Temperature and the expression of myogenic regulatory factors (MRFs) and myosin heavy chain isoforms during embryogenesis in the common carp Cyprinus carpio L.
1 Division of Cell and Developmental Biology, MSI/WTB Complex, University of
Dundee, Dow Street, Dundee, DD1 5EH, UK
2 Gatty Marine Laboratory, School of Biology, University of St Andrews, St
Andrews, Fife KY16 8LB, UK
3 Sir Harold Mitchell Building, School of Biology, University of St.
Andrews, Fife, KY16 9TH, UK
4 Laboratory of Aquatic Microbiology, School of Fisheries Sciences, Kitasato
University, Sanriku, Iwate 022-0101, Japan
5 Graduate School of Agricultural and Life Sciences, The University of
Tokyo, Bunkyo, Tokyo 113-8657, Japan
* Author for correspondence at present address: Victor Chang Cardiac Research Institute, 384 Victoria Street, Darlinghurst, Sydney, NSW 2010, Australia (e-mail: t.hall{at}victorchang.unsw.edu.au)
Accepted 27 August 2004
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Summary |
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Key words: Cyprinus carpio, temperature, development, muscle, in situ hybridization, carp, phylogeny, myogenic regulatory factor, MRF
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Introduction |
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During myogenesis, the transcription factors Myf-5 and MyoD are required
for the initial determination of the myogenic lineage. Gene knockout studies
in mice show that lack of MyoD and Myf-5 results in failure of myoblast
formation, and a consequent lack of all head and trunk skeletal muscle
(Rudnicki et al., 1993). In
zebrafish, targeted knockdown with a Myf-5 morpholino has been shown
to induce defects in myogenesis and brain formation
(Chen and Tsai, 2002
). The
expression of myogenin and MRF4 is activated during myoblast
differentiation (Rhodes and Konieczny,
1989
; Wright et al.,
1989
; Miner and Wold,
1990
; Edmondson and Olson,
1993
; Pownall et al.,
2002
), and myogenin and MRF4 probably have cooperative functions
with MyoD and Myf-5 as transcription factor regulators for the activation of
muscle contractile protein genes (Lassar
et al., 1991
). In myogenin-knockout mice, myoblasts form in the
correct place but do not fuse into muscle fibres
(Hasty et al., 1993
;
Nabeshima et al., 1993
;
Venuti et al., 1995
). The
function of MRF4 is less clear because in all three mutants constructed to
inactivate it, Myf-5 production is also affected
(Olson et al., 1996
;
Summerbell et al., 2000
,
2002
).
In the zebrafish, Danio rerio, Myf-5 and MyoD transcripts
are initially seen at approximately 7.5 h at 28.5°C (80% epiboly) in
bilateral bands of cells flanking the presumptive notochord
(Weinberg et al., 1996;
Chen et al., 2001
;
Coutelle et al., 2001
). The
expression patterns of these two genes overlap considerably, incorporating the
adaxial cells as they form. Expression of Myf-5 extends further into
the presomitic mesoderm than that of MyoD but, strikingly, as the
adaxial cells become incorporated into the somites, Myf-5
transcription dramatically declines. Expression of MyoD persists in
the differentiated somites until much later, after they become chevron-shaped,
whereupon it is downregulated. Expression of myogenin begins at 10.5
h (at 28.5°C) in a subset of the MyoD/Myf-5-expressing
cells (Weinberg et al., 1996
;
Chen et al., 2000
). The
myogenin transcripts first appear in bands of cells extending
laterally away from the adaxial cells. However, this lateral extension of
expression is narrower than in the case of MyoD and, due to its later
onset, first expression is within the somites rather than the presomitic
mesoderm. Transcription of myogenin is also transient, and persists
until shortly after the disappearance of MyoD transcription.
Furthermore, there are some differences in MRF gene expression between fish
species. In the rainbow trout, Oncorhynchus mykiss, for instance,
MyoD expression, rather than spreading laterally, remains confined to
the medial domain of the somite for a prolonged period
(Delalande and Rescan, 1999
).
In the herring Clupea harengus, myogenin mRNA shows a more transient
expression pattern than that seen in zebrafish
(Weinberg et al., 1996
) and
trout (Delalande and Rescan,
1999
), disappearing from the somites before the downregulation of
MyoD (Temple et al.,
2001
). A number of species including the trout
(Rescan and Gauvry, 1996
),
gilthead seabream Sparus aurata
(Tan and Du, 2002
) and
Xenopus laevis (Scales et al.,
1990
;
1991
;
Charbonnier et al., 2002
) also
possess multiple copies of one or more MRF-encoding genes.
Temperature has been shown to influence many aspects of development in
teleosts, including muscle cellularity
(Stickland et al., 1988;
Vieira and Johnston, 1992
;
Nathanailides et al., 1995
;
Johnston and McLay, 1997
;
Matschak et al., 1998
;
Galloway et al., 1998
,
1999
;
Hall and Johnston, 2003
) and
the relative timing of myofibrillogenesis (Johnston et al.,
1995
,
1996
,
1997
). There is also a small
body of evidence to suggest the timing and extent of MRF gene expression
varies with temperature. Xie et al.
(2001
) detected MyoD
and myogenin mRNAs in a greater number of somites in trout embryos of
the same developmental stage, reared at 12°C compared with 4°C. This
change in expression was apparently concomitant with a `relatively advanced'
state of muscle development at 12°C compared with 4°C. Similarly,
Wilkes et al. (2001
) used
quantitative northern blots to show that MyoD and myogenin
mRNA levels in trout and sea bass Dicentrarchus labrax were highest
at temperatures close to those of the usual environmental spawning
temperatures for the species. By contrast, Temple et al.
(2001
) found no difference in
the timing of MyoD or myogenin expression in herring embryos
reared at 5, 8 and 12°C. Hall et al.
(2003
) also found no
difference in the timing of MyoD expression between Atlantic cod
Gadus morhua embryos reared at 4, 7 and 10°C, although the timing
of blastopore closure relative to somite stage was relatively delayed at 7 and
10°C when compared with 4°C, and the number of deep fibres at hatching
in the 10°C group was significantly higher than in the lower temperature
groups.
Fishes from cold environments express myosin heavy chain (MyHC) protein
isoforms with a higher specific myofibrillar ATPase activity and a lower
thermal stability than those from warmer environments (Johnston et al.,
1973,
1975a
,b
),
and there is an apparent trade off between these traits. Species with a broad
temperature tolerance, such as the goldfish Carassius auratus and the
common carp Cyprinus carpio, can alter their Mg2+
Ca2+ ATPase activity depending on the ambient temperature by
differential expression of multiple MyHC genes
(Goldspink et al., 1992
;
Watabe et al., 1995
;
Imai et al., 1997
;
Cole and Johnston, 2001
). The
control of such acclimation responses is unknown and, to date, has not been
demonstrated in embryos, which express many of their own developmental
stage-specific isoforms of muscle proteins
(Scapolo et al., 1988
;
Crockford and Johnston, 1993
;
Johnston et al., 1997
). In
mammals, there is evidence for involvement of the MRFs in the determination of
contractile protein isoform expression and fibre typing
(Voytik et al., 1993
;
Hughes et al., 1999
) along
with other influences, such as hormones and innervation
(Hughes et al., 1993
;
Lefeuvre et al., 1996
).
The common carp is a eurythermal species commonly inhabiting waters that
fluctuate between near freezing and 30°C seasonally
(Michaels, 1988). Spawning
occurs in the summer months at a minimum temperature of
18°C, and the
eggs and larvae develop normally between temperatures of 18 and 25°C
(Penáz et al., 1983
;
Balon, 1995
). In the presnt
study, the spatial and temporal expression patterns of MyoD,
myogenin, and Myf-5 were characterised, and the hypothesis that
temperature influences expression of the MRFs within the normal limits of
thermal tolerance was investigated by comparing embryos and larvae reared at
18 and 25°C. The in situ expression pattern of Myf-5 was
of particular interest because within the Teleostei, to date, it has only been
described in the zebrafish and has never been investigated in relation to
temperature. In addition, the expression of five different MyHC
transcripts (two embryonic types, Ennion
et al., 1999
; and three temperature-specific types,
Imai et al., 1997
) were
characterised and compared between temperature groups. The aims of the present
study were to investigate the initial expression of temperature-specific
MyHC isoforms in larvae, and whether embryonic isoforms are
differentially expressed in response to rearing temperature, and to
characterise the timing of expression switching from embryonic to adult
isoforms. Finally, since many MRF cDNAs from teleosts have been cloned in
recent years and parologous genes have been identified, a comprehensive
phylogeny of vertebrate MRFs was also undertaken. Neighbour-joining and
parsimony analyses were used to generate phylogenies to elucidate evolutionary
relationships between the genes and the relative timing of gen(om)e
duplication events.
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Materials and methods |
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Plasmid clones and cRNA probes
The MyoD, myogenin and Myf-5 clones used were as
previously described by Kobiyama et al.
(1998). 10°C-type,
intermediate-type, and 30°C-type MyHC were as described by Imai
et al. (1997
). The two
embryonic-type MyHC clones (Eggs22 and Eggs24) were
generously supplied by Geoff Goldspink and are described by Ennion et al.
(1999
). DIG-labelled cRNA
probes were constructed from linear plasmids according to Hall et al.
(2003
). Details of plasmids,
restriction endonucleases and transcriptases are shown in
Table 1.
|
In situ hybridization
Five embryos of equivalent developmental stages from each sample were
selected per cRNA probe. In situ hybridization was carried out using
the procedure described by Hall et al.
(2003). Photographs were taken
on a Leica MZ7.5 binocular microscope (Leica, Milton Keynes, UK) using
darkfield illumination and a Zeiss Axiocam imaging system (Zeiss, Welwyn
Garden City, UK).
RNA dot-blotting
Total RNA was extracted from the trunk muscle of hatched larvae (the head,
tail and yolk sac were removed) using Tri-reagent (Sigma, Poole, UK). RNA
dot-blots were performed by spotting 2.5 µg of total RNA in 0.5 µl water
onto nitrocellulose (Hybond-N+; Amersham-Pharmacia, Little
Chalfont, UK), and fixing at 120°C in an oven for 30 min. A 30 min
prehybridization was carried out in 50% (v/v) formamide, 0.1% (m/v)
N-lauroylsarcosine, 0.02% (m/v) SDS, 2% (v/v) blocking reagent (Roche, Lewes,
UK) at 65°C, before addition of probe at 100 ng ml-1. After
hybridization overnight at 65°C, the blots were washed 2x15 min in 2
x SSC, 0.1% (m/v) SDS at room temperature, followed by 2x15 min in
0.5x SSC, 0.1% SDS at 65°C. Membranes were blocked in 2% (v/v)
blocking reagent, 100 mM maleic acid, 150 mM NaCl, pH 7.5 for 1 h, before
addition of an alkaline-phosphatase-conjugated anti-DIG antibody, Fab
fragments (Roche, Lewes, UK) at a dilution of 1/100,000. After a 30 min
incubation in the antibody solution, membranes were washed 2x15 min in
100 mM maleic acid, 150 mM NaCl, pH 7.5, 0.3% (v/v) Tween-20. Detection was
achieved using a 1:100 dilution of the chemiluminescent substrate CSPD (Roche,
Lewes, UK), in 100 mM Tris-HCl, 100 mM NaCl, pH 9.5 followed by exposure to
X-ray film.
Phylogenetic analysis of MRF sequences
A phylogenetic analysis was undertaken using full-length amino acid
sequences of vertebrate MRFs taken from the GenBank database (NCBI, Bethesda,
USA). Five additional sequences were predicted from Ensembl
(www.ensembl.org)
and Genoscope
(www.genoscope.cns.fr)
genome assemblies (see Data 1 in supplementary material), using Blast2
(v2.2.6) (Altschul et al.,
1997) and Genewise (Birney et
al., 2004
). An initial multiple alignment was constructed using
the Clustal algorithm in Lasergene (DNAstar Inc., Madison, USA), which was
then improved by eye. A neighbour-joining (NJ) tree was constructed in PHYLIP
(Felsenstein, 1995
) and
bootstrapped 1000 times to provide statistical support. Parsimony analysis was
carried out using PAUP (Swofford,
2002
) (see Data 2 in supplementary material).
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Results |
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Expression of MyoD and Myf-5 occurred simultaneously
following epiboly in the pre-somitic mesoderm. MyoD was expressed in
a pair of bilaterally symmetrical strips corresponding to the position of the
adaxial cells (Fig. 1c,d),
adjacent to the notochord. Myf-5 was also expressed in the adaxial
cells, but as development proceeded, transcripts spread further laterally into
the mesoderm (Fig. 1a,b).
Before the appearance of the first somite furrows, Myf-5 expression
could be seen very faintly in two bands corresponding to the cellular fields
of the first somites (Fig. 2a).
As soon as each somite formed, however, expression of Myf-5 was
downregulated. By contrast, expression of MyoD persisted as the
somites were formed (Figs
1c,d). The dynamics of expression were such that at any time
during somitogenesis, the newest 12 somites stained positive for
MyoD mRNA (Fig.
2b).
|
|
Expression of myogenin was switched on in the somites later than
Myf-5 and MyoD (Fig.
1e,f). The extent of staining lagged behind that of MyoD
by 5 somites, and
12 were stained at any one time
(Fig. 1c). The expression
patterns of all three transcripts gave the appearance of a rostral-caudal
wave, initiated by Myf-5, and followed by MyoD and
myogenin, respectively (Fig
1a-f). No differences were seen between 18 and 25°C groups
relative to developmental stage.
The embryonic forms of MyHC, Eggs22 and Eggs24 were first seen at the 25-30 somite stage, beginning in the anterior-most somites and progressing caudally (Fig 1g-j). After the completion of somitogenesis, Eggs22 transcripts became concentrated in the caudal somites, whereas Eggs24 predominantly stained the anterior somites. Expression persisted post-hatch, but was much reduced. No differences were seen between the 18 and 25°C groups with respect to developmental stage (Fig. 1g-j). No expression of mRNA for the 10°C-type, intermediate-type and 30°C-type MyHC isoforms were seen at any stage. Positive dot-blots using RNA isolated from fast muscle of 10 and 30°C acclimated adult carp (10 cm total length), alongside negative blots from the 18°C and 25°C incubated post-hatch larvae provided a positive control for the in situ results (Fig. 3).
|
The neighbour-joining tree separated the four MRFs in relation to the outgroup Ascidian sequence (Fig. 4; for accession numbers see Data 2 in supplementary material). Within genes, clades broadly reflected evolutionary relationships, and the majority of the bootstrap values were high (>90%). Further support was given by comparison with the tree from parsimony analysis, which was almost identical. Importantly, the Xenopus MyoD and myogenin paralogues clustered together, as did the trout MyoD paralogues. By contrast, the seabream amino acid sequences were more highly divergent.
|
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Discussion |
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The expression patterns of the genes encoding the embryonic MyHC isoforms
(Eggs22 and Eggs24) also showed no difference in timing
between temperature groups, and the timing of transcription was broadly
similar to that described by Ennion et al.
(1999). However, the finding
that the adult 10°C-type, intermediate-type and 30°C-type
MyHCs were not expressed, even as the embryonic forms disappeared,
was significant although not altogether unexpected. Other MyHC isoforms must
be present to bridge the gap, either further embryonic forms, adult forms, or
forms specific to the larval stages. Embryonic MyHC isoforms have been
described in a variety of other species including human
(Eller et al., 1989
;
Karsch-Mizrachi et al., 1989
)
rat (Strehler et al., 1986
),
chicken (Molina et al., 1987
;
Hofmann et al., 1988
) and
Xenopus (Radice and Malacinski,
1989
). However, the myosin heavy chain multigene family in the
carp is particularly large. Kikuchi et al.
(1999
) isolated 29 different
genomic clones, more than twice the number present in humans
(Soussi-Yanacostas et al., 1993; Kikuchi
et al., 1999
). Such diversity in carp myosin genes probably
reflects the need for different molecular characteristics during the life
cycle, as a result of allometric scaling relationships and temperature
acclimation (Imai et al.,
1997
; Ennion et al.,
1999
; Kikuchi et al.,
1999
; Cole and Johnston,
2001
).
The neighbour-joining tree for the MRF family is shown in
Fig. 4. The topology supports
the notion, proposed by Atchley et al.
(1994), that all four members
evolved from a common ancestor by gene duplication. After an initial
duplication, each lineage divided again, one giving rise to Myf-5 and
MyoD, and the other giving rise to myogenin and
MRF4. However, despite the fact that MRF4 is most-closely
related to myogenin, in the human and pufferfish the MRF4
gene is most-closely associated spatially with Myf-5. In human,
MYF5 and MRF4 are located on chromosome 12, with their start
codons only 8.5 kb apart (Patapoutian et
al., 1993
) and in pufferfish they are even closer together, with
their start codons differing by less than 5 kb (genomic clone encoding
Myf-5 and MRF4, NCBI accession no. AJ308546). It is possible
that the functions of the two genes demand that they respond to the same
control regions, or that their close proximity is essential for their
autoregulation, a hypothesis that is supported by the fact that in all of the
three Mrf4-knockout mice constructed, Myf5 function is also
affected (Summerbell et al.,
2002
).
Recently, the view of the MRFs as a discrete family of four
transcription-factor-encoding genes has been clouded by the discovery of
parologous forms, which have diverged in function in some species. Rescan and
Gauvry (1996) isolated a
second form of MyoD from the trout, and demonstrated different
expression patterns using in situ hybridization. MyoD1 was
expressed in the adaxial cells of the unsegmented mesodermal plate and in the
developing somites. MyoD2 expression, however, was initiated later
and was limited to the posterior compartment of the somite. Similarly, in
Xenopus, paralogous forms of MyoD and myogenin have
been isolated. One MyoD transcript (xlmf25) is expressed as
a maternal mRNA in the early embryo, while the other (xlmf1) is
activated from the zygotic genome near to the beginning of somitogenesis
(Scales et al., 1990
,
1991
). Of the
myogenin transcripts, one (XmyogU2) is expressed during
embryogenesis, while the other (XmyogU1) is exclusive to the adult
skeletal muscle (Charbonnier et al.,
2002
).
The expression of parologous genes is common in some organisms, such as
trout and Xenopus, both of which have undergone recent genome
duplication events and are in a state of pseudotetraploidy
(Allendorf and Thorgaard, 1984;
Hughes and Hughes, 1993
;
Rescan, 2001
). However, the
non-tetraploid gilthead seabream also differentially expresses two parologous
forms of MyoD (Tan and Du,
2002
). In this case, the sequence identity of the two forms is
lower than for the tetraploid organisms
(Fig. 4), suggesting a
more-ancient duplication event. Interestingly, a cDNA that clustered with
seabream MyoD2 (Fig.
3) was recently isolated from the Atlantic cod
(Hall et al., 2003
).
No parologous forms of MRF family genes have been isolated from any of the
tetrapod lineage, with the exception of the tetraploid Xenopus, and,
paradoxically, despite the availability of whole genome shotgun sequences, in
the zebrafish or pufferfish. The dynamics of teleost genome evolution is
extremely complex, with evidence for specific genome duplication events
remaining a contentious issue (Meyer and
Malaga-Trillo, 1999; Meyer and
Schartl, 1999
; Robinson-Rechavi et al.,
2001a
,b
;
Taylor et al.,
2001a
,b
).
In any case, whether at the whole-genome or more-regional level, teleost
genomes are characterised by a high rate of duplication followed by
substantial gene loss (Robinson-Rechavi et
al., 2001c
; Sibthorpe,
2002
; Smith et al.,
2002
). Further characterizing the molecular evolution of the MRF
family in relation to function remains a challenging, but potentially
rewarding, task.
Note added in proof
Since going to press, important new evidence has arisen regarding genome
duplication in the teleost lineage. Jaillon et al.
(2004) present near definitive
evidence from Tetraodon nigroviridis of an ancient full-scale genome
duplication. They demonstrate firstly, that every chromosome was involved in
large-scale duplication, and secondly, a striking pattern of double synteny,
with one chromosomal region in humans matching two in the pufferfish, across
the whole genome.
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Acknowledgments |
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Footnotes |
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These authors contributed equally to this work
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