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First published online May 26, 2006
Journal of Experimental Biology 209, 2249-2264 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02153
Review Article: Phenotypic Plasticity in Skeletal Muscle |
Environment and plasticity of myogenesis in teleost fish
Gatty Marine Laboratory, School of Biology, University of St Andrews, St Andrews, Fife, KY16 8LB, Scotland, UK
e-mail: iaj{at}st-andrews.ac.uk
Accepted 7 February 2006
Summary
Embryonic development in teleosts is profoundly affected by environmental conditions, particularly temperature and dissolved oxygen concentrations. The environment determines the rate of myogenesis, the composition of sub-cellular organelles, patterns of gene expression, and the number and size distribution of muscle fibres. During the embryonic and larval stages, muscle plasticity to the environment is usually irreversible due to the rapid pace of ontogenetic change. In the early life stages, muscle can affect locomotory performance and behaviour, with potential consequences for larval survival. Postembryonic growth involves myogenic progenitor cells (MPCs) that originate in the embryo. The embryonic temperature regime can have long-term consequences for the growth of skeletal muscle in some species, including the duration and intensity of myotube formation in adult stages. In juvenile and adult fish, abiotic (temperature, day-length, water flow characteristics, hypoxia) and biotic factors (food availability, parasitic infection) have complex effects on the signalling pathways regulating the proliferation and differentiation of MPCs, protein synthesis and degradation, and patterns of gene expression. The phenotypic responses observed to the environment frequently vary during ontogeny and are integrated with endogenous physiological rhythms, particularly sexual maturation. Studies with model teleosts provide opportunities for investigating the underlying genetic mechanisms of muscle plasticity that can subsequently be applied to non-model species of more ecological or commercial interest.
Key words: temperature, oxygen, myotomal muscle, environmental genomics, phenotypic plasticity, ectotherm, developmental plasticity, skeletal muscle
Introduction
Teleost fish are found in fresh, brackish and marine habits that often show
complex temporal-spatial variations in temperature, salinity, oxygen content,
pH, light availability and water flow. Individually and in combination,
environmental inputs affect all physiological systems including the skeletal
musculature. Environment can have direct effects on the skeletal muscle, as
with temperature and flow regime, or act via other physiological
systems, as is the case with a variation in the chemical composition of the
external medium (Fig. 1). Thus
the gills detect changes in the chemical composition of the water (oxygen, pH,
salinity, etc.) whereas altered day-length and/or light intensity are sensed
via the retina and pineal gland
(Fig. 1). The brain integrates
all environmental inputs and modifies the outputs of the nervous, endocrine
and cardiovascular systems in ways that alter phenotype and muscle function
(Fig. 1). Resulting changes in
behaviour may lead the fish to seek a new environment and/or over time result
in muscle plasticity. Phenotypic plasticity can be defined as the ability of
an organism to respond to an environmental input with a change of form, state,
movement or rate of activity
(West-Eberhard, 2003
). The
range of phenotypes that are expressed in response to environmental variation
can be conveniently considered in terms of a reaction norm (Schlichting and
Pigliucci, 1998). Muscle plasticity often involves structural changes in
cellular organelles (Johnston and
Maitland, 1980; Tyler and
Sidell, 1984; Penney and
Goldspink, 1980) or supporting structures such as capillaries
(Johnston, 1982;
Egginton and Sidell, 1989),
and typically requires several weeks for a new steady state to be reached.
|
),
both of which may modify phenotypic responses to environmental change and
associated outputs (locomotion, metabolism and growth)
(Fig. 1). Muscle plasticity and
its consequences vary with the directional signal of environmental change. For
example, in the threespine stickleback (Gasterosteus aculeatus) the
effect of temperature acclimation on fast-start performance was shown to
differ between the spring and the autumn when the day length was increasing
and decreasing, respectively (Guderley et
al., 2001).
Two broad categories of muscle plasticity can be distinguished on the basis
of the reversibility of the response (Fig.
2). During the embryonic and larval stages, muscle plasticity to
the environment is usually irreversible due to the rapid pace of ontogenetic
change. Following the establishment of the adult body plan, seasonal
acclimatization to environmental change produces completely reversible changes
in muscle phenotype. An exception is probably myogenesis because this
continues well into adult life. Acclimatization responses require a stable
environmental cue, may develop during ontogeny
(Cole and Johnston, 2001), and
are more pronounced in species from environments with highly seasonal climatic
inputs (Johnston and Temple,
2002).
|
). Muscle plasticity is acquired during ontogeny as
adult stages migrate offshore to deeper water where the temperature is more
stable over short time periods, but is markedly different between summer
(
15°C) and winter (5°C)
(Johnston et al., 1995;
Temple and Johnston, 1998).
Maximum swimming performance at 15°C was improved under summer conditions
whereas performance at 5°C was relatively little affected by acclimation.
Tested at the maximum summer temperature of 20°C, length-specific speed
and acceleration were 110% higher and 55% higher, respectively, in 15°C-
than 5°C-acclimated individuals
(Temple and Johnston, 1998),
reflecting an increase in the maximum shortening speed and power output of
fast muscle fibres (Johnston et al.,
1995).
Following sexual maturation, seasonal acclimatization responses are closely
coupled to reproductive cycles. In common with other species from the northern
hemisphere, short-horn sculpin spawn in the early spring, but build up their
gonads during the winter. In part, the materials for gonad development are
obtained by mobilising energy reserves from the liver, adipose tissue and
myotomal muscle, producing phenotypic changes that parallel starvation
(Love, 1980). The eggs
comprised 39% of body mass prior to spawning, producing increased drag forces
on the body and stretching of fast muscle fibres in abdominal myotomes (James
and Johnston, 1988). Compared to fish outside the spawning season the fast
muscle fibres of gravid individuals had a lower resting membrane potential
(Altringham and Johnston, 1988)
and a faster maximum contraction speed, but a lower power output, as
determined from the force–velocity relationship
(James and Johnston, 1998).
These physiological changes plus the added mass of eggs contributed to a
decreased escape performance in gravid fish
(James and Johnston,
1998).
The molecular mechanisms of plasticity of contractile properties with
temperature acclimation have been extensively studied in the cyprinid species,
common carp (Cyprinus carpio) and goldfish (Carassius
carassius). These species show a classical trade-off in swimming
performance between seasonal high and low temperatures with acclimatization
(Fry and Hart, 1948;
Johnson and Bennett, 1995),
involving changes in myofibrillar ATPase activity
(Johnston et al., 1975a;
Johnson and Bennett, 1995),
muscle shorting speed (Johnston et al.,
1985), twitch duration
(Fleming et al., 1990) and
power output (Wakeling et al.,
2000). Microarray studies indicate hundreds of protein targets
(Gracey et al., 2004),
including the class II myosins (Imai et
al., 1997). A complex pattern of myosin heavy chain expression has
been found in fast muscle, with various embryonic, slow- and fast-type
isoforms being expressed at some acclimation temperatures, but not others
(Nihei et al., 2006).
There are many barriers to gaining a deep understanding of the mechanisms
of muscle plasticity induced by environmental change. These undoubtedly
include the complexity of environmental interactions observed in nature, which
are often difficult to replicate in an experimental setting. Indeed, the
overwhelming majority of published studies have involved either seasonal
acclimatization in wild fish (with only a few of the relevant abiotic or
ecological factors recorded) or laboratory experiments, in which a single
environmental variable has been manipulated with others held constant or
unrecognised. The complexity of genotype–environmental interactions and
the poorly characterised genetic background of most study organisms represent
another set of challenges. Reproductive isolation of populations along a
latitudinal gradient of distribution or between lakes that have become
separated over time often leads to genetic differentiation and local
adaptation between populations (Schluter,
1996; Quinn et al.,
2000; Penn et al.,
2002). Population level differentiation at many genetic loci and
the complexity of environment–genotype interactions can lead to a poor
appreciation, definition and/or control of critical variables affecting muscle
plasticity.
There have been recent reviews on temperature acclimation responses and
locomotory behaviour (Johnston and Temple,
2002) and there is a large literature on the effects of hypoxia on
muscle metabolism in fish (e.g. Van den
Thillart, 1982; Gracey et al.,
2001). The focus of this short review will therefore be on the
plasticity of myogenesis to environmental change. There is an extensive
literature on the regulation of myogenesis in mammals, which might be expected
to be a good starting point for unravelling the corresponding mechanisms in
teleosts, particularly given the conservative features of vertebrate genomes.
However, there are several reasons for exercising caution in extrapolating
between vertebrate models. Firstly, myogenesis has some unique features in
teleosts compared to amniotes: these include the earlier stage at which the
fate of muscle cells is specified, the presence of adaxial cells, and the
production of myotubes throughout much of ontogeny
(Currie and Ingham, 2001;
Rowlerson and Veggetti,
2001). Fish also have less control over their internal environment
than amniotes and in nature are subject to marked seasonal fluctuations in
food supply with conditions for growth varying throughout the year. These
factors are likely to have profound consequences for the genetic mechanisms
regulating myogenesis.
Common mechanisms of vertebrate myogenesis?
The fundamental events in myogenesis that are common to all vertebrates are
the specification of stem cells to a myogenic lineage (myoblasts),
proliferation, cell cycle exit, differentiation, migration and fusion
(Fig. 2). The transcription
factors (myogenic regulatory factors, MRFs) responsible for committing
mesodermal cells to the muscle lineage (myoD and myf-5) and those involved in
initiating and maintaining the muscle differentiation programme (myogenin,
MRF4, MEF2 gene family members) are highly conserved in teleosts and amniotes
(for a review, see Rescan,
2001). In mammals, the activities of MRFs are controlled by both
negative (Id proteins, LIM proteins, Twist, I-mf proteins) and positive
(CBP/p300, MEF2 proteins) regulatory factors (for reviews, see
Buckingham, 2001;
Brand-Saberi, 2005).
Myoblast to myoblast fusion creates short myotubes that can be extended by
the absorption of additional myoblasts [the mammal literature has recently
been reviewed (Horsley and Pavlath,
2004)] (Fig. 2).
Muscle fibres also absorb myoblasts (myoblast-muscle fibre fusion) as they
increase in diameter and length during growth
(Fig. 2). A large number of
factors that potentially regulate myoblast fusion have been identified in
mammals, including caveolin-3, IL-4, PGF2
, calpain, calpastatin,
NFATC2, and the transmembrane semaphorin Sema4c
(Horsley and Pavlath, 2004;
Ko et al., 2005). The binding
of prostaglandin F2 to its receptor produces an increase in
intracellular calcium concentration, which activates the transcription factor
NFATC2 required for nuclear accretion
(Horsley and Pavlath, 2003).
The factors regulating myoblast fusion and nuclear accretion in teleost fish
have not yet been investigated, although orthologues of the key regulatory
molecules found in mammals can be identified in fish genomes.
In mammals, insulin-like growth factor-1 (IGF-1) and the autocrine actions
of IGF-II have major roles in regulating muscle mass and fibre size
(Barton-Davies et al., 1999).
IGF-I activates the Akt-mTor signalling pathway, which has a central role in
regulating protein synthesis and degradation in muscle
(Stitt et al., 2004;
Ohanna et al., 2005). The
autocrine IGF-II transcription required for skeletal myocyte differentiation
is regulated by mTOR and the availability of amino acids
(Erby et al., 2003). Thus the
mTOR–IGF axis provides a molecular link between nutritional levels and
protein synthesis leading to muscle fibre hypertrophy. Growth in fish is also
primarily controlled by the availability of growth hormone, IGF-I and IGF-II
and their respective receptors, and IGF-binding proteins
(Moriyama et al., 2000;
Castillo et al., 2002;
Castillo et al., 2004;
Peterson et al., 2004). In
mammals, IGF-II mRNA decreased during postnatal development
(Daughaday and Rotwein, 1989).
In contrast, IGF-II mRNA was reported at higher levels than
IGF-1 mRNA in several tissues of adult fish, including muscle and
liver (Gabillard et al., 2003;
Peterson et al., 2004).
Myostatin-II (MSTN-II) is a negative regulator of muscle mass in prenatal
mammals and belongs to the transforming growth factor beta (TGF-ß)
superfamily of signalling molecules. Myostatin-null mice and cattle with
genetic mutations in MSTN genes show dramatic increases in skeletal
muscle mass with increased fibre hyperplasia and hypertrophy
(McPherron et al., 1997). It
has been reported that myostatin inhibits myoblast proliferation by
upregulating p21Waf1,Cip1 and downregulating cyclin-E-Cdk2 activity
(Thomas et al., 2000) and
activates myoblast differentiation by downregulating the expression of MyoD,
Myf5 and Pax-3 (Yang et al.,
2005). Transgenic zebrafish that overexpressed MST-II showed a
small but significant increase in fibre number relative to the wild type, but
no change in fibre size, consistent with some role for myostatin as an
inhibitor of embryonic hyperplasia (Xu et
al., 2003). The role of MSTN in postembryonic growth is less
clear. Administration of exogenous myostatin to adult mice induces muscle and
fat loss analogous to human cachexia syndromes
(Zimmers et al., 2002). The
rainbow trout genome contains two paralogues of myostatin, TMyostatin 1 and
TMyostatin 2 (Rescan et al.,
2001). TMST 1 is ubiquitously expressed in all tissues whereas
TMST 2 is specific to the brain and skeletal muscle, where it starts to be
expressed in the free-swimming stages. The muscle wasting that accompanies
sexual maturation produced no change in TMST-1 mRNA transcript levels
but was associated with a significant decease in TMST 2 expression in
both slow and fast muscle (Rescan et al.,
2001).
Myotomal muscle in teleost fish
Fish swim using a combination of paired and unpaired fins and rhythmic
contractions of the segmentally arranged myotomes. Embryonic myotomes have a
simple block shape in two-dimensional projections, which transforms to a
V-shape in a rostral to caudal progression. In zebrafish, the adult myotome
shape is not attained until 6 weeks after hatching
(Raamsdonk et al., 1974). In
adult stages, the myotomes have a W-shape in two dimensions, but consist of a
series of overlapping cones in three dimensions
(Van Leeuwen, 1999). In
larval common carp, longitudinal reconstructions revealed that six myotomes
were sectioned at different levels when preparing a transverse section through
the trunk (Alami-Durante et al.,
2000). Different muscle fibre types are organised into discrete
layers within the myotome, greatly facilitating molecular and physiological
studies and their interpretation. There is a superficial layer of aerobic slow
twitch muscle that powers sustained activity
(Johnston et al., 1977;
Rome et al., 1984). Fast
muscle fibres, which comprise the bulk of the myotome, develop 3–5 times
higher power outputs than the superficial slow muscle fibres at higher
tail-beat frequencies (Altringham and
Johnston, 1990), reflecting their role in providing the power
required for escape responses and predation behaviour. Intermediate muscle
fibre types, where present, have relatively high aerobic and glycolytic
capacities and intermediate contractile properties and recruitment patterns to
slow and fast muscle fibres (Johnston et
al., 1977; Mascerello et al., 1995). The shape, muscle mass and
structural components of myotomes and their dynamic interactions vary along
the length of the trunk, reflecting their particular roles in generating
swimming movements (Davies et al.,
1995; Thys et al.,
1998; Coughlin et al.,
2005).
Phases of myogenesis
The main phases of myogenesis in teleosts and their relative importance to muscle fibre production are illustrated in Fig. 3.
|
).
Somites condense from the paraxial mesoderm and segment in a rostral to caudal
progression. Cell labelling and fate studies have shown the paraxial mesoderm
originates from a specific region of the embryo identifiable just prior to
gastrulation (Kimmel et al.,
1990). MyoD expression starts in two triangular fields on either
side of the forming axial mid-line
(Weinberg et al., 1996). A
4x5 array of relatively large myoD expressing cuboidal cells can be
identified on either side of the notochord prior to segmentation
(Kimmel et al., 1995;
Weinberg et al., 1996;
Devoto et al., 1996). Adaxial
cells are surrounded by more numerous and irregularly shaped cells of the
presomitic mesoderm. A sub-set of these adaxial cells, the muscle pioneers,
elongate to span the somite width, differentiate and develop striations
(Felsenfeld et al., 1991).
Myotubes derived from adaxial cells migrate through the myotome from their
position at the notochord to form a superficial layer of slow muscle fibres
(Devoto et al., 1996).
Glycoproteins from the hedgehog family that are secreted from the notochord
are thought to be responsible for slow muscle fibre specification
(Devoto et al., 1996;
Blagden et al., 1997). Sonic
hedgehog sense mRNA injected into eggs results in the activation of myoD
expression throughout the presomitic paraxial mesoderm and its subsequent
differentiation into slow muscle fibres
(Barresi et al., 2000).
Mutations in the u-boot (ubo) gene cause the adaxial cells
to abort their developmental programme, fail to migrate or express the slow
fibre marker Prox 1 and adopt the fast muscle phenotype. The blocking of
hedgehog signalling has been shown to disrupt the elongation of fast muscle
fibres (Henry and Amacher,
2004). It has been suggested the medial to lateral migration of
slow muscle fibres provides a morphogenetic signal that patterns fast muscle
fibre elongation (Henry and Amacher,
2004). In rainbow trout, muscle-specific genes were shown to be
expressed at approximately the 25-somite stage in the medial part of the
somite where the slow muscle precursors are initially located, proceeding down
the trunk in a rostral to caudal wave
(Chauvigné et al.,
2005). At the 30-somite stage the adaxial cells started to express
the slow myosin light chain and the Lim protein SLIM1/FHL1. The adaxial cells
migrated through the somite to a superficial position as described in the
zebrafish. Double in situ hybridisations revealed a common myogenic
programme during the early stages of myogenesis with co-expression of slow and
fast isoforms throughout the myotome. Later during embryogenesis the
inappropriate isoforms for particular fibre types were downregulated and other
genes such as parvalbumins started to be expressed
(Chauvigné et al.,
2005).
Stratified hyperplasia
The number of embryonic slow muscle fibres in the initial wave of
myogenesis is not sufficient to account for all those present at hatching
(Barresi et al., 2001).
Additional slow muscle myotubes are formed in the late embryo in discrete
germinal zones at the lateral margins of the myotome
(Barresi et al., 2001); a
process termed stratified hyperplasia
(Rowlerson and Veggetti,
2001). Normal striated hyperplasia of slow muscle is observed in
the zebrafish slow-muscle-omitted gene mutant (smu–/–), which is
deficient in Shh signalling. Thus stratified hyperplasia of slow muscle fibres
in late embryonic stages is not dependent on the scaffold of adaxial
cell-derived slow fibres formed earlier in development. Stratified hyperplasia
is the main mechanism responsible for the increase in the number of slow
muscle fibres after hatching (Veggetti et
al., 1990; Rowlerson et al.,
1995; Barresi et al.,
2001). The formation of slow muscle myotubes from germinal zones
apparently continues throughout life. For example, in the Arctic charr
(Salvelinus alpinus) slow fibre number was found to increase with
body length, scaling to body mass0.45
(Johnston et al., 2004).
Labelling experiments with the thymidine analogue
5'-2-bromo-deoxyuridine (BrdU) have also identified germinal zones of
myotube formation in the fast muscle that become exhausted in the late larval
or early juvenile stage, e.g. in sea bream Sparus auratus
(Rowlerson et al., 1995),
Atlantic herring Clupea harengus
(Johnston, 1993; Johnston et
al., 1998), Atlantic cod Gadus morhua
(Galloway et al., 1999).
Stratified hyperplasia is the only postembryonic mechanism of fast muscle
myotube production in certain families (Harpagiferidae, Channichthyidae) of
Antarctic notothenioids that show an associated dramatic reduction in the
number of fast muscle fibres and a corresponding increase in fibre size
(Johnston et al., 2003a).
Myogenesis of intermediate muscle has been little studied but probably occurs
by stratified hyperplasia from germinal zones adjacent to the slow muscle
layer (Mascarello et al.,
1995; Rowlerson and Veggetti,
2001).
Mosaic hyperplasia
Mosaic hyperplasia is so-called because in this final phase of myogenesis
myotubes form on the surface of fast muscle fibres throughout the myotomal
cones, giving rise to a mosaic of fibre diameters. The immature fibres
transiently express developmentally regulated isoforms of myosin heavy chains
(Enion et al., 1995) and often
have a higher content of glycogen and mitochondria than the more mature muscle
fibres (Johnston et al.,
1975b). Mosaic hyperplasia is important in species with a
prolonged larval phase, such as Atlantic herring
(Johnston et al., 1998a). It
is the main mechanisms for expanding fast fibre number in the juvenile and
adult stages of the vast majority of species, continuing until approximately
40% of the maximum fish length
(Weatherley et al., 1988).
Subsequent growth exclusively involves an increase in the length and diameter
(hypertrophy) of the fibres. Thus postembryonic growth is achieved through an
expansion in diameter of the immature muscle fibres. The maximum fibre
diameter, on the other hand, is set by diffusional constraints that vary with
body mass, activity patterns and metabolic demand
(Johnston et al., 2003a;
Johnston et al., 2004). All
other things being equal, as body size increases and mass-specific metabolism
declines as a function of body mass–0.25, the relaxation of
diffusional constraints allows the maximum fibre diameter
(Dmax) to increase. For sedentary species living at very
low temperatures Dmax continues to increase with body
length until the maximum body length, resulting in giant fibres of
500–600 µm diameter in some Antarctic teleosts
(Johnston et al., 2003a). In
warmer water and/or more active species Dmax reaches a
limiting value at much less than the maximum body length
(Johnston et al., 2003b)
(I.A.J., unpublished results).
Individual muscle fibres absorb additional myoblasts from the proliferating
myogenic precursor cell (MPC) population as fibre diameter and length increase
(Fig. 2). For salmonids the
number of myonuclei increases as an approximately linear function of fibre
diameter (Johnston et al.,
2003b; Johnston et al.,
2004). Very little is known about the genetic mechanisms
regulating the formation of myotubes in fast muscle. Injury to the muscle can
result in a new wave of myotube production to repair the damage even if muscle
recruitment has stopped (Rowlerson et
al., 1997). This suggests some mechanism for inhibiting myotube
formation in undamaged muscle in fish that are greater than 40% of their
maximum length. We have used suppression subtractive hybridisation (SSH) in
the model species, the tiger pufferfish (Takifugu rubripes), to
identify genes that were differentially expressed between myotube (+) and
myotube (–) growth stages (Fernandes et al., 2005). The different
patterns of myotube formation in slow and fast muscles, and gene expression
patterns in non-muscle tissues, were used to distinguish between potential
candidate genes involved in myotube formation and genes that changed with body
size but were not related to myotube formation. Four strong candidates with
appropriate tissue-specific expression patterns were identified that were
5–25-times upregulated concomitant with the inhibition of myotube
formation in fast muscle (Fernandes et al., 2005). The expression of
orthologues of these putative myotube inhibitory genes was investigated in the
fast muscle of the zebrafish in relation to the cessation of muscle fibre
recruitment (H. T. Lee and I. A. Johnston, manuscript submitted for
publication). Two of the candidates were significantly upregulated at the body
length where myotube production stopped, consistent with them having a role in
the control of fibre recruitment. Candidate 1 (GenBank Accession No. CK829660
Takifugu rubripes) had nine exons predicted on Ensembl with conserved
B302, fibronectin and SPRY receptor domains, suggesting it might be involved
in the regulation of transcription and/or cell migration, differentiation and
adhesion (Dickson et al.,
1990). The Ensembl-predicted transcript structure for candidate 2
(GenBank Accession No. CK829660 Takifugu rubripes) comprised five
exons that translated into a 483-residue protein with conserved POZ/BTB and
BTB/kelch domains (Fernandes et al., 2005).
Plasticity of myogenesis in early life stages
Temperature
Prior to hatching there is no scope for fish embryos to select a new
environment and thus they are at the mercy of ambient conditions of
temperature, oxygen, salinity, pH, etc. Adverse environmental conditions in
nature can be the cause of significant embryonic mortality
(Laprise and Pepin, 1995).
Sub-lethal environmental stress impacts on all aspects of development,
including myogenesis, with potential consequences for the morphology,
physiology, behaviour and survival of the hatched larvae.
At hatching, teleost myotomes usually have a single superficial layer of
slow muscle fibres surrounding an inner core of rapidly differentiating
embryonic fast muscle fibres (Fig.
4A,B). Both of these `embryonic muscle fibre types' have a higher
volume density of mitochondria (Vieira
and Johnston, 1992) and a less well-developed anaerobic capacity
than the corresponding muscle fibre types in juveniles
(El-Fiky and Wieser, 1988). In
Atlantic herring (Clupea harengus), the mitochondrial content in
embryonic slow and fast muscle fibres increased with increasing rearing
temperature to the hatching stage (Fig.
4C), whereas the myofibrillar volume density decreased
(Vieira and Johnston, 1992).
In contrast, cold acclimation in the juvenile stages of several species
resulted in an expansion of the mitochondrial compartment
(Johnston and Maitland, 1980;
Egginton and Sidell, 1989),
presumably to compensate for the effects of low temperature on diffusion and
ATP synthesis rates. Embryonic temperature regime affects the relative timing
of muscle differentiation in herring larvae, including the body lengths at
which developmental-stage specific isoforms of the various myofibrillar
isoforms and adult patterns of motor innervation first appeared
(Vieira and Johnston, 1992;
Johnston et al., 1997; Johnston et al.,
1998b). Interestingly, the embryonic temperature continued to
exert an effect on the relative timing of development even after temperature
groups were transferred to a common temperature
(Johnston et al., 2001). In
herring, such heterochronies in the development of the paired and unpaired
fins and associated fin ray musculature were found to affect escape swimming
performance, and may influence larval mortality
(Johnston et al., 2001).
|
; Lopez-Albors et al.,
2003), or fewer, larger diameter fibres, e.g. Atlantic salmon
Salmo salar (Stickland et al.,
1988), turbot Scophthalmus maximus
(Calvo and Johnston, 1992),
whitefish (Hanel et al., 1996)
and plaice Pleuronectes platessa (Brookes and Johnston, 1993), or
more fibres of smaller diameter, e.g. Atlantic herring Clupea
harengus (Vieira and Johnston,
1992) and Atlantic cod Gadus morhua
(Hall and Johnston, 2003). The
number of slow muscle fibres at hatching is also sensitive to rearing
temperature although the response observed may differ from that in fast muscle
(Stoiber et al., 2002;
Hall and Johnston, 2003;
Johnston et al., 2000).
Population level variations in the responses have been documented for Atlantic
herring spawning at different times of the year
(Johnston et al., 1998a),
reproductively isolated Atlantic salmon from different parts of a river
catchment (Johnston et al.,
2000), and between sea bass from the NE Atlantic and Mediterranean
sea (Ayala et al., 2001).
Clearly, the effects of temperature on the first two phases of myogenesis are
complex and depend on the precise characteristics of the temperature regime
(Stoiber et al., 2002).
The various patterns of muscle cellularity described cannot be interpreted
without a detailed knowledge of how the norms of reaction for myotube
formation change with respect to each phase of myogenesis.
Fig. 5 illustrates how it is
entirely possible to produce different patterns of muscle cellularity
depending on the temperatures and time of sampling chosen for study. Thus such
descriptive studies of myogenesis are of most value if the phenotypes are
catalogued over the entire temperature range for development at multiple
stages of ontogeny. The mechanisms whereby temperature can alter the number of
muscle fibres is perhaps of more interest. Changes in the relative timing of
the transcriptional networks, extracellular signalling molecules and/or
intracellular growth factors regulating any of the steps in embryonic
myogenesis and stratified hyperplasia have the potential to alter the number
of muscle fibres present in embryos at hatch or first feeding. In general,
factors that promote myoblast proliferation at the expense of cell cycle exit
and differentiation would be expected to result in an increase in fibre number
during the early phases of myogenesis. It is likely that heterochronies in
numerous molecular species underlie changes in muscle cellularity with
temperature. In Atlantic cod, closure of the blastopore occurred later with
respect to segmentation at higher temperatures, at the 3-somite, 10-somite and
12-somite stages at 4, 7 and 10°C, respectively
(Hall and Johnston, 2003). It
was suggested that this change in the relative timing of epiboly might alter
the time window for myoblast proliferation and/or their exposure to inductive
signals (Hall and Johnston,
2003).
|
;
Temple et al., 2001). MyoG
expression was retarded with respect to somite stage in rainbow trout embryos
reared at 4°C compared to 12°C, consistent with a change in the
relative timing of differentiation (Xie
et al., 2001). At the eyed stage, northern analysis indicated
greater myosin heavy chain expression, but lower MyoG expression in the caudal
myotomes at high than low temperatures, consistent with a more advanced state
of muscle differentiation. Examination of a broader range of temperatures
established that there was an optimal temperature for both MRF and myosin
heavy chain expression with respect to developmental stage
(Wilkes et al., 2001). In
contrast, in the model pufferfish Takifugu rubripes the relative
timing of myoG expression was similar at 15, 18 and 21°C
(Fig. 6). However,
myoG were significantly higher at 21°C than 15°C
(Fernandes et al., 2006).
Changes in myoG and other factors have the potential to alter the timing of
muscle differentiation and hence the time window for myoblast proliferation.
However, given the redundancy of the transcriptional networks regulating
myogenesis it is necessary to study the expression of many factors, preferably
at the protein level, and to conduct functional (knockdown/over-expression)
studies to establish the mechanisms.
|
). It has been
suggested that at high temperatures during the later stages of embryogenesis
the metabolic requirements of the developing embryo may not be matched by the
supply of oxygen across the chorion, resulting in a physiological hypoxia
(Matschak et al., 1995). The
number of fast muscle fibres in Atlantic salmon (Salmo salar) embryos
at hatch was found to be 15% higher at 6.5°C than 11°C in intact eggs,
but was independent of temperature in dechorionated eggs
(Matschak et al., 1995). The
average fibre size was 30% greater at high temperatures in intact eggs,
whereas average fibre size was greater at low than high temperatures in
dechorionated eggs. In subsequent experiments, the effects of varying oxygen
(50%, 100% and 150%) air saturation on fast fibre number, fibre size and
myonuclear density was investigated in intact and dechorionated embryos
(Matschak et al., 1997).
Whilst lowering oxygen availability had some effects on the measured
parameters, the results were not consistent with hypoxia being the main
explanation for temperature effects on muscle cellularity, although it is
probably a contributing factor. Hypoxia is also unlikely to be a factor in the
development of small diameter pelagic eggs that hatch at a relatively early
stage of organogenesis.
Persistent effects of embryonic temperature on post-embryonic growth
Embryonic myogenesis and stratified hyperplasia together only account for
30% of the total fast muscle fibres recruited in zebrafish (H. T. Lee and I.
A. Johnston, manuscript submitted for publication), and less than 5% of the
maximum fibre number (FNmax) in Atlantic salmon
(Johnston et al., 2003b). Thus
environmental plasticity in the first two phases of myogenesis may affect
growth performance of the early life stages, but may not make much difference
to FNmax in adult stages. Myogenic progenitor cells
(MPCs), analogous to the satellite cells in adult mammalian muscle, are
responsible for postembryonic growth in teleosts. MPCs in teleosts are not
always found beneath the basal lamina of muscle fibres
(Veggetti et al., 1990;
Johnston et al., 2003b) and
should not be called satellite cells. Recently, using chick–quail
grafting experiments, the embryonic origin of the myogenic progenitor cells
involved in postembryonic growth in amniotes was shown to be the dorsal
compartment of the somite, the dermomyotome
(Gros et al., 2005). Although
the origin of myogenic progenitor cells in teleost embryos is unknown, changes
in the number formed in the embryo have the potential to produce persistent
effects on growth in adult stages.
Embryonic temperature was shown to produce long-lasting effects on
myogenesis in the larvae of spring-spawning Clyde herring (Clupea
harengus) (Fig. 7). This
spawning stock deposit their eggs in dense mats on the seabed in March at an
average temperature of 4.8°C to 10°C, depending on natural climatic
variation (Jones and Jeffs,
1991). The transparent larvae remain in the plankton until late
summer when they complete metamorphosis to the juvenile stage at 33–40
mm total length, by which time the sea temperature has risen to
12–16°C. The number of slow and fast muscle fibres recruited during
the larval phases was found to differ with temperature regime, more myotubes
being produced for a given body length at higher temperatures
(Fig. 7). In 1 day old larvae,
the density of myoblasts per myotomal cross-section, as identified from
electron micrographs, was around threefold higher at 8°C than 5°C, and
was intermediate at 12°C (Johnston,
1993). In a subsequent study, eggs from the same population were
incubated at either 5°C or 8°C until first feeding and then
transferred to a common ambient temperature
(Johnston et al., 1998a). The
effects of embryonic temperature regime remained imprinted on myogenesis in
later larval stages, resulting in a higher fibre number in the 5°C than
8°C groups.
|
Our working hypothesis to explain these results was that the temperature
regime prior to first feeding affected the number of undifferentiated
myoblasts and hence future growth potential. Manx herring spawn at higher sea
temperatures than Clyde herring, but the larvae experience cooling rather than
warming temperatures prior to metamorphosis the following spring. Larvae of
Manx herring were shorter at first feeding than Clyde herring and had a higher
temperature optimum for myogenesis and growth
(Johnston et al., 1998a).
Early thermal experience also affected the number of muscle fibres produced in
relation to larval length in Manx herring
(Johnston et al., 1998a).
Differences in the number of slow and fast muscle fibres in relation to body
length have also been reported for European pilchard larvae (Sardina
pilchardus) sampled in the field during different seasons of the year
(Catalán et al.,
2004).
Atlantic salmon (Salmo salar) spends from just over a year to up
to 5 years in freshwater prior to undergoing smoltification and migrating to
the sea. The temperature regime during freshwater life was found to affect
muscle fibre recruitment during the seawater stage of the life cycle
(Fig. 8A). The eggs from of a
minimum of 64 families from an inbred line of farmed salmon were incubated at
either cool ambient temperatures or in water heated by 1–3°C
relative to ambient. Fish were individually tagged and reared in the same
replicated sea cages under identical environmental conditions and diet.
Following smoltification and prior to transfer to sea cages, post-smolts were
on average almost twice as heavy in the heated (61.6 g) than in the ambient
(34.0 g) treatments, reflecting their greater growth opportunity: 4872
degree-days and 4281 degree-days, respectively. The seawater growth rate of
the heated group was lower than the ambient group, such that both groups
attained a mass of 3.7–3.9 kg after 450 days. The intensity of myotube
production was higher in the ambient than in heated groups, resulting in 22.4%
more fibres at the end of the fibre recruitment phase of growth
(Fig. 8A). The density of
myogenic progenitor cells, identified using an antibody to c-met, was also
higher in the ambient than heated treatments
(Johnston et al., 2003b).
Since the fish had been exposed to the same growth opportunity during seawater
life the observed differences in myogenesis must have been imprinted from the
freshwater stage, and may reflect an altered complement of myogenic progenitor
cells. Interestingly, the myonuclei content of isolated fast fibres was also
higher in the ambient than heated fish, e.g. 20.6% cm–1
higher in fibres of the maximum diameter
(Fig. 8B). Thus a higher number
of MPCs in the ambient than heated treatments may have resulted in a higher
intensity of fibre recruitment and a higher content of myonuclei. These
observations are consistent with a model in which there is a single population
of MPCs providing the founder myoblasts for myotube formation and the
myoblasts required for nuclear accretion, with their fate determined by local
signalling.
|
The signalling pathways regulating the proliferation and differentiation of
myogenic progenitor cells are sensitive to environmental factors and feeding.
In the sub-Antarctic plunderfish (Harpagifer bispinis), giving fasted
individuals a satiating meal was shown to result in an increase in the number
of cells in fast muscle expressing MyoD and PNCA (a cofactor to DNA polymerase
), and this was followed by an increased abundance of c-met and
myogenin expressing cells (Brodeur et al.,
2003). This sequence of events is consistent with an initial
activation of myogenic cell proliferation (expression of myoD/PCNA) followed
by the production of new cells (increase in c-met positive cells) and the
commitment of at least some of the progeny to differentiation (myogenin
expression).
Photoperiod is probably the most important proximal cue regulating the
seasonal timing of sexual maturation and somatic growth in salmonids,
resulting in modified output of the neuroendocrine system
(Hansen et al., 1992;
Bromage et al., 1993). The
rate of muscle fibre recruitment and hypertrophy in Atlantic salmon occurs at
reduced rates during the winter months, when appetite is reduced due to low
temperatures and short days (Johnston et
al., 2003c). In salmon farming, artificial lighting is often used
to boost growth during the winter months. We investigated myogenesis in the
fast muscle of Atlantic salmon during their first sea-winter, comparing groups
maintained under a natural photoperiod with fish subjected to continuous light
(Johnston et al., 2003c).
Lights were switched-on in duplicate sea cages on the 1st November, producing
a small but significant increase in the number of MPCs (identified using an
antibody to c-met) after 24–30 h relative to fish held in other sea
cages under natural day-length. This increase in MPCs was transient and peaked
at 70% of pre-light treatment levels after 40 days, corresponding to the
period when the natural day-length was still shortening. Growth rate and the
intensity of myotube production (Fig.
9A) were also significantly higher in the ambient than continuous
light groups during the first 40 days. However, once day-length started to
lengthen in the early spring the rate of muscle fibre recruitment was similar
in both groups. It was suggested that short days inhibited the proliferation
of MPCs and that this effect was counteracted by the continuous light
treatment, causing an increase in the number of times the myogenic progenitor
cells divided and/or a decrease in cell cycle time
(Johnston et al., 2003c).
Fibres isolated from fish from the continuous light cages also had a higher
content of myonuclei than fish at ambient photoperiod, 27% more nuclei in 150
µm diameter fibres (Fig.
9B). In this experiment photoperiod manipulation had presumably
altered the signalling pathways controlling myoblast proliferation, resulting
in proportional increases in myotube production and the myonuclear content of
fibres. Since this environmental intervention occurred just prior to the point
that fibre recruitment terminated it had a permanent effect on
FNmax, which was 23% higher in salmon from cages receiving
continuous light (881 000) than in the ambient photoperiod fish (717 000)
(Fig. 9A).
|
Myogenesis and exercise
Changing patterns of water flow that are maintained over long periods, e.g.
between wet and dry seasons in freshwater rivers, may also result in altered
patterns of swimming behaviour. The frequency and amplitude of tail-beats can
potentially modify the characteristics of intracellular calcium transients and
numerous downstream signalling pathways influencing muscle phenotype
(Fig. 2). Several weeks of
forced exercise training has been shown to result in a marked hypertrophy of
slow and fast muscles in a number of teleost species relative to non-exercised
groups, e.g. brook trout Salvelinus fontinalis
(Johnston and Moon, 1980),
Atlantic salmon (Totland et al.,
1987), dace Leuciscus cephalus
(Sänger, 1992), saithe
Pollachius virens (Walker and
Pull, 1973). In the common carp (Cyprinus carpio), forced
swimming is also a powerful stimulus for nuclear accretion, and resulted in a
higher myonuclear content in fibres from exercised than non-exercised fish
(Martin and Johnston,
2006).
In mammals, the calcineurin signalling pathway is thought to play a role in
regulating hypertrophic growth of skeletal muscle
(Musaro et al., 2001).
Prolonged increases in intracellular Ca2+ levels selectively
activate calcineurin, resulting in the dephosphorylation of nuclear factor of
T-cells 2 (NAFT2) and nuclear localisation of the calcineurin/NAFT2 complex
(Dolmetsch et al., 1997). The
latter event is thought to synergistically initiate a programme of gene
expression leading to fibre hypertrophy
(Musaro et al., 1999;
Semsarian et al., 1999).
However, exercise training leading to fast muscle hypertrophy in the rainbow
trout only resulted in a minor increase in calcineurin localisation in the
nucleus and total NFAT2 concentration decreased relative to tank-rested
controls with no nuclear translocation
(Martin and Johnston, 2005).
These results indicate differences in the response of this signalling pathway
to exercise stimuli between teleosts and mammals.
Potential ecological significance of environmental plasticity of myogenesis
Fast myotomal muscle comprises at least 60% of body mass in most teleosts
and is therefore quantitatively an important tissue in determining the overall
energy budget. Around 20–40% of routine energy consumption in teleosts
is thought to be involved in maintaining ionic homeostasis
(Jobling, 1994). Theoretically
the cost of counteracting passive ion movements across the muscle sarcolemma
would be expected to increase with the surface to volume ratio of the muscle
fibres, i.e. to increase with increasing fibre number. We have proposed an
optimal fibre number hypothesis, in which there is a trade-off between
requirements to avoid diffusional constraints whilst maximising fibre diameter
to minimise the energy costs of ionic homeostasis
(Johnston et al., 2003a). Thus
the maximum diameter of single fibres (Dmax) should be
small enough to avoid anoxia in the centre, but as large as possible to reduce
the maintenance costs of ion pumping across the membrane surface area, which
is higher for small than large diameter fibres. As expected, the maximum fibre
number is strongly correlated with body size for closely related species from
the same habitat (Johnston et al.,
2003a). Dwarfism is relatively common in land-locked salmonid
populations and has occurred since the last Ice-age 9000 years ago. Ecological
factors related to energetics and feeding are almost certainly responsible for
establishing dwarfism, as was documented for Lake Whitefish populations
(Trudel et al., 2001).
However, once established we hypothesised that physiological factors related
to scaling and the relatively high maintenance costs of supporting an excess
number of fibres for the body size would have acted as a powerful selective
force for reducing fibre number. In support of our hypothesis, dwarfism was
shown to be associated with a 50% reduction in FNmax in
the dwarf relative to large benthic Arctic charr morphs from Thingvallavatn,
Iceland (Johnston et al.,
2004) and a 75% reduction in FNmax in the
landlocked Bleke salmon relative to migratory populations
(Johnston et al., 2005).
Temperature and oxygen availability and activity will also influence the
`ideal' fibre number for a given body size. An extreme example is provided by
the core radiation of the Antarctic notothenioids. The relaxation of
diffusional constraints due to the low temperature and sluggish lifestyle of
these fishes resulted in a dramatic increase in maximum fibre diameter, and
corresponding reduction in FNmax
(Johnston et al., 2003a). The
metabolic and fitness consequences of changes in muscle cellularity have not
been addressed experimentally and this is an important area for future
research.
Conclusions and future perspectives
There are considerable advantages to studying muscle plasticity in model
fish species because of the extensive molecular and genetic resources
available and the large community of scientists that has evolved around them.
Four species have had their genomes sequenced to draft level (Danio rerio,
Takifugu rubripes, Tetraodon nigroviridis, Oryzius latipes). The Japanese
medaka (O. latipes) originates in a highly seasonal environment and
is therefore likely to be particularly useful for investigating
environment-induced muscle plasticity. Popular non-model species such as the
common carp (Cyprinus carpio) and goldfish (Carrasius
auratus) show enormous plasticity to environmental change. Focusing
effort on a relatively few non-model freshwater and marine species that show
significant environmental plasticity is probably the best way to increase
understanding of the underlying mechanisms, because it will facilitate the
establishment of a critical mass of molecular and genetic tools. In this
regard, cDNA libraries, Expressed Sequence Tags and DNA microarrays are
already available for the common carp, flounder (Platichthys flesus)
and Atlantic salmon (Salmo salar)
(Cossins and Crawford,
2005).
A good starting point for studies of muscle plasticity is the natural
history of the species of interest. Salmon and trout embryos are subject to
hypoxic conditions in the wild, which vary in severity in relation to water
flow characteristics and the degree of infiltration of oxygen depleted
groundwater. For example, in a study of 33 natural egg pockets of chum salmon
Oncorhyncus keta, dissolved oxygen levels were found to vary from 2
to 10 mg l–1 at the time of spawning and generally declined
during embryonic development (Peterson and
Quinn, 1996). The interactive effects of temperature and oxygen on
myogenesis during the development of salmonids in situ would be a
fruitful area for future research. It is important to record as much
information as possible about the genetic background and environmental history
of the population being studied. Field observations of environmental
parameters for the population under study can then be used to design
laboratory experiments in which one or more parameters are systematically
varied to investigate mechanisms.
Whether wild or captive populations are studied, there is considerable merit in adopting a systems biology approach in which environmental inputs, information from interacting physiological systems and muscle outputs are integrated and modelled with a quantitative framework. A systems approach may be equally useful for investigating the mechanisms and evolutionary significance of muscle plasticity. The acclimation of male mosquito fish to cool temperatures resulted in an increased swimming performance and mating success at cool relative to warm test temperatures (R. S. Wilson, E. Hammill and I. A. Johnston, manuscript submitted for publication). However, warm-acclimated fish were much more aggressive, presumably reflecting modified outputs of the neuroendocrine system. Under conditions of male-male competition, copulation success was highest for warm-acclimated individuals at all test temperatures (R. S. Wilson, E. Hammill and I. A. Johnston, manuscript submitted for publication). These experiments nicely illustrate that both the benefits of muscle plasticity are context-dependent and that the influence of the environment on other interacting physiological systems should also be considered.
Acknowledgments
The author's research was supported by grants and NER/A/S/2000/00558 and NER/T/S/2001/00250 from the Natural environmental Research Council of the United Kingdom. I am also grateful to Marguerite Abercromby for help with preparing the Figures and members of the Fish Muscle Research Group for useful discussions.
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