: 12.5 cmx5 cmx5 cm, but smaller
45 ml respirometers (lengthxheightxwidth: 7.5 cmx2.5
cmx2.5 cm) were used for winter fish in order to detect accurately the
smaller variations of dissolved oxygen concentrations generated by this group
(due to lower oxygen consumption rates). Both types of respirometers were made
of Perspex (60 mm thick) and possessed a port (1.5 cm diameter) covered with a
rubber cap to allow water samples to be taken and food to be introduced
without disturbing the fish. Black plastic sheets were fixed onto the sides
and top of the chambers to reduce visual disturbance. Six respirometers were
used in parallel for both groups of fish (1 fish per respirometer). The
respirometers were immersed into two adjacent tanks of well-aerated seawater
kept under either simulated winter or summer conditions of temperature and
photoperiod. A variable speed pump continuously circulated water from the tank
into the respirometers.
Oxygen consumption was estimated by sealing the respirometers and measuring the decrease in dissolved oxygen concentrations over a period of 60-180 min, depending on the metabolic state of the animal (fed or not). Water samples of 0.3 ml were taken through the rubber cap of the respirometers with a plastic syringe at the beginning and the end of the experimental period, and dissolved oxygen concentrations were immediately measured using a Clark-type polarographic electrode (model 5300, Yellow Springs Instruments, Yellow Springs, OH, USA). Fish were first fasted for 5 days before being placed in the respirometry chambers to remove the influence of digestive state on metabolic rate. After the animals were left to acclimatize to the chambers for 2 days without food, prefeeding levels of oxygen consumption were measured twice a day over the following 3 days. For the fish acclimatized to simulated winter conditions, this meant that measurements were taken both in daylight and in the dark. Due to the longer photoperiod, all the measurements were taken in daylight for fish under simulated summer conditions.
Once prefeeding levels were established, the fish were fed a single satiating meal of live amphipods collected from the Beagle channel. In order to reproduce as closely as possible the influence of season on muscle growth, summer fish were fed a larger ration after preliminary observations showed that they had a greater appetite. Winter fish were fed an amount of amphipods corresponding to 10% of their body mass while summer fish ate an amount equivalent to 15% of their body mass. The fish consumed the prey readily in 15-20 min leaving only a few items, which indicates that the ration offered was close to satiation levels. The respirometers were sealed during feeding to prevent the prey from escaping, and uneaten food items were flushed out of the respirometer when water flow was reinstalled 30 min after food was offered. Postfeeding oxygen consumption was first measured 2 h after the meal was taken to ensure that the effect of prey capture on metabolic rate was minimal. Oxygen consumption was thereafter monitored regularly until it returned to prefeeding levels. The first few days after feeding, oxygen consumption was measured 2-3 times a day, but measurements were reduced to once per day as metabolic rate stabilised.
Myogenic progenitor cells
All 60 fish used were fasted during the last 12 days of the month's
acclimatization period to simulated winter or summer conditions. After this
initial period, each fish was weighed, individually placed in a cylindrical
250 ml plastic chamber (8.8 cm diameter) and left to acclimatize to the
chamber for 2 days. The 60 chambers were immersed in tanks of well-aerated
seawater kept under either simulated winter or summer conditions of
temperature and photoperiod.
The bottom of the chambers was filled with small rocks, and the top end was covered with a piece of dark mesh fabric held in place with an elastic band to allow water exchange with the holding tank. At the end of the acclimatization period, six winter and six summer fish were sampled for muscle tissue (controls) while the remaining animals were individually fed a satiating meal of live amphipods collected from the Beagle channel (10% of body mass for winter fish and 15% of body mass for summer fish). Based on the data obtained relative to the time course of the SDA (see Fig. 1), muscle tissue was sampled in six animals at 6 h, 30 h, 72 h and 165 h after feeding for the winter fish, and 2 h, 8 h, 48 h and 120 h after feeding for the summer fish. These time points corresponding to the beginning, the peak, the decline and the end of the SDA, respectively.
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Fish were killed by a sharp blow to the head. A transverse slice of the trunk (5 mm thick) was taken at a distance from the head equal to 0.7 of the fork length of the fish. The trunk slices were frozen on cork strips in isopentane cooled near its freezing point in liquid nitrogen, and stored at -20°C until sectioning. Frozen trunk slices (7 µm thick) were cut on a cryostat and mounted on glass slides coated with poly-L-lysine. The sections were air-dried and either processed for immunohistochemistry (see below) or stained with Sytox Green (Molecular Probes, Leiden, The Netherlands) for total myonuclei counts. When staining with Sytox Green, the sections were first washed twice in 2x SSC (300 mmol l-1 NaCl, 30 mmol l-1 sodium citrate, pH 7.0), then incubated for 5 min in the dark in a solution of Sytox Green diluted 1:300 in 2x SSC. Afterwards sections were washed four times in 2x SSC and mounted under coverslips with fluorescence mounting medium. Total numbers of myonuclei per cross-sectional area (i.e. all nuclei present in the muscle) were determined from these sections using the image generated by combining a series of images taken at every µm throughout the whole thickness of the section using a Bio-Rad 2000 confocal microscope (z-series).
Immunohistochemistry
Two different staining procedures were used: a single staining against
either MyoD or myogenin, and a double staining against both c-met and the
proliferating cell nuclear antigen (PCNA). PCNA is a cofactor to DNA
polymerase , whose levels correlate with DNA synthesis, reaching a
maximum during the S-phase (Bravo et al.,
1987
; Baserga,
1991
). Rabbit polyclonal antibodies obtained from Santa Cruz
Biotechnology Inc were used against MyoD (M-318), myogenin (M-225) and c-met
(m-met, SP260). The MyoD and myogenin antibodies react against a single band
in western blots of fish muscle nuclear extracts (C. Martin and I. A.
Johnston, unpublished data). A mouse monoclonal (clone PC10) antibody coupled
to a dextran polymer molecule itself joined to a number of horseradish
peroxidase molecules was obtained from Dako A/S (Dako EPOSTM, cat. no.
U7032) to stain for PCNA. For the single staining, the antibodies used against
MyoD and myogenin were diluted 1:20 in a solution containing 1% (v/v) Triton
X-100 and 1% (m/v) bovine serum albumin (BSA) in phosphate-buffered saline
(PBS). For the double staining, the antibody used against c-met was diluted
1:20 in the Dako EPOS solution containing the antibody against PCNA.
Sections were fixed in acetone for 10 min and then placed in a solution
containing 5% (v/v) normal goat's serum, 1% (v/v) Triton X-100 and 1% (m/v)
BSA in PBS for 15 min to rehydrate them and block non-specific binding sites.
Sections were subsequently washed 3x for 2 min in PBS and incubated
overnight at 4°C with the solutions containing either one (single
staining) or two (double staining) primary antibody. After three washes in
PBS, sections were incubated for 30 min with biotinylated goat anti-rabbit
secondary antibody (Sigma Chemicals, Poole, UK) diluted 1:20 in a solution
containing 1% (v/v) Triton X-100 and 1% (m/v) BSA in PBS. The sections were
again washed 3x 2 min in PBS and incubated for 30 min in a 1:20 dilution
of extraAvidin peroxidase (single staining) or extraAvidin alkaline
phosphatase (double staining; Sigma chemicals, Poole, UK) in 1% (v/v) Triton
X-100 and 1% (m/v) BSA in PBS. For the double staining, alkaline phosphatase
activity was developed first using a solution containing Fast Blue BB,
levamisole, naphtol-ASMX-phosphate and N,N-dimethylformamide in Tris
buffer, which gives a blue end product
(Van der Loos, 1999). For both
the double and single staining, peroxidase activity was developed using
3-amino-9-ethylcarbazole, which gives a red end product. Counts of the numbr
of immunoreactive cells were made from 30 fields of 0.01 mm2 for
each fish. For the double staining, it was noted whether the stained cells
were red (PCNA positive), blue (c-met positive) or purple (c-met and PCNA
positive).
Statistical analysis
For each molecular marker examined (MyoD, myogenin, PCNA, c-met), the
number of immunoreactive cells observed before feeding and at the different
sampling times after the meal were compared using a one-way analysis of
variance (ANOVA), followed by a Tukey test for multiple comparisons when a
significant difference was found between the groups. When normality and equal
variance could not be achieved by transformation of the data, the various
groups were compared by a non-parametric analysis of variance on ranks,
followed by a Dunn test for multiple comparisons when a significant difference
was found between the groups. The number of immunoreactive cells observed
before feeding was also compared between winter and summer fish using a
t-test or a MannWhitney Rank Sum test if normality and equal
variance could not be achieved.
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Results |
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Myogenic progenitor cells
Seasonal variations in MRFs expression
Total numbers of myonuclei did not significantly differ between fish
acclimatized to simulated summer and winter conditions of temperature and
photoperiod (winter: 887±30 myonuclei mm-2, summer:
886±55 myonuclei mm-2, mean ± S.E.M.). The density of
myogenic progenitor cells per muscle cross-sectional area (as illustrated by
the number of c-met positive cells) was also unaffected by acclimatization
conditions in fasting individuals (5.8% and 6.6% of total number of myonuclei,
respectively). However, the percentage of c-met positive cells expressing MyoD
was significantly (P<0.05) higher in summer (74%) than in winter
(40%) fish whereas the proportion of myogenic cells expressing myogenin was
greater in winter (71%) than in summer (33%) fish (Tables
1 and
2). The number of myogenic
progenitor cells expressing PCNA was independent of acclimatization state
(Tables 1 and
2).
|
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Response to feeding
In fish acclimatized to simulated winter conditions, the number of cells
immunopositive for PCNA and MyoD were significantly increased to 140% and 111%
of pre-feeding values 30 h after the meal, i.e. when oxygen consumption was
reaching its maximum (Table 1,
Fig. 1A). This increase in PCNA
and MyoD expression was followed by an increase in the number of c-met (75%
and 85% of pre-feeding values) and myogenin (97% and 77% of pre-feeding
values) positive cells 72 and 165 h after feeding, respectively, which denotes
a net production of myogenic progenitor cells
(Table 1). MyoD expression was
back to prefeeding levels when the last samples were taken 165 h after
feeding, but PCNA expression still remained elevated
(Table 1).
As observed in winter fish, feeding also resulted in an increase in the number of cells expressing PCNA and MyoD in H. bispinis acclimatized to simulated summer conditions (Table 2). This elevation in the number of PCNA (88% of pre-feeding values) and MyoD (51% of pre-feeding values) positive cells was observed 48 h after the meal but was no longer detectable 120 h after feeding, when oxygen consumption was back to prefeeding levels (Table 2, Fig. 1B). As for winter animals, the number of c-met positive cells also increased towards the end of the SDA (74% of pre-feeding values, Table 2). However, in this case, no significant increase in the number of cells expressing myogenin was found, although slightly higher numbers were measured 120 h after the meal (Table 2).
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Discussion |
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Although it is the first time, to our knowledge, that food intake has been
directly linked with a stimulation of myogenic progenitor cell proliferation
in vivo, this finding is not unexpected. Protein intake is known to
increase growth hormone release in fish and growth hormone is a powerful
stimulator of IGF-1 expression, which is, in turn, known to stimulate myogenic
progenitor cells proliferation (Mommsen,
2001). In this context, the induction of myogenic cell
proliferation by feeding may be seen as part of a wider regulatory system,
orchestrated by the growth hormone, which aims at promoting growth when energy
resources are available.
The number of myogenic cells generated in response to feeding did not
appear to be directly related with temperature or the amount of food eaten
since cell density approximately doubled in both groups of fish (Tables
1 and
2). Low temperatures could have
been expected to extend the time needed for the cells to divide
(Lloyd and Kippert, 1987;
Vinogradov, 1999
), but the low
frequency of sampling used does not permit a conclusion to be drawn about the
time course of the cell proliferation. The main difference between the
responses to feeding of fish acclimatized to simulated winter and summer
conditions resided in the expression of myogenin, which was much less
pronounced in summer. This finding, along with the differences found in
prefeeding levels of MyoD and myogenin between the two groups of fish (Tables
1 and
2), points to an influence of
temperature and photoperiod in the control of cell differentiation.
Interestingly, the interval between the ingestion of the meal and the
appearance of new c-met positive cells observed in the present study was
shorter than the cell cycle durations previously estimated for the myogenic
progenitors of unfed H. bispinis at both summer and winter
temperatures. Indeed, whereas cell cycle durations of 150 and 81 h have been
found for the myogenic progenitors of H. bispinis acclimatized to 5
and 10°C (J. C. Brodeur, J. Calvo, A. Clarke and I. A. Johnston,
manuscript submitted for publication), the abundance of c-met positive cells
was already significantly increased 72 and 48 h after the meal at the same two
temperatures in the present study. This difference may either indicate that
cell cycle progression rate is increased by feeding, or that a proportion of
the activated cells were cells stopped at either one of the two cell-cycle
checkpoints and that they therefore could divide faster since they had already
progressed through part of the cell cycle
(Walworth, 2000). This last
possibility is in agreement with previous results on Notothenia
coriiceps, which suggested that the myogenic cells activated by feeding
were cells stopped at the G1/S checkpoint of the cell cycle
(Brodeur et al., 2002
).
If all the cells produced after a single meal in the present experiment
were incorporated into myofibres, the number of myonuclei would increase by
approximately 5% after each meal, which is considerable. A proportion of these
new cells may, however, be involved in nuclear turnover rather than fiber
growth, since studies in the rat have shown that, in adult stages, 2% of the
nuclei are replaced each week (Schmalbruch
and Lewis, 2000). Programmed cell death (apoptosis) may also be
involved in reducing the final number of myonuclei produced as it is a normal
developmental event in proliferating myoblasts and postmitotic myofibres
(Mampuru et al., 1996
).
Finally, it is also possible that the increase in myogenic cell number
observed after feeding illustrates the re-establishment of an actively
dividing population of myogenic progenitors that had been greatly reduced
during fasting. Such an interpretation would be consistent with the
observation of Fauconneau and Paboeuf
(2000
) that fasting suppresses
initial proliferation of the myogenic cells in vitro.
There are now several lines of evidence suggesting the existence of
distinct subpopulations of satellite cells in mammals
(Schultz, 1996;
Molnar et al., 1996
). The
picture emerging from the development of molecular markers for quiescent and
activated satellite cells suggests the presence of at least three distinct
subpopulations of cells with different levels of commitment
(Hawke and Garry, 2001
;
Qu-Petersen et al., 2002
).
However, much less is known about the different types of myogenic progenitors
present in fish. In salmon fry, 80% of the myogenic cells identified by c-met
staining also expressed MyoD and/or myogenin, suggesting a late state of
commitment (Johnston et al.,
2000
). A similarly high proportion of MyoD and/or myogenin
positive cells was also found in the present study (70%, Tables
1 and
2), and the number of activated
myogenic progenitors was furthermore shown to vary with temperature,
photoperiod and feeding. Although it is still an open question whether the
myogenic population supporting hypertrophic growth is the same as that able to
create new fibers, the results obtained in the present study can be considered
specific of hypertrophic growth since H. bispinis of the size studied
grows only by fibre hypertrophy.
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Acknowledgments |
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