Temperature and the expression of seven muscle-specific protein genes during embryogenesis in the Atlantic cod Gadus morhua L.
1 Gatty Marine Laboratory, School of Biology, University of St Andrews,
Fife, KY16 8LB, UK
2 Division of Cell and Developmental Biology, MSI/WTB Complex, University of
Dundee, Dow Street, Dundee, DD1 5EH, UK
* Author for correspondence at present address: CSIRO Livestock Industries, Queensland Bioscience Precinct, 306 Carmody Road, St Lucia Australia (e-mail: tom.hall{at}csiro.au)
Accepted 10 June 2003
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Summary |
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Key words: Gadus morhua, temperature, development, muscle, in situ hybridization, cod, myofibril, MyoD, myosin, troponin, creatine kinase
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Introduction |
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The first aim of the present study was therefore to characterize and
investigate the expression of MSP genes required for myofibril assembly in the
Atlantic cod Gadus morhua L., including a full-length cDNA
of MyoD. Myogenic regulatory factors (MRFs) of the MyoD gene
family play a key role in lineage determination (MyoD, Myf-5) and in
initiating and stabilizing the differentiation programme (myogenin,
MRF4), in cooperation with other basic helixloophelix and
MADS box transcription factors (MEF-2 proteins) (for reviews, see
Sabourin and Rudnicki, 2000;
Pownall et al., 2002
;
Johnston et al., 2002
). The
promoter regions of most muscle-specific genes, including MyHC,
contain MyoD and MEF-2 recognition sites
(Giger et al., 2000
;
Wheeler et al., 1999
). It has
been shown that MyoD mRNA expression precedes the de novo
expression of MyHC IIB mRNA in rat fast muscle following hind limb
suspension (Wheeler et al.,
1999
). Other MSP cDNA clones characterized included
-actin, which forms the backbone of the thin filament in the
myofibril (Gordon et al.,
2000
); myosin heavy chain (MyHC), which is the
major component of the thick filament and the most abundant protein of the
sarcomere (Lu et al., 1999
);
muscle creatine kinase (CK-M), which plays a central role in
the catalysis of ADP to form high energy ATP
(Wallimann et al., 1992
), and
the three troponin (Tn) subunit genes troponin C (TnC),
troponin I, (TnI) and troponin T (TnT),
which are involved in calcium binding and signal transduction
(Filatov et al., 1999
).
Temperature is known to have major effects on early muscle development in
teleosts, altering the timing of myofibril assembly with respect to somite
stage (Atlantic herring, Johnston et al.,
1995), as well as the number and size of embryonic muscle fibres
in numerous species (Stickland et al.,
1988
; Vieira and Johnston,
1992
; Brooks and Johnston,
1993
; Gibson and Johnston,
1995
; Hanel et al.,
1996
; Matschak et al.,
1998
), including Atlantic cod, Gadus morhua
(Galloway et al., 1998
;
Hall and Johnston, 2003
).
During ontogeny, embryonic isoforms of the myofibrillar proteins are gradually
replaced by larval and adult isoforms, reflecting increases in body sizes and
associated changes in swimming behaviour
(Martinez et al., 1991
;
Chanoine et al., 1992
;
Mascarello et al., 1995
). The
relative timing of expression of developmentalstage specific isoforms varies
for different myofibrillar components and is altered by rearing temperature
(Johnston et al., 1997
,
1998
). For example, in
Atlantic herring Clupea harengus the appearance of adult isoforms of
myosin light chain 2, troponin T and troponin I occurred at longer body
lengths in larvae reared at 5°C compared to 12°C
(Johnston et al., 1997
).
In a recent study in rainbow trout Oncorhynchus mykiss it was
shown that MRF expression was delayed and prolonged at low compared to high
egg incubation temperatures, and it was suggested that this resulted in a
higher number of muscle fibres in hatched embryos, due to a longer period for
proliferation of the myogenic precursor cells prior to terminal
differentiation (Xie et al.,
2001). In contrast, the onset of MyoD and
myogenin expression relative to developmental stage was found to be
similar at a range of temperatures in the Atlantic herring
(Temple et al., 2001
).
The second aim of the present study was therefore to test the hypothesis
that differences in muscle cellularity with temperature in cod embryos
(Hall and Johnston, 2003) are
correlated with changes in the relative expression of MSP genes required for
myofibril assembly. Somite stage was used as a normalized index of development
at the different temperatures studied
(Hall and Johnston, 2003
;
Hall et al., 2003
).
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Materials and methods |
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Isolation of cDNA clones
Total RNA was extracted from embryos of mixed developmental stages using
Tri-reagent (Sigma, Poole, UK). mRNA was purified from the total RNA using a
poly-T+ spin column (Amersham Pharmacia Biotech, Little Chalfont,
UK). A first-strand reaction was carried out with 1 µg poly(A)+
RNA using Superscript II reverse-transcriptase (Gibco BRL, Paisley, UK) and
either an oligo-DT, 3' RACE cDNA synthesis primer (Gibco BRL) or an
oligo-DT, 5' RACE cDNA synthesis primer (Clontech, Basingstoke, UK) in
conjunction with a SMART II oligonucleotide
(Chenchik et al., 1998).
Primers were designed to conserved regions of multiple nucleotide sequence
alignments of genes from related species (Tables
1,
2), prepared using the Clustal
algorithm in Lasergene (DNAstar Inc, Madison, USA). Polymerase chain reaction
(PCR) conditions were complex and often involved multiple rounds and touchdown
cycles. Final PCR products were purified by agarose gel electrophoresis
followed by gel extraction on a spin column (Qiagen, Crawley, UK). cDNAs were
ligated into the PCR-4-TOPO vector (Invitrogen, Paisley, UK) and transformed
into TOP-10-F competent cells (Invitrogen) according to the manufacturer's
instructions. All clones were sequenced twice in either direction, and the
nucleotide and deduced amino acid sequences submitted to the NCBI database
(Table 1).
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|
In addition to the MSP genes, the 60S ribosomal subunit gene L15 was cloned
for use as an internal standard during RT-PCR analysis. None of the clones
have been previously isolated or sequenced elsewhere, all are novel sequences
reported for the first time. Sequence manipulation was carried out using
DNAman (Lynnon Biosoft, Vaudreuil, Canada) and Lasergene (DNAstar Inc.). The
phylogenetic tree was constructed from a Clustal alignment followed by
neighbour joining in PHYLIP (Felsenstein,
1995). Initial homology searches were carried out on the DNA data
bank of Japan (DDBJ) protein-blast engine.
Preparation of DIG-labelled cRNA probes
Plasmids were linearized using SpeI or NotI restriction
endonucleases and purified on an enzymatic cleanup spin column (Qiagen). 50 pg
µl1 of linear plasmid was used to transcribe the probes
in a reaction containing 1/10th volume DIG-RNA labeling mix (Roche,
Lewes, UK), transcription buffer and 2 U µl1 of the
appropriate RNA polymerase (T3 for NotI digests, T7 for SpeI
digests). Following incubation at 37°C for 2 h, the labelled probe was
purified by lithium chloride/ethanol precipitation and dissolved in
diethylpyrocarbonate (DEPC)-treated water, before storage at 80°C.
All probes were made using the longest plasmid insert possible, with the
exception of -actin, the 3' UTR of which was used to avoid
cross-hybridization with ß-actin, which is ubiquitously expressed
(Xu et al., 2000
).
In situ hybridization
20 embryos of mixed somite stages from each temperature group per cRNA
probe were used for in situ hybridization. Sense probes were also
used in each case as negative controls. In situ hybridization was
carried out using a procedure incorporating aspects of those described by
Wilkinson (1992) and Ennion
et al. (1999
), which permitted
a high throughput with small embryos and gave an excellent signal. The
triethanolamine wash, antibody preabsorption step and RNAse digestion step
were found to be unnecessary, and use of CHAPS rather than SDS allowed briefer
stringency washes carried out at a single temperature. Importantly, the length
of hybridization was lengthened considerably and appeared to result in a
stronger final signal.
Details of the in situ hybridization are as follows. Embryos were dechorionated on ice under a dissecting microscope using no. 10 watchmaker's forceps, then rehydrated at room temperature through 75% methanol:25% 0.1% Tween-20 in phosphate-buffered saline (PBST), 50%:50% methanol:PBST, 25%:75% methanol:PBST, followed by two washes in 100% PBST. Permeabilization was achieved by digestion in 20 µg ml1 proteinase K in PBST for 10 min, followed by 2x 5 min washes in PBST. Embryos were refixed in 4% (w/v) paraformaldeyde, 0.1% gluteraldehyde in PBST, followed by 3x 5min washes in PBST. A pre-hybridization step was carried out in hybridization buffer [50% formamide, 2% (w/v) blocking reagent (Roche), 0.1% Triton X-100, 0.1% (w/v) CHAPS, 20 µg ml1 yeast tRNA, 50 µg ml1 heparin in 5 mmol l1 EDTA] for 20 min at 70°C before addition of 0.5 µg ml1 digoxygenin (DIG)-labelled cRNA probe. The hybridization step lasted for 3 days at 70°C. Subsequent to hybridization, the embryos were washed with decreasing stringency to remove unbound probe. The post-hybridization washes were carried out at 70°C and consisted of 2x 10 min in 2x SSC, 3x 20 min in 2x SSC, 0.1% (w/v) CHAPS, and a further 3x 20 min washes in 0.2x SSC, 0.1% (w/v) CHAPS. Embryos were then rinsed 2x 10 min in `Heaven Seven' (HS) solution (150 mmol l1 NaCl, 1% Tween-20 in 100 mmol l1 Tris, pH 7.5) at room temperature followed by a 20 min blocking step in 20% sheep serum in HS. Bound probe was conjugated to an alkaline-phosphatase labelled anti-DIG antibody (Roche), which was used at a dilution of 1:4000, overnight at 4°C. Free antibody was removed by 4x 1 h washes in 1 mmol l1 levamisole in HS. The final colour reaction was carried out in `Divine Nine' (DN) solution (100 mmol l1 NaCl, 1% Tween-20, 1 mmol l1 levamisole, 100 mmol l1 Tris, pH 9.5) containing 1 mg ml1 of nitroblue tetrazolium (NBT) and 0.5 mg ml1 of 5-bromo-4-chloro-3-indolylphosphate (BCIP). After 24 h of development in the dark at 4°C, the reaction was stopped with 4% paraformaldehyde in PBS. Photographs were taken on a binocular microscope (Lieca MZ7.5, Milton Keynes, UK) using darkfield illumination and Zeiss (Welwyn Garden City, UK) Axiocam imaging system.
Analysis of expression patterns.
Expression patterns were determined for the structural/contractile mRNAs by
scoring the most posterior somite expressing a particular mRNA against the
somite stage. For MyoD, however, this was not considered appropriate
since expression preceded somite formation and was confined transiently to a
small number of somites. Instead, expression was compared visually and RT-PCR
analysis was carried out on RNAcDNA extracted from different stages of
development, as in Wyzykowski et al.
(2002
) and Lin-Jones and
Hauschka (1997
). Primers are
shown in Table 2. Statistics,
one-way analysis of variance (ANOVA) and multiple analysis of covariance
(MANCOVA) were performed according to Zar
(1999
).
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Results |
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Sequence analysis
Of the amplified cDNAs, deduced amino acid sequence conservation was
generally high. -actin was the most highly conserved, with an identical
deduced amino acid sequence to those of Alaskan pollack Theragra
chalcogramma and rat-tail fish Coryphaenoides cinereus
(Table 1).
The MyHC cDNA was a partial sequence (the full coding cDNA is >5000 bp
in carp; Hirayama and Watabe,
1997). The isolated clone came from the 3' end and spanned
779 bp of coding region and 89 bp of untranslated region (UTR). The deduced
amino acid sequence most closely matched that of chum salmon Oncorhynchus
keta adult fast skeletal muscle MyHC, exhibiting 88% sequence identity
(Table 1). No specific
functional domains were defined in this region.
Troponin I (TnI) exhibited the lowest identity with published sequences, 62% when compared with Atlantic salmon Salmo salar, and just 55% when compared to Atlantic herring (Table 1, Fig. 3). The most highly conserved region within the TnI molecule was the actin/troponin C (TnC) binding site located towards the center of the sequence. This binding site exhibited the motif characteristic of invertebrates (KPXLK) rather than that usually seen in vertebrates (RPXLR).
|
Troponin T (TnT) showed 86% sequence identity with the Atlantic salmon
isoform 3 (Table 1). A short
region of low conservancy at the N terminus
(Fig. 4) was present in a
position that spans several known splice sites in avian and mammalian TnTs
(Smillie et al., 1988).
|
Surprisingly, troponin C most closely matched the trout cardiac/slow isoform (Table 1), despite being expressed exclusively in the skeletal muscle and not in the heart (see Fig. 8, below). Sequence identity was 83% with both the trout and salmon cardiac/slow sequences (Fig. 5) and 81% with the Xenopus cardiac/slow sequence (not shown). The portion of the TnC sequence isolated incorporated the second, third and fourth Ca2+ binding sites (Fig. 5). Sites II and IV were highly conserved, exhibiting only five differences in 65 residues (92% identity) with the trout sequence. Site III showed less conservation, sharing 64% sequence identity with that of the trout.
|
|
The fast muscle creatine kinase (CK) clone was most closely related to that
from Mozambique tilapia Oreochromis mossambicus showing 89% identity
in deduced amino acid sequence (Table
1), and 87% with that of the zebrafish. It was possible to
recognise the active site motif CPSNLGT
(Fig. 6), which is absolutely
conserved between all known CK isoforms
(Taylor et al., 1990;
Fritz-Wolf et al., 1996
).
|
When blast searched on the DDBJ protein-blast engine, the full-length cod MyoD amino acid sequence showed greatest identity with zebrafish MyoD (64%; Table 1). The most conserved regions were the basic and the helixloophelix domains, with the extent of sequence identity declining towards the C terminus (Fig. 7).
|
In situ hybridization
mRNA signals for all of the MSP genes began in the most differentiated
somites at the anterior of the embryo and progressed rostrocaudally,
mirroring the pattern of somite formation
(Fig. 8). The onset of
expression of different genes was sequential, MyoD being the first to
be expressed in a single band in the presomitic mesoderm. Upon formation of
somites, expression was seen in the posteriormost seven, plus a single band
equivalent to the field of the next somite to be formed
(Fig. 9). After approximately
the 35-somite stage, expression faded, and somites continued to be added
caudal to the anal pore, unstained for MyoD mRNA. However, RT-PCR
analysis showed that transcripts were still present at the 40- and 50- somite
stages despite the lack of in situ hybridization staining
(Fig. 10). No expression was
seen in the adaxial cells adjacent to the notochord at any stage
(Fig. 9).
|
|
Subsequent expression of the contractile/structural MSPs was correlated with myotube and myofibril synthesis (Figs 1, 2). Expression occurred throughout the fibres/myotubes and no localization of message was seen either within cells or within the myotome. Unfortunately it was not possible to deduce whether expression occurred differentially in the slow and fast muscle. Whilst slow muscle fibres were undoubtedly stained, their presence as a superficial monolayer meant that unspecific bleed-through of products from the alkaline-phosphatase colour reaction was indistinguishable from any specific staining. Expression of all MSPs preceded development of organized myofibrils (Fig. 2).
No significant differences in expression of any genes were seen between
embryos raised at different temperatures
(Table 3,
Fig. 1). Expression of
MyoD was not scored against somite stage, because it was expressed
before the first somite formed, but the expression pattern remained the same
at different temperatures nonetheless. In all cases the characteristic pattern
of expression of a single stained band in the presomitic mesoderm followed by
seven stained somites was observed. At the initiation of myogenesis, however,
the body axis of embryos incubated at 10°C was frequently slightly shorter
than those incubated at lower temperatures, as a result of asynchrony between
the extent of epiboly and segmentation in these fish
(Fig. 11;
Hall and Johnston, 2003).
RT-PCR analysis showed that no transcript was detectable at the embryonic
shield stage, shortly prior to the initiation of myogenesis, but as
segmentation began, expression of MyoD was switched on
(Fig. 10). Furthermore,
low-level expression persisted even after completion of formation of somites
at the
50-somite stage, when transcripts are no longer visible by in
situ hybridization (Fig.
8).
|
|
When the expression patterns of different MSP transcripts were compared
with each other by MANCOVA, all were highly significantly different in terms
of slope or intercept, with the exception of
MyHC/-actin and TnC/CK-M (Tables
4,
5,
Fig. 2).
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Discussion |
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A common feature of many muscle proteins is that they have multiple
isoforms, which are generated either from separate genes or by alternate mRNA
splicing from the same gene. This situation is complicated in fish by an
ancestral whole-genome duplication event
(Meyer and Schartl, 1999;
Taylor et al., 2001a
), which
is thought to have occurred after the radiation of the sarcopterygian lineage,
which includes all terrestrial vertebrates. A second tetraploidization of the
salmonid genome is also thought to have taken place more recently
(Allendorf and Thorgaard, 1984
;
Rescan and Gauvry, 1996
).
Evidence for genome duplication events is far from conclusive (see Taylor et
al.,
2001a
,b
,c
;
Robinson-Rechavi et al.,
2001a
,b
),
but whatever the reason, teleost genomes are characterized by expanded gene
families (Robinson-Rechavi et al.,
2001c
).
There are at least six different actin genes present in mammals, the
products of which are expressed in various and overlapping cell types. ß-
and -actins are constituents of the cytoskeleton and are ubiquitously
expressed. A further four actins are specific to muscle cells. These include
two striated muscle (
-skeletal and
-cardiac) and two smooth
muscle (
-aortic and
-enteric) actins (Vandekerckhove and Weber,
1978
,
1979
). Polymerized actin
chains form the backbone of the thin filament, consisting predominantly of
mixed
and ß chains (Gordon et
al., 2000
). Single cDNAs encoding skeletal muscle
-actin
have been isolated from channel catfish Ictalurus punctatus
(Kim et al., 2000
), common
carp and goldfish (Watabe et al.,
1995
). However, in a recent study of the Japanese pufferfish
Fugu rubripes, Venkatesh et al.
(1996
) isolated nine distinct
genomic actin clones. These were classified as two skeletal
-actins,
three
-cardiac actins, one testis-type
-actin, two ß-actins
and one vascular ß-cytoplasmic actin. The two skeletal muscle types had
identical genomic organization and differed in only five amino acid residues.
Such high sequence identity is a common feature of actins, even between
distantly related species. This was consistent with the finding that cod
skeletal
-actin exhibited 100% deduced amino acid sequence
identity with that of Alaskan pollack and rat-tail fish
(Table 1). The expression
pattern was also comparable with that of zebrafish skeletal
-actin (Xu et al.,
2000
), being switched on shortly after the onset of somitogenesis
and before the expression of MyHC.
The MyHCs of vertebrates are encoded by multi-gene families and are
expressed in a tissue-specific manner
(Konig et al., 2002). It has
been reported that there are at least eight skeletal and two cardiac MyHCs in
humans (Soussi-Yanicostas et al.,
1993
). However, in the common carp Cyprinus carpio over
29 different genomic sequences have been identified
(Kikuchi et al., 1999
).
Different MyHC mRNA isoforms in teleosts have been shown to be
expressed under different conditions of temperature
(Imai et al., 1997
), at
different stages of development (Ennion et
al., 1999
) and in different fibre types
(Rescan et al., 2001
). In the
present study, no difference in MyHC expression was seen with
different rearing temperature. It is possible that the probe used in this
study bound heterologously to multiple MyHC mRNA isoforms, since the
proportion of 3' UTR:cds was much greater in this case than with the
other clones used (89 bp:779 bp, respectively). It is equally possible that
the probe hybridized to a specific isoform, which showed a broad pattern of
expression.
Troponin (Tn), is an actin-associated protein complex, consisting of three
interacting subunits, each with an identifying letter from the first
identified property: troponin C (TnC) binds Ca2+, troponin I (TnI)
binds to actin and inhibits the actomyosin ATPase and troponin T (TnT) links
the Tn complex to tropomyosin (Gordon et
al., 2000). Three TnT genes exist in mammals, encoding
fast, slow and cardiac forms (Huang et
al., 1999
). In the mouse, these are alternatively spliced into at
least 13 fast isoforms (Wang and Jin,
1997
) and three slow isoforms
(Jin et al., 1998
). Splicing
usually occurs close to the N terminus and different splice variants are
thought to be involved in ontogenetic changes in phenotype and in different
fibre-typing in the adult (Briggs and
Schachat, 1996
). Five TnT protein isoforms have been isolated from
Atlantic salmon, two from slow muscle and three from fast muscle
(Waddleton et al., 1999
). A
single fast muscle cDNA has been isolated from the zebrafish
(Xu et al., 2000
). The
TnT isoform isolated from cod showed greatest identity with an
Atlantic salmon fast muscle isoform. The most degenerate area of sequence was
at the N terminus, in a region spanning several known splice sites in mammals
(Smillie et al., 1988
).
As with TnT, the TnI isoform found in this study showed
greatest identity with an Atlantic salmon fast muscle isoform. Three genes
code for slow, fast and cardiac isoforms of TnI in birds and mammals
(Guenet et al., 1996;
Mullen and Barton, 2000
). Much
less is known about TnI in fish. Three cDNAs have been isolated from salmon
(Jackman et al., 1998
) and one
from herring (Hodgson et al.,
1996
). Surprisingly, however, in each case the amino acid sequence
identity was considered too low to assign orthology to either the fast, slow
or cardiac varieties seen in other vertebrates. In addition, the actin/TnC
binding site contained a motif (KPXLK) peculiar to
invertebrates, rather than that seen in avian and mammalian species
(RPXLR). This same, invertebrate-type motif was also seen in
the cod sequence found in this study (Fig.
3). The significance of this finding is unknown, but it appears
that TnI is more heterologous in fishes than in other vertebrates. At the
protein level too, Crockford et al.
(1991
) resolved two different
isoforms of TnI being co-expressed in the fast fibres of Oreochromis
niloticus and O. andersoni, using two-dimensional gels and
affinity chromatography. No genomic, cDNA or proteomic information on TnI has
yet been presented for the zebrafish.
Troponin C exists as two distinct tissue-specific types rather than the
three exhibited by the other Tn subunits. In birds, mammals and amphibians, a
fast-fibre type and a type specific to both slow and cardiac fibres have been
identified (Reinach and Karlsson,
1988; Gahlmann and Kedes,
1990
; Parmacek et al.,
1990
; Jin et al.,
1995
; Tiso et al.,
1997
; Warkman and Atkinson,
2002
). Numerous studies have investigated aspects of TnC function
in teleosts at the protein level (Demaille
et al., 1974
; McCubbin et al.,
1982
; Gerday et al.,
1984
; Feller and Gerday,
1989
; Crockford and Johnston,
1993
; Francois et al.,
1997
), but until now the only published nucleotide sequences were
those from zebrafish (showing highest identity to Xenopus fast-type;
Xu et al., 2000
) and trout
(showing highest identity to Xenopus slow/cardiac-type;
Moyes et al., 1996
). Because
protein sequences with homology to both fast-skeletal and slow/cardiac forms
have been isolated from fish, it has been supposed that their nature is
equivalent to those in birds and mammals
(Yuasa et al., 1998
). In this
study, however, the cod TnC sequence showed highest identity with the
trout cardiac form, but was only expressed in the myotomal muscle, and not in
the heart. Tissue-specific expression has not been investigated in the trout,
but the timing of expression shown in this study was quite different to that
of the zebrafish fast-type TnC shown by Xu et al.
(2000
). In zebrafish,
fast-type TnC was one of the first MSPs to be switched on, whereas in
the cod, expression occurred last out of the seven MSPs, towards the end of
somitogenesis. It may be, therefore, that TnC expression in teleosts is more
complex than previously thought, as has been demonstrated in the case of
TnI.
Fast skeletal muscle TnC contains four Ca2+ binding sites, which facilitate conformational changes in the protein according to calcium concentration. Sites I and II, in close proximity to the N terminus, have a lower Ca2+ affinity than sites III and IV, which are located towards the C terminus. In the cardiac/slow form of TnC, site I is non-functional. The nucleotide sequence isolated from cod did not cover site I, so comparison of this region could not be made with fast and slow isoforms from other species. However, binding sites II and IV were highly conserved, sharing 89% identity with the trout sequence. Site III was less highly conserved, sharing 64% sequence identity with the trout sequence.
In cells and tissues with intermittently high and fluctuating energy
requirements, including skeletal muscle, creatine kinase plays a central role
in the catalysis of the reversible transfer of a phosphate ion from
phosphorylcreatine to ADP to form high energy ATP
(Wallimann et al., 1992).
Creatine kinase enzymes constitute a family of different isoforms with
tissue-specific expression and isoenzyme-specific subcellular localization
(Stolz and Wallimann, 1998
).
Four isoform types are present in all vertebrates: a cytosolic brain-type
(CK-B), a cytosolic muscle-type (CK-M) and two mitochondrial types, CK-MiA and
CK-MiB (Benfield et al., 1984
;
Ordahl et al., 1984
;
Sun et al., 1998
). The genetic
organization of the creatine-kinase enzymes has been little studied in any
species, although it is known that three sub-isoforms of CK-M are encoded by
three different genes in the common carp
(Sun et al., 1998
) and that at
least two CK-M genes exist in the zebrafish
(Harder and McGowan, 2001
) and
in the channel catfish (Liu et al.,
2001
). Only one CK-M gene has been identified in any
mammalian species and it has been argued that the multiple copies found in
teleosts play a role in overcoming the rate-depressing effect of seasonal
cooling, and therefore help to retain muscle function over a broad temperature
range (Sun et al., 1998
). The
number of CK-M encoding genes in the cod is not known, but the
CK-M mRNA isoform examined in this study did not show any change in
its timing of expression, with respect to somite stage, between different
rearing temperatures.
There is an apparent paradox regarding the myofibrillar proteins, in that
despite the large number of splice variants found, and the enormous number
theoretically possible (Miyadzaki et al.,
1999), only a relatively small number of protein isoforms have
been isolated (Yao et al.,
1992
). This could be for several reasons; it might be that the
differences in protein structure are so subtle as to not be resolved by
currently available techniques, or that many proteins are inefficiently
transcribed or not stably incorporated into the myofibrils. Alternatively, the
explanation could simply be that isoform diversity is not so important at the
level of the protein. Duplication of genes at the genomic level might allow
them to be placed under different conditions of transcriptional control, and
divergence in mRNA primary structure might be a prerequisite for differential
timing and maintenance of translation.
Expression of MyoD in the cod was very unusual in that the
expression pattern appeared to be more limited than that shown previously in
the zebrafish (Weinberg et al.,
1996) and in the herring
(Temple et al., 2001
).
MyoD was not expressed in the adaxial cells adjacent to the
notochord, and was undetectable with ISH after approximately the 35-somite
stage (Fig. 8). It is well
known that two paralogues of MyoD exist in the salmonids, apparently
produced from a recent tetraploidization of the salmonid genome
(Rescan and Gauvry, 1996
), and
that these genes have diverged in function
(Delalande and Rescan, 1999
).
However, two non-allelic MyoD genes have recently been cloned from
the (non-salmonid) gilthead seabream Sparus aurata
(Tan and Du, 2002
). In this
case, MyoD2 transcripts are much more restricted in their expression
pattern than MyoD1. To test the hypothesis that the cod MyoD
clone was an orthologue of seabream MyoD2, a neighbour-joining
phylogenetic tree was constructed in PHYLIP
(Felsenstein, 1995
), using all
available full-length vertebrate MyoD sequences. Whilst the two trout
paralogues clustered together, the seabream paralogues were more highly
divergent. In addition, the seabream MyoD2 and cod MyoD
sequences also clustered together (Fig.
12).
|
In summary, muscle development in the Atlantic cod is canalized over the
temperature range studied (410°C). Although the number of fibres
has been shown to differ between temperature groups
(Hall and Johnston, 2003), the
relative timing of muscle development and expression patterns of the
myofibrillar mRNAs are independent of temperature. Myofibrillar genes are
activated asynchronously and follow a distinct temporal order during
myogenesis; a potentially exciting prospect is the application of these and
related cDNAs to the characterization of teleost embryos from pelagic sampling
studies. Surveys of fish egg abundance have been used to estimate spawning
biomass in stock assessments, and require the determination of the age
distributions and mortality rates of eggs
(Armstrong et al., 2001
). It is
suggested that the timing of MSP gene expression using in situ
hybridisation could be employed as the basis of a convenient species-specific
method of identification and staging.
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