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First published online February 13, 2009
Journal of Experimental Biology 212, 656-661 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.024000
Continuous light affects mineralization and delays osteoid incorporation in vertebral bone of Atlantic salmon (Salmo salar L.)
Institute of Marine Research, Bergen, Norway
* Author for correspondence (e-mail: anna.wargelius{at}imr.no)
Accepted 9 December 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: sonic hedgehog, collagen type I, alkaline phosphatase, matrix Gla protein, photoperiod, circadian rhythm
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). The
pineal gland is the main source of melatonin production, and is the primary
endocrine mediator of photoperiod changes. Pinealectomy has serious effects on
the vertebral column in mammalians, birds and fish (reviewed by
Pandi-Perumal et al., 2006).
Studies of Atlantic salmon after 6 months under continuous light
(Fjelldal et al., 2005) and 1
year after pinealectomy (Fjelldal et al.,
2004) revealed a lower mineral content and mechanical strength in
the bone of the vertebrae than under natural light, and after sham operation
and under natural light. The primary mechanism of pineal mediation of the
effect on the vertebral column is unknown. However, the action of melatonin on
bone can be mediated directly by action on membrane-bound receptors on
osteoblast cells or through the function of melatonin in setting the
suprachiasmatic circadian rhythm in the brain. Recent reports support the
hypothesis that osteoblasts can receive a direct innervation by sympathetic
neurons controlled by the circadian rhythm in the suprachiasmatic nucleus
(reviewed by Patel and Elefteriou,
2007). Studies in mammals have reported that light manipulation
changes the pattern of osteoblast proliferation and bone mass in response to
changes in circadian pattern. Seasonality in bone mass has also been reported
in the teleost Atlantic salmon (Wargelius
et al., 2005a). The molecular signals that bring about change in
bone mass are unknown, but it is likely that light treatment stimulates a
change in the formation rate of osteoid tissue and/or the mineralization
ability of the tissue.
In this study the gene expression of the gene sonic hedgehog
(shh) was selected as a marker of osteoblast cell proliferation since
the protein product is crucial for development and growth of bone in mouse
(Chiang et al., 1996;
St-Jacques et al., 1999) and
ectopic expression of shh results in excess dermal bone formation in
regenerating zebrafish (Danio rerio) caudal fins
(Quint et al., 2002). Alkaline
phosphatase (Alp) was selected because of its involvement in the mineralizing
function of the osteoblasts, and the expression of its gene is commonly used
in mammalian species to measure the level of extracellular matrix
mineralization (ECM) (Rawadi et al.,
2003). Matrix Gla protein (Mgp) was selected based on its
involvement in the calcification of ECM, and mgp deficiency in mice
results in overcalcification of bone and cartilage
(Luo et al., 1997), suggesting
that the protein functions, to some extent, as an inhibitor of calcification.
The expression of this gene has also been found to be induced during
mineralization of a bone-derived cell line from sea bream (Sparus
aurata L.) (Pombinho et al.,
2004). Another marker, collagen type I alpha 2 (col
I; also known as col1 a2) was selected, because collagen I is
the major structural protein that is incorporated into bone. Two of the genes
used in this study, shh
(Wargelius et al., 2005b) and
mgp (Laize et al.,
2005), have been cloned and/or identified previously in Atlantic
salmon, and the other genes have been identified by sequence homology;
alp, has been identified in fugu (Takifugu rubripes, GenBank
acc. no. NM_001032651) and Atlantic salmon (acc. no. CO472235). Collagen type
I precursors have been identified in a number of fish species, including
rainbow trout (Oncorhynchus mykiss Walbaum)
(Saito et al., 2001). In
rainbow trout, type I procollagen has a trimer structure 
1(I)
2(I) 3(I) (Saito et al.,
2001) and in this study it was used as a homologous sequence to
the 2 chain (acc. no. CA064459).
To summarize, the effects of photoperiod and pinealectomy on the gene
expression of proteins involved in bone cell proliferation, and in the
production and mineralization of osteoids, remain to be elucidated. To study
the photoperiodic effect on vertebral bone, we reared Atlantic salmon under
continuous light or natural light [following the protocol by Porter et al.
(Porter et al., 1999)], and
the gene expression levels of proteins involved in cell proliferation,
mineralization and osteoid formation were measured in vertebral bone once a
month from January until the summer solstice. In addition, yield-load and
stiffness were used as markers of osteoid incorporation and mineralization
respectively, as it is known that stiffness reflects the mineral content of
bone, whereas yield-load is a measure of the collagen content and structure of
the bone (reviewed by Currey,
2003).
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The experiment was designed with one experimental and one control group,
each with three replicates in separate cages, and the experiment lasted from
mid January until the summer solstice (19 June). At the start of the
experiment, the fish were randomly allocated to one of six cages (5 m x5
m x7 m), so that each cage contained 154 tagged and 220 untagged fish.
Three cages of the experimental group were reared under a natural photoperiod
with additional 24 h continuous light, while the fish in the three cages of
the control group were reared under a natural photoperiod. For continuous
illumination, one asymmetric metal halide lamp per cage was employed
(Euroflood, Siemens, Trondheim, Norway; Osram Powerstar HQI-TS 150W/NDL UVS).
The lamps were mounted on the side of the cages, 2 m above the water surface,
yielding an illuminance of 105±7 lux at a depth of 1 m. A light-tight
barrier separated the illuminated cages from the others. The fish were reared
at ambient temperature, which decreased from 7.9°C in January to 5.6 in
March and then increased to 10.5°C in June (measured at a depth of 5 m).
The salinity at 5 m was stable at approximately 31
.
The fish were fed Bio-optimal® dry feed (BioMar Ltd, Trondheim,
Norway), to excess, using a computer-operated feeding system (ARE,
Storebø, Norway). Three pellet sizes (3 mm, 4 mm and 6 mm) were used as
the fish grew throughout the experiment. To control sea lice infestation, the
fish were given SLICE® (Schering-Plough AS, Farum, Denmark) at a dose of
0.5% of biomass per day for 1 week in the middle of the experimental period.
The growth performance of the tagged fish during the experimental period is
published in Fjelldal et al. (Fjelldal et
al., 2005) and Nordgarden et al.
(Nordgarden et al., 2006). The
mean mass at the start of the experiment was 135 g, and at the end of the
experiment was 457 g and 372 g in the continuous and natural light groups,
respectively. The mortality rate during the experimental period was 0.7% in
the continuous light group and 0.6% in the natural light group. Throughout the
experiment 16 fish from each tank were sampled for gene expressional studies
(N=3/tank) and biomechanical analysis (N=3/tank: stiffness,
yield-load and mineral content) and X-ray (N=10/tank). Owing to the
monthly sampling and the general mortality in the fish groups 264 and 276 fish
remained in the two light treatment groups and the end of the experiment.
Tissue sampling
First sampling was carried out on 13 January, followed by samplings after
3, 6, 10, 15 and 22 weeks. At each sampling, 16 fish from each cage were
anaesthetized with metomidate hydrochloride (Wildlife Pharmaceuticals, Fort
Collins, CO, USA) according to Olsen et al.
(Olsen et al., 1995), and
killed by a blow to the head, before sampling of vertebral tissue (six fish),
and dissection of vertebral columns for lateral radiographs (10 fish). The
fortieth vertebra (V40), which is located in the caudal region of the
vertebral column, was carefully dissected out and immediately frozen in liquid
nitrogen for later analysis of gene expression, and whole fish were frozen
(–20°C) for measurement of vertebral mineral content and mechanical
strength.
Radiology
Radiographs were taken using a portable X-ray apparatus (HI-Ray 100,
Eickenmeyer Medizintechnik für Tierärzte e.K., Tuttlingen, Germany)
and 30 x40 cm film (AGFA Structurix D4 DW ETE, Agfa-Gevaert N.V.,
Mortsel, Belgium). The film was exposed twice for 50 mA and 72 kV, and
developed using a manual developer [Cofar Cemat C56D, Arcore (MI), Italy] with
Kodak Professional manual fixer and developer (Kodak S.A., Paris, France). The
images were digitized using an A3 positive scanner (Epson Expression 10000 XL,
Seiko Epson, Kagano-Ken, Japan). Each fish was evaluated for vertebral
deformities, and the number of affected vertebrae was recorded.
Bone properties
The vertebrae were compressed in the cranial–caudal direction using a
texture analyzer (TA-XT2 Texture Analyzer, Stable Micro Systems, Haslemere,
UK) with a steadily advancing piston (6 mm min–1).
Load-deformation data were continuously recorded, and the stiffness (g
mm–1) and yield-load (g) were calculated for each vertebra
according to the method of Fjelldal et al.
(Fjelldal et al., 2004). After
mechanical testing, the vertebrae were defatted in hexane baths, dried
overnight at 90°C, and then incinerated for 13.5 h in a muffle furnace
(115°C for 0.5 h, 540°C for 5 h, and 750°C for 8 h). The ash
(mineral) weight of each vertebra was weighed to within 1
x10–2 mg. Mineralization per day was calculated as
increase in mineral mass per day (mg day–1). This was done
based on the ash mass of the sampled vertebrae, using the following formula;
{[average ash mass in tank Xn at time (t)
2]–(average ash mass in tank Xn at
t1)}/(number of days between samplings). As stated above, we used
three fish (N=3) in each replicate tank and three replicate tanks
(X1, X2 and X3)
were used per treatment.
Real-time PCR
Total RNA was extracted from vertebral tissue using FastRNA Pro Green Kit
(Qbiogene, Cambridge, UK). RNA was DNAse treated (37°C for 30 min,
Promega, Madison, WI, USA) and then extracted once more with phenol pH 4.5.
First-strand cDNA was reverse transcribed using a Reverse Transcription Core
Kit (RT-RTCK-05; Eurogenetec, Seraing, Belgium) using 500 ng of RNA. For
amplification of shh (GenBank acc. no. AY370830), col I
(acc. no. CA064459), alp (acc. no. CO472235), mgp (acc. no.
AY182239) and the normalization gene, elongation factor 1
[e1; Acc no AF321836
(Olsvik et al., 2005)], the
primers and probes listed are listed in
Table 1. Primers were tested
using conventional PCR and shown to amplify a single band of approximately 80
bp. Real-time PCR was carried out on an ABI 7700 system (Applied Biosystems,
Foster City, CA, USA). Thermal cycling conditions were 50°C for 2 min
followed by 98°C for 10 min. Subsequently, the reactions proceeded through
40 cycles of 95°C for 15 s followed by 60°C for 1 min. Each reaction
(25 µl) contained 5 µl of cDNA diluted 1:5 in ddH2O, 12.5
µl of Taqman Universal PCR master mix (Applied Biosystems) and 0.9 µmol
l–1 of forward and reverse primers. Each sample was run in
triplicate and each stage contained six RNA replicates (samples from six
different fish). The efficiency of the targets (shh, mgp, col I and
alp) in relation to the reference (el) was determined
using a standard curve method together with a validation experiment (Applied
Biosystems, User Bulletin #2 for ABI 7700 sequence detections system). In the
validation experiment, 500, 250 and 125 ng of RNA were used for cDNA synthesis
and the slope of log input amount of RNA versus delta Ct for
shh/e1 was 0.028, for mgp/e1
was 0.061, col I/e1 was 0.025 and
alp/e1 was 0.042, which is <0.1, which
demonstrates that the efficiency of target and reference were approximately
equal. The relative expression level was calculated using the Comparative Ct
method (Applied Biosystems, User Bulletin #2 for ABI 7700 sequence detection
system). In all experiments no-template controls were run together with the
samples.
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Statistics
All data was subjected to Kolmogorov–Smirnov test for Gaussian
distribution. Stiffness, Yield-load and gene expression of col I, shh
and alp were confirmed to have Gaussian distribution and were
subjected to two-way ANOVA with photoperiod and time as the dependent factors
when analyzing for differences among photoperiod groups or variation over
time, respectively. The data were further subjected to Bonferroni
post-hoc tests. Expression of mgp and mineral incorporation
per day did not meet the assumption of Gaussian distribution; these data were
subjected to an unpaired t-test with Welch's correction. Data
analyses were performed using GraphPad Prism 5.0 (La Jolla, CA 92037, USA). A
P value <0.05 was taken to indicate statistical significance.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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shh expression
In the natural light group, shh expression increased from 3
February until 24 February and remained high throughout the study
(P<0.001; Fig. 1C,
white bars). In the continuous light group shh expression increased
on 28 April in comparison with 13 January (P<0.05;
Fig. 1C, black bars). When
light groups at each time point were compared, shh showed higher
expression in the natural light group on 24 February (P<0.05).
Stiffness
In the natural light group, vertebral stiffness (gmm–1)
increased from 3 February to 28 April (P<0.05;
Fig. 2A, white bars). In the
continuous light group, stiffness increased from 13 January to 24 March
(P<0.05) and then again from 28 April to 19 June
(P<0.05; Fig. 2A,
black bars).
alp expression
In both light groups the expression of alp
(Fig. 2B, white and black bars)
was low and stable in the period between 13 January and 24 March, and
increased from 24 March until 28 April (P<0.001 in both light
groups), and then decreased significantly from 28 April until 19 June
(P<0.001 in both light groups). When light groups at were
compared, no differences were detected between light groups.
Mineral incorporation per day
In the natural light group the per diem mineral incorporation was
higher between 28 April and 19 June than between 13 January and 3 February
(P<0.05). In the continuous light group, mineral incorporation per
day was higher between 28 April and 19 June than between 13 January and 3
February (P<0.05) or 24 February and 28 April (P<0.05;
Fig. 2C). When light groups at
each time point were compared, no differences were detected.
mgp expression
In both light groups the expression of mgp
(Fig. 2D, white and black bars)
was at a low steady state between 13 January and 24 March, increasing on 28
April (P<0.001 in both light groups), and then decreasing between
28 April and 19 June in the natural light group (P<0.005). When
light groups at were compared, lower mgp expression was detected in
the continuous light group on 28 April (P<0.05).
Vertebral deformities
To assay if continuous light treatment affected the occurrence of vertebral
deformities, fish were X-rayed at the end of the experiment
(N=30/light group). The prevalence of individuals with one or more
deformations of vertebral bodies was 6.7% at the start of the experiment, and
3.3% and 10% in the natural and continuous light groups, respectively, at the
end of the experiment on 19 June. The deformities were located in all regions
of the vertebral column, and there were no severe cases. The number of
affected vertebrae per deformed fish ranged between 1 and 3.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). These factors may also contribute to the actual
level of collagen fibril incorporation into the bone. In bovine cortical bone,
the extracellular post-translational modifications of collagen are the major
determinants of its biomechanical properties
(Garnero et al., 2006). This
suggests that collagen I abundance in bone was controlled at the
post-translational level during the first phase of the experiment, while its
abundance was regulated at the level of gene expression during the last
phase.
In the natural light group, the increase in shh expression on 24
February was followed by an increase in col I expression and
yield-load between 24 February and 19 June. Shh has been shown to be involved
in osteoblast proliferation in zebrafish bone
(Quint et al., 2002), and this
suggests an increase in osteoblast proliferation between 24 February and 19
June in the present experiment. Furthermore, increased osteoblast
proliferation could explain why both col I and yield-load increased
between 24 February and 19 June. Taken together, these results suggest that in
Atlantic salmon the expression of both col I and shh can be
used as markers of osteoid incorporation and osteoblast proliferation,
respectively.
This experiment found a clear link between stiffness (g
mm–1) and expression of both the alkaline phosphatase and
matrix Gla protein genes. Stiffness provides a measure of the mineral phase of
the bone (reviewed by Currey,
2003) and this result suggests that both mgp and
alp are involved in bone mineralization in salmon. If mgp
and alp are involved in mineralization, our results imply that
mineralization has a seasonal component. Similar results have been found
previously, with a significant increase in expression of the genes for both
IGF-1 and its receptor during the same time of year
(Nordgarden et al., 2006;
Wargelius et al., 2005a).
However, mineral incorporation (mg mineral per day) was not directly related
to expression of the alp and mgp genes. Mineral
incorporation per day seems to be related to both stiffness and alp
and mgp expression during the last phase of the experiment (28 April
to 19 June), since stiffness increased from April to June and both
alp and mgp showed a peak in expression on 28 April.
Moreover, the gradual increase in stiffness between February and April was not
reflected in mineral incorporation per day or the expression of alp
or mgp, which suggests that there are other factors promoting the
long-term increase in mineralization in Atlantic salmon vertebrae.
The increase in the relative expression of col I over the last
three samplings in the natural light group compared to the increase in col
I between the last two samplings in the continuous light group indicates
that there was a delay in the induction of collagen production in the fish
exposed to continuous light. Similarly, it is known in mammals and birds that
the increase in collagen production takes place at night
(Hassager et al., 1992;
Simmons and Nichols, 1966).
Our results suggest that the dark phase of the photoperiod plays a role in the
regulation of collagen I expression in salmon. It has previously been
reported that DNA synthesis in rat osteoblasts peaks during the night
(Fu et al., 2005). However,
this study is the first to demonstrate an effect of photoperiod at the level
of expression of the collagen I gene.
The expression of Shh rose 1 month later in the continuous light
group. If shh is involved in the recruitment of osteoblasts in
salmon, our results suggest that there is a lower early recruitment of
osteoblasts in fish exposed to continuous light. This presumption is based on
results from zebrafish dermal bone, where ectopic expression of shh
induces osteoblast proliferation (Quint et
al., 2002). The delay in induction of both shh and
col I expression in the continuous light group is then reflected in a
1 month delayed increase in yield-load, which is probably is a result of a
delay in osteoblast recruitment (shh expression) and a subsequent
reduction in organic matrix production (col I expression). These
results leads us to suggest that constant light delays both osteoblast
proliferation and thereafter collagen I production, which lead to temporal
changes in the properties of the extracellular matrix.
If Mgp plays a similar role in salmon as in mammals, i.e. inhibition of
mineralization (Luo et al.,
1997), the lower mgp expression in the continuous light
groups in late April would suggest that mineralization increased in fish on
continuous light towards the end of the experiment. This is also reflected in
the per diem rate of mineral incorporation, which rose significantly
during the last phase (April to June) of the experiment. This was not the case
in the normal light group, in which the mineral incorporation per day
increased gradually throughout the whole experimental period (February to
June).
In the continuous light group, stiffness increased between February and
March, while in the normal light group the increase occurred between February
and April. The more rapid increase in mineral incorporation in the bone is not
reflected in the molecular markers used in this study. However, a previous
growth study showed that IGF-1 gene expression in bone was significantly
higher in the continuous light group 2 weeks after onset of the light
(Nordgarden et al., 2006). In
mice, IGF-1 promotes mineralization of trabecular bone
(Zhang et al., 2002). The
earlier increase in stiffness in the vertebral bone of
continuous-light-treated fish can perhaps be explained by an increase in local
IGF-1 production, which then results in a temporary higher mineralization rate
of the vertebral bone. Also a growth-promoting effect of light was observed at
the whole fish level, for which there was higher specific growth rates in
response to continuous light (Nordgarden
et al., 2006). This observation implies that in salmon the
stiffness (mineral content) of the bone is altered in response to the higher
growth rates induced by the continuous light, while the osteoid incorporation
is delayed.
Plasma levels of melatonin in Atlantic salmon are under diurnal regulation,
and increase during the dark phase (Iigo
et al., 1997; Porter et al.,
2001). It is possible that the effects of constant light on the
vertebral bone have been mediated by the action of melatonin on bone, through
the suprachiasmatic nucleus in setting the circadian rhythm, and further
through sympathetic signaling directly to osteoblastic cells, resulting in
changes in the bone-specific circadian clock
(Patel and Elefteriou, 2007).
In mice, an interrupted circadian clock increases the number of osteoblasts in
bone and the bone formation rate (Fu et
al., 2005). The opposite results were obtained in this experiment,
with a decrease in osteoid production (reduced col I expression,
reduced yield-load) and a potential reduction in osteoblast numbers (reduced
shh expression) in response to constant light. Our results therefore
suggest that the circadian rhythm of the osteoblasts might have been altered,
in that they showed loss of a higher rate of bone formation at night, which
implies that circadian rythmicity may have been temporarily lost, resulting in
the delayed induction of osteoblast proliferation and organic matrix
production.
Exposure to constant light alters the pattern of vertebral growth in
Atlantic salmon, by delaying proliferation and bone formation while advancing
mineralization. However, by the end of the experiment, close to the summer
solstice, the fish had managed to balance out the changes induced by the
continuous light treatment, thereby displaying similar levels of both
yield-load and stiffness. The light-induced change in bone properties during
the spring did not result in any bone deformities, implying that continuous
light treatment does not promote vertebral deformities. In addition it would
appear that col I, shh, mgp and alp can be used as markers
of changes in bone properties related to both the organic and inorganic
extracellular matrices of salmon vertebrae. To conclude, continuous light
exposure has a large impact at the whole organism level in salmon, where it
affects the growth rate, timing of smoltification and reproduction
(Berg et al., 1992;
Krakenes et al., 1991;
Saunders and Henderson, 1988;
Stefansson et al., 1991).
Little is known about how light affects the physiology at the specific tissue
level, but it is known that other tissues than bone are affected by light,
such as the composition and cellularity of muscle
(Johnston et al., 2003;
Nordgarden et al., 2003).
Results from this study and previous reports clearly indicate that light has a
substantial impact both at the tissue as well as on the whole organism
level.
LIST OF ABBREVIATIONS
2 gene
gene
|
Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Berg, A., Hansen, T. and Stefansson, S. (1992). 1st feeding of Atlantic salmon (Salmo salar L) under different photoperiods. J. Appl. Ichthyol. 8,251 -256.[CrossRef]
Chiang, C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H. and Beachy, P. A. (1996). Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383,407 -413.[CrossRef][Medline]
Currey, J. D. (2003). Role of collagen and other organics in the mechanical properties of bone. Osteoporos. Int. 14 Suppl. 5,S29 -S36.[CrossRef][Medline]
Fjelldal, P. G., Grotmol, S., Kryvi, H., Taranger, G. L., Hansen, T., Porter, M. J. R. and Totland, G. K. (2004). Pinealectomy induces malformation of the spine and reduces the mechanical strength of the vertebrae in Atlantic salmon, Salmo salar. J. Pineal Res. 36,132 -139.[CrossRef][Medline]
Fjelldal, P., Nordgarden, U., Berg, A., Grotmol, S., Totland, G., Wargelius, A. and Hansen, T. (2005). Vertebrae of the trunk and tail display different growth rates in response to photoperiod in Atlantic salmon, Salmo salar L., post-smolts. Aquaculture 250,516 -524.[CrossRef]
Fu, L., Patel, M. S., Bradley, A., Wagner, E. F. and Karsenty, G. (2005). The molecular clock mediates leptin-regulated bone formation. Cell 122,803 -815.[CrossRef][Medline]
Garnero, P., Borel, O., Gineyts, E., Duboeuf, F., Solberg, H., Bouxsein, M. L., Christiansen, C. and Delmas, P. D. (2006). Extracellular post-translational modifications of collagen are major determinants of biomechanical properties of fetal bovine cortical bone. Bone 38,300 -309.[CrossRef][Medline]
Ge, G. and Greenspan, D. S. (2006). Developmental roles of the BMP1/TLD metalloproteinases. Birth Defects Res. C Embryo Today 78,47 -68.[CrossRef][Medline]
Hassager, C., Risteli, J., Risteli, L., Jensen, S. B. and Christiansen, C. (1992). Diurnal variation in serum markers of type I collagen synthesis and degradation in healthy premenopausal women. J. Bone Miner. Res. 7,1307 -1311.[Medline]
Iigo, M., Hara, M., Ohtani-Kaneko, R., Hirata, K., Tabata, M. and Aida, K. (1997). Photic and circadian regulations of melatonin rhythms in fishes. Biol. Signals 6, 225-232.[Medline]
Johnston, I. A., Manthri, S., Smart, A., Campbell, P., Nickell,
D. and Alderson, R. (2003). Plasticity of muscle fibre number
in seawater stages of Atlantic salmon in response to photoperiod manipulation.
J. Exp. Biol. 206,3425
-3435.
Krakenes, R., Hansen, T., Stefansson, S. O. and Taranger, G. L. (1991). Continuous light increases growth-rate of Atlantic salmon (Salmo-Salar L.) postsmolts in sea cages. Aquaculture 95,281 -287.[CrossRef]
Laize, V., Martel, P., Viegas, C. S., Price, P. A. and Cancela,
M. L. (2005). Evolution of matrix and bone
gamma-carboxyglutamic acid proteins in vertebrates. J. Biol.
Chem. 280,26659
-26668.
Luo, G., Ducy, P., McKee, M. D., Pinero, G. J., Loyer, E., Behringer, R. R. and Karsenty, G. (1997). Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 386,78 -81.[CrossRef][Medline]
Nordgarden, U., Ornsrud, R., Hansen, T. and Hemre, G. I. (2003). Seasonal changes in selected muscle quality parameters in Atlantic salmon (Salmo salar L.) reared under natural and continuous light. Aquac. Nutr. 9,161 -168.[CrossRef]
Nordgarden, U., Fjelldal, P. G., Hansen, T., Bjornsson, B. T. and Wargelius, A. (2006). Growth hormone and insulin-like growth factor-I act together and independently when regulating growth in vertebral and muscle tissue of Atlantic salmon postsmolts. Gen. Comp. Endocrinol. 149,253 -260.[CrossRef][Medline]
Olsen, Y. A., Einarsdottir, I. E. and Nilssen, K. J. (1995). Metomidate anesthesia in Atlantic salmon, Salmo-salar, prevents plasma-cortisol increase during stress. Aquaculture 134,155 -168.[CrossRef]
Olsvik, P. A., Lie, K. K., Jordal, A. E., Nilsen, T. O. and Hordvik, I. (2005). Evaluation of potential reference genes in real-time RT-PCR studies of Atlantic salmon. BMC Mol. Biol. 6,21 .[CrossRef][Medline]
Pandi-Perumal, S. R., Srinivasan, V., Maestroni, G. J., Cardinali, D. P., Poeggeler, B. and Hardeland, R. (2006). Melatonin: nature's most versatile biological signal? FEBS J. 273,2813 -2838.[CrossRef][Medline]
Patel, M. S. and Elefteriou, F. (2007). The new field of neuroskeletal biology. Calcif. Tissue Int. 80,337 -347.[CrossRef][Medline]
Pombinho, A. R., Laize, V., Molha, D. M., Marques, S. M. and Cancela, M. L. (2004). Development of two bone-derived cell lines from the marine teleost Sparus aurata: evidence for extracellular matrix mineralization and cell-type-specific expression of matrix Gla protein and osteocalcin. Cell Tissue Res. 315,393 -406.[CrossRef][Medline]
Porter, M. J. R., Duncan, N. J., Mitchell, D. and Bromagea, N. R. (1999). The use of cage lighting to reduce plasma melatonin in Atlantic salmon (Salmo salar) and its effects on the inhibition of grilsing. Aquaculture 176,237 -244.[CrossRef]
Porter, M. J. R., Duncan, N., Handeland, S. O., Stefansson, S. O. and Bromage, N. R. (2001). Temperature, light intensity and plasma melatonin levels in juvenile Atlantic salmon. J. Fish Biol. 58,431 -438.[CrossRef]
Quint, E., Smith, A., Avaron, F., Laforest, L., Miles, J.,
Gaffield, W. and Akimenko, M. A. (2002). Bone patterning is
altered in the regenerating zebrafish caudal fin after ectopic expression of
sonic hedgehog and bmp2b or exposure to cyclopamine. Proc. Natl.
Acad. Sci. USA 99,8713
-8718.
Rawadi, G., Vayssiere, B., Dunn, F., Baron, R. and Roman-Roman, S. (2003). BMP-2 controls alkaline phosphatase expression and osteoblast mineralization by a Wnt autocrine loop. J. Bone Miner. Res. 18,1842 -1853.[CrossRef][Medline]
Saito, M., Takenouchi, Y., Kunisaki, N. and Kimura, S. (2001). Complete primary structure of rainbow trout type I collagen consisting of alpha1(I)alpha2(I)alpha3(I) heterotrimers. Eur. J. Biochem. 268,2817 -2827.[Medline]
Saunders, R. L. and Henderson, E. B. (1988). Effects of constant day length on sexual maturation and growth of Atlantic salmon (Salmo salar) parr. Can. J. Fish. Aquat. Sci. 45,60 -64.
Simmons, D. J. and Nichols, G., Jr (1966).
Diurnal periodicity in the metabolic activity of bone tissue. Am.
J. Physiol. 210,411
-418.
St-Jacques, B., Hammerschmidt, M. and McMahon, A. P.
(1999). Indian hedgehog signaling regulates proliferation and
differentiation of chondrocytes and is essential for bone formation.
Genes Dev. 13,2072
-2086.
Stefansson, S. O., Bjornsson, B. T., Hansen, T., Haux, C., Taranger, G. L. and Saunders, R. L. (1991). Growth, parr-smolt transformation, and changes in growth hormone of Atlantic salmon (Salmo salar) reared under different photoperiods. Can. J. Fish. Aquat. Sci. 48,2100 -2108.[CrossRef]
Wargelius, A., Fjelldal, P. G., Benedet, S., Hansen, T., Bjornsson, B. T. and Nordgarden, U. (2005a). A peak in gh-receptor expression is associated with growth activation in Atlantic salmon vertebrae, while upregulation of igf-I receptor expression is related to increased bone density. Gen. Comp. Endocrinol. 142,163 -168.[CrossRef][Medline]
Wargelius, A., Fjelldal, P. G. and Hansen, T. (2005b). Heat shock during early somitogenesis induces caudal vertebral column defects in Atlantic salmon (Salmo salar). Dev. Genes Evol. 215,350 -357.[CrossRef][Medline]
Zhang, M., Xuan, S., Bouxsein, M. L., von Stechow, D., Akeno,
N., Faugere, M. C., Malluche, H., Zhao, G., Rosen, C. J., Efstratiadis, A. et
al. (2002). Osteoblastspecific knockout of the insulin-like
growth factor (IGF) receptor gene reveals an essential role of IGF signaling
in bone matrix mineralization. J. Biol. Chem.
277,44005
-44012.
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