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Institut National de la Recherche Agronomique, INRA – SCRIBE, IFR 140, Campus Beaulieu, 35000 Rennes, France
1 Department of Fisheries Sciences, Faculty of Agriculture and Natural Resources, University of Kurdestan, 416 Sanandaj, Iran
2 Departament de Fisiologia, Facultat de Biologia, Universitat de Barcelona, Avinguda Diagonal 645, E-08071 Barcelona, Spain
(Requests for offprints should be addressed to J-C Gabillard; Email: jean-charles.gabillard{at}rennes.inra.fr)
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResultsDiscussionReferences |
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Fish growth depends mostly on nutrient availability, known to modulate the GH/IGF system activity. Starvation increases plasma GH levels (Sumpter et al. 1991, Duan & Plisetskaya 1993, Pérez-Sánchez et al. 1995, Marchelidon et al. 1996, Weber & Grau 1999, Pierce et al. 2005) and pituitary GH content (Marchelidon et al. 1996, Weber & Grau 1999). In contrast, hepatic GH-binding capacities are lowered after several weeks of starvation (Gray et al. 1992, Pérez-Sánchez et al. 1994, 1995). Recently, it was shown that starvation decreased the expression of GHR mRNA in the liver (Deng et al. 2004, Fukada et al. 2004), but the effect of starvation on the gene expression of the two GHRs present in salmonids is unknown. It has been hypothesized that the hepatic resistance to GH would partly account for the low plasma levels of IGF-I observed in starved fish (Pérez-Sánchez et al. 1995, Baños et al. 1999, Shimizu et al. 1999) and that the increase in GH levels results from the decline of IGF-I feedback on GH cells. Nevertheless, the evidence for this hypothesis is still lacking and the possible role of IGF-II has never been explored.
IGFBPs are important components of the GH/IGF system, since they modulate IGF activity and availability, but the regulation of their expression by nutritional status is rare. Starvation increases plasma IGFBP-1 (Siharath et al. 1996, Shimizu et al. 1999, Kelley et al. 2001) and IGFBP-2 mRNA levels in zebrafish (Duan et al. 1999a, Maures & Duan 2002). Plasma IGFBP-3 is decreased in starved salmon (Shimizu et al. 2003), but no difference of IGFBP-3 mRNA abundance is observed in starved zebrafish (Chen et al. 2004). To date, nutritional regulation of IGFBP-4 to IGFBP-6 and IGFBP-rP1 is completely unknown in fish and their possible implication in muscle growth recovery has never been studied.
Although the effect of starvation on the GH/IGF system has been extensively studied, the time course of events leading to the restoration of the GH/IGF system activity after starvation is largely unknown. We, therefore, studied the plasma levels of GH, IGF-I, and IGF-II during refeeding as well as the expression profiles of the GH/IGF system genes in liver and muscle. This approach allowed us to show that plasma IGF-I was restored after plasma GH and that the muscular expressions of IGF-I, IGFBP-5, and IGFBP-rP1 were coordinated and associated with muscle growth recovery.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Two groups of female immature trout (Oncorhynchus mykiss), with a mean weight of 136 ± 10 g, were constituted. Three experimental groups (S1, S2, and S3) reared in triplicate (nine different tanks, 50 fish/tank) were starved for 1 month and refed for 1 month with food available ad libitum. The control group (reared in triplicate) had food available ad libitum throughout the experiment. Fish were reared in freshwater tanks (PEIMA-INRA, Sizun, France) under a natural photoperiod and fed with a commercial diet (BioMar, Nersac, France). The water temperature was 18 °C before starvation (day 30), 15.3 °C at day 0, and 12.3 °C at day 29.
Sample collection
Investigations were conducted according to the guiding principles for the use and care of laboratory animals and in compliance with French and European regulations on animal welfare. Before starvation (day 30) and at days 0, 1, 2, 4, 7, 15 and 29 days following refeeding, 12 fish (four per tank) were sampled for the experimental groups. To limit the stress caused by repeated sampling, fish were collected from group S1 on days 0, 4, and 15; from group S2 on days 1 and 7; and from group S3 on days 2 and 29. For the control group, 12 fish were sampled (four per tank) on days 0 and 29. Fish were anesthetized with eugenol (10 ml/l), killed by a blow on the head and blood was collected within 10 min.
Sample analysis
Plasma GH, IGF-I and IGF-II levels were measured by homologous RIA as previously described (Le Bail et al. 1991, Gabillard et al. 2003).
Total RNA was extracted from 100 mg tissue (muscle or liver) using TRIzol (Gibco BRL). This was quantified, based on absorbance at 260 nm (NanoDrop ND-1000 spectrophotometer), and the integrity was checked for all RNA samples on 1% agarose gel, stained with ethidium bromide. Then, 5 µg total RNA were used to perform the reverse transcription reaction (Applied Biosystems kit #N808-0234; Applied Biosystems, Foster City, CA,USA).
Quantitative PCR analyses were carried out with 5 µl reverse transcriptase (RT) reaction using a real-time PCR kit provided with an SYBR Green fluorophore (Eurogentec, Seraing, Belgium), according to the manufacturer’s instructions and using 600 nM of each primer (Table 1
). After a 2-min incubation step at 50 °C and a 10-min incubation step at 95 °C, the amplification was performed using the following cycle: 95 °C, 20 s; 62 °C, 1 min, for 40 times. The relative abundance of target cDNA within the sample set was calculated from a serially diluted (standard curve) liver cDNA pool using the iCycler iQTM software (Bio-Rad, Hercules, CA, USA). Subsequently, real-time PCR data were normalized using eF1a transcript abundance as follows:
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With this method, the correcting factor includes variations due to RT efficiency independent of changing eF1a due to treatment and (or) time. In our experiments, PCR results without normalization gave exactly the same tendency as that obtained by following our method of normalization with eF1a, but with a lower variability. Moreover, no correlation between eF1a and other parameters was observed, which confirm the reliability of our method.
Statistical analysis
The refeeding effect was analyzed with a one-way ANOVA using the non-parametric Wilcoxon/Kruskal–Wallis rank test. If a significant effect was found, the significance between two means was determined by the non-parametric Mann–Whitney’s U-test. All the data are presented as the mean ± S.E.M. All parameters measured were subjected to a principal component analysis (PCA) using PAST software, version 1.18, http://folk.uio.no/ohammer/past/; Hammer et al. 2001). Pearson’s linear regression was used to assess the relationship between IGF-I, IGFBP-5, and IGFBP-rP1 mRNA abundance.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Fish of the fed group grew rapidly during the experiment, whereas starved fish lost weight (136 ± 2.9 vs 125.9 ± 3.5 g; P < 0.05). Thereafter, fish grew rapidly as in the control group (Fig. 1).
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). Refeeding for 1 day restored plasma GH levels to those of the control fish. Thereafter, plasma GH continued to decrease and at days 4 and 7, GH levels were significantly lower than those measured on days 1 or 2. After 15 and 29 days of refeeding, GH levels were again similar to the values observed in the control fish. Plasma IGF-I levels were significantly decreased by 1 month’s starvation, leading to a threefold decrease in IGF-I levels in starved fish compared with the controls (9.9 ± 0.7 vs 34.8 ± 2.8 ng/ml; P < 0.001). Two days after refeeding, plasma IGF-I remained low. After 4 days, plasma IGF-I started to increase slightly, but it needed 2 weeks for the level to be restored compared with the control group. One month after refeeding, no difference in plasma IGF-I was seen between the controls and starved fish. The expression profile of IGF-I in the liver was similar to what was observed at plasma level. Nevertheless, it is noteworthy that after refeeding, IGF-I mRNA abundance continued to decrease up to 4 days.
Plasma IGF-II levels (Fig. 1) were also significantly decreased by 1 month’s starvation. At day 0, the IGF-II levels of starved fish were threefold lower than in control fish (26.5 ± 1.9 vs 86.8 ± 9.2 ng/ml; P < 0.001). At day 1, the plasma IGF-II level in refed fish had nearly doubled and thereafter increased progressively, but never reached the levels measured in the control fish for a given time. Indeed, even after 1 month of refeeding, plasma IGF-II levels in the control group were always higher (128 ± 9 vs 162 ± 16 ng/ml; P < 0.01). In control fish, plasma IGF-II levels increased throughout the experiment.
The expression profile of IGF-II in the liver was close to that observed at the plasma level. Indeed, it is noteworthy that a transitory peak of IGF-II expression occurred at day 2. Thereafter, as observed for plasma IGF-II level, IGF-II mRNA abundance increased progressively without reaching the IGF-II mRNA abundance measured in the control fish for a given date.
Expression profile of the GH receptor
Changes of GHR1 and GHR2 mRNA abundance in liver and muscle are shown in Fig. 2. In liver, 1 month of fasting stimulated the expression of the GHR1 gene compared with control fish (136 ± 26 vs 49 ± 9 A.U.; P < 0.01). By contrast, no obvious effect of starvation was observed on GHR2 gene expression in the liver. Whereas 1 day of refeeding decreased GHR1 mRNA abundance, an increase in GHR2 mRNA abundance was simultaneously observed. Thereafter, GHR1 mRNA decreased continuously until day 7, while GHR2 mRNA abundance returned to a level similar to that of the controls, as early as day 7. In muscle, 1 month of food deprivation raised both GHR mRNA abundances to the same extent (twofold) followed by a rapid return to control values after 4 days. At day 29, there was no longer any difference between the refed fish and the control groups.
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Changes of IGFBP-1 to IGFBP-6 and IGFBP-rP1 mRNA abundance in the liver are presented in Fig. 3. Among the seven genes studied, IGFBP-1, IGFBP-3, IGFBP-5, and IGFBP-rP1 did not exhibit obvious changes either after starvation or refeeding. IGFBP-2 and IGFBP-6 mRNA abundances were similar in starved and fed fish. Next, the mRNA abundances of both IGFBPs rose up to day 7 and then returned to values similar to those of control fish. After 29 days of refeeding, IGFBP-2 and IGFBP-6 mRNA abundances were similar to those of control fish. One month of food deprivation decreased IGFBP-4 mRNA abundance leading to sevenfold less mRNA in starved than in control fish (21 ± 6 vs 147 ± 32 A.U.; P < 0.01). Thereafter, from day 2, IGFBP-4 mRNA levels increased progressively and no difference between refed and control fish was any longer observed at day 29.
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. Among the seven IGFBPs/IGFBP-rP studied, only the IGFBP-1 expression profile could not be monitored above background level in the muscle. Starvation or refeeding influenced all IGFBP/IGFBP-rP gene expressions, except IGFBP-3 where no obvious effect on mRNA abundance was seen. After 1 month of starvation, IGFBP-2 mRNA abundance was lowered (69 ± 10 vs 152 ± 18 A.U.; P > 0.05) compared with the control group. A low level of IGFBP-2 mRNA was maintained until day 4, but from day 7, it was restored and was similar to that of the controls. IGFBP-4 mRNA abundance was also lower (twofold) in starved fish than in fed fish. Surprisingly, a sevenfold increase of IGFBP-4 mRNA abundance was monitored as soon as 1 day after refeeding, followed from day 2 by a return to a level comparable to that of control fish. The abundance of IGFBP-5 mRNA was also lower in starved than in control fish. A first peak of its mRNA abundance was observed at day 2 followed by a second one at day 7. Next, from day 15, IGFBP-5 mRNA abundance returned to a level similar to the control fish. It is noteworthy that the IGFBP-5 mRNA abundance at day 7 was above the level observed in the control fish. For IGFBP-6, the treatment had a weak, but significant (P < 0.05) effect on the mRNA level. One day of refeeding led to a significant decrease (60 ± 12 vs 130 ± 30 A.U.; P < 0.05), leading to a quick and complete restoration of IGFBP-6 mRNA levels. IGFBP-rP1 mRNA abundance was lower in starved than in control fish. A first peak of its mRNA abundance was observed at day 2 followed by a second one at day 7. Next, from day 15, IGFBP-rP1 mRNA abundance returned to a level similar to the control fish. While no obvious effect of the treatment was observed on the expression of IGF-II in muscle (Fig. 4), the response of IGF-I was very strong. Starvation led to a fivefold decrease of IGF-I mRNA abundance compared with control fish. As soon as 1 day of refeeding, the IGF-I mRNA level was restored. Thereafter, a peak of IGF-I expression (sevenfold higher compared with starved fish) was monitored at day 7 followed by a return to normal value from day 15. Myogenin mRNA abundance (Fig. 5) was measured as a marker of myogenesis activity. Starvation induced a threefold decrease of myogenin mRNA abundance compared with control fish. Thereafter, a peak of myogenin expression (fivefold compared with starved fish) was monitored at day 7 followed by a return to normal values from day 15.
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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In order to produce a strong disruption of the GH/IGF system, we starved rainbow trout for 1 month. As expected, food deprivation increased plasma GH levels and lowered plasma IGF-I and IGF-II levels, as previously reported in trout (Sumpter et al. 1991, Gentil et al. 1996, Shimizu et al. 1999). Since plasma IGF-I inhibits GH release (Blaise et al. 1995), it is often considered that the decrease of IGF-I leads to the increase in the GH levels. Likewise, when hepatic production of IGF-I was deleted in the mouse, plasma IGF-I was only 25% of the normal value and these mice exhibited a threefold higher GH level (Sjogren et al. 1999). In our study, refeeding rapidly restored plasma GH, since the plasma GH of refed fish was identical to that of the controls after 1 day. Surprisingly, plasma IGF-I started to increase only from day 4. Therefore, plasma IGF-I cannot account for the restoration of plasma GH during refeeding. This is reminiscent of a recent study on the time-course response of the GH/IGF system to fasting in salmon (Pierce et al. 2005). Indeed, during fasting, it has been observed that plasma GH increases before the plasma IGF-I decreases. Together, these results show that plasma IGF-I is not a key regulator of plasma GH level during starvation and refeeding. On the other hand, our results indicated that the plasma IGF-II doubled at day 1 when plasma GH decreased. Given that IGF-II can inhibit GH release (Blaise et al. 1995, Duval et al. 2002) and that plasma IGF-II levels are two- to fivefold higher than plasma IGF-I in the trout, it seems likely that plasma IGF-II could exert an in vivo negative control on GH release. Likewise, we previously reported a negative correlation between plasma GH and plasma IGF-II when fish were subjected to a moderate food restriction (Gabillard et al. 2003). In the present study, we also found a negative correlation between plasma GH and plasma IGF-II from days 0 to 4 (r = –0.68; P < 0.0001), whereas no correlation was found with plasma IGF-I. Therefore, the precocious increase in plasma IGF-II in addition to its high plasma concentration (compared with IGF-I) suggest that plasma IGF-II instead of IGF-I may be implicated in the plasma GH regulation during refeeding and perhaps during fasting. Our data also indicated that in the liver, the nutritional state differentially regulated IGF-I and IGF-II genes suggesting that they have a distinct function in endocrine control of growth.
As a result of the recent genome duplication, two genes coding for the GH receptor are present in rainbow trout and our study provides the first data on their regulation during starvation and refeeding. One month of food deprivation increased the hepatic GHR1 mRNA abundance, while GHR2 mRNA remained unchanged. In muscle, the levels of the two GHR transcripts were higher in starved fish than in controls. One day of refeeding is sufficient to restore GHR1 mRNA abundance in liver, whereas a peak of GHR2 mRNA was observed at day 1. In muscle both GHR mRNA abundances were restored after 4 days. A recent study performed in black seabream (Acanthopagrus schlegeli) reported a lower GHR mRNA level in liver of starved fish (Deng et al. 2004). This apparent discrepancy between these data and ours could be related to species differences as well as to the environmental conditions, since water temperature and salinity were not tightly controlled in the Deng et al. study. In salmon, the level of hepatic GHR mRNA was slightly lower in starved fish compared with fed fish (Fukada et al. 2004). However, in this latest study, primers were designed to amplify simultaneously the mRNA of both GHRs, which prevents conclusion about specific regulation of both GHR genes. Moreover, given that we observed an opposite effect of starvation on both GHR genes expression, the measurement of each gene appears essential for precisely understanding the regulation of GHR genes. Together, our results show that in trout, both GHR genes are differentially regulated during starvation and refeeding. In starved fish, the low plasma IGF-I level, with high plasma GH level, is considered to be the result of hepatic GH resistance in accordance with the low GH-binding capacities of the liver (Pérez-Sánchez et al. 1994, 1995). Given that the GHR mRNA level in liver rapidly returned to the normal control value, it cannot explain the late recovery of plasma IGF-I level. There is an apparent discrepancy between previous studies on GH-binding and our study on GHR gene expression in response to fasting. However, we recently reported in trout that high temperatures decrease hepatic GH-binding, but increase GHR mRNA levels (Gabillard et al. 2006). Furthermore, hepatic GH-binding is strongly influenced by circulating GH independent of the GHR protein expression (Yao et al. 2006). In salmon, Fukada et al.(2004) showed that as little as 1 week of fasting, decreased plasma IGF-I levels despite an increase of circulating GH. In this typical situation of hepatic GH resistance, GHR mRNA was unaffected within the first 2 weeks, suggesting that GHR mRNA in such a situation cannot explain hepatic GH resistance. Indeed, in mammals, it has been shown that fasting does not change the content of GHR protein, and that GH resistance is rather due to the impairment of the signal transduction pathway (Beauloye et al. 2002).
IGFBPs are important components of the GH/IGF system, since they modulate IGF activity and availability, but the regulation of their expression by nutritional status is largely unknown. Our data indicated that after 4 weeks of starvation, hepatic mRNA abundance of IGFBP-1 was similar between starved and fed fish. In zebrafish, starvation increased IGFBP-1 mRNA abundance (Maures & Duan 2002) to a lesser extent after 3 weeks (twofold) than after 2 weeks (fourfold). Therefore, it cannot be excluded that prolonged starvation (4 weeks in the present study) allowed the recovery of IGFBP-1 mRNA abundance. Starvation and refeeding did not alter IGFBP-3, IGFBP-5, and IGFBP-rP1 mRNA abundance in the liver suggesting that nutrient availability is not a key regulator of the expression of these genes in the liver. Together, these data suggest that the expressions of IGFBP-1, IGFBP-3, IGFBP-5, and IGFBP-rP1 in the liver are not key regulators in growth recovery after starvation. We observed that IGFBP-4 expression decreased after 4 weeks of starvation following a progressive recovery. This observation is reminiscent of that observed in mammals (Chen & Arnqvist 1994), but the physiological significance is still largely unknown. Interestingly, IGFBP-2 and IGFBP-6 exhibited a similar expression profile, i.e., no effect of starvation followed by a peak of mRNA abundance after 7 days of refeeding. The significance of the IGFBP-2 and IGFBP-6 peaks is not known but IGFBP-2 is known to inhibit IGF-I action in zebrafish (Duan et al. 1999a), and it is considered to be a marker of the catabolic state in fish (Kelley et al. 2001). Moreover, in humans, refeeding may lead to a transitory diabetes (Marinella 2005) which is known to increase IGFBP-2 mRNA levels in the liver (Chen & Arnqvist 1994). Therefore, during refeeding, changes of IGFBP-2 and IGFBP-6 mRNA levels could result from metabolic changes in the liver (Navarro & Gutierrez 1995, Pottinger et al. 2003) within the first weeks of refeeding.
In muscle, IGFBP-1 mRNA expression was not detected and IGFBP-3 mRNA was not influenced by the nutritional status. In zebrafish, 3 weeks of food deprivation did not significantly modify the IGFBP-3 mRNA abundance (Chen et al. 2004). Together, this suggests that IGFBP-1 and IGFBP-3 do not participate in muscle growth recovery. Starvation decreased IGFBP-2 mRNA levels as observed in zebrafish (Duan et al. 1999a) and refeeding started to restore IGFBP-2 mRNA levels from day 7, suggesting that it is not involved in the precocious events leading to muscle growth recovery. Starvation slightly increased IGFBP-6 mRNA abundance and refeeding quickly restored it. In terms of their differences in expression profile in liver and muscle, it appears that IGFBP-2 and IGFBP-6 should not have similar functions in muscle and liver. IGFBP-4 has a unique expression profile consisting of a lower mRNA abundance in starved fish, followed by a transitory but strong increase 1 day after refeeding. Given that in muscle, IGFBP-4 mRNA has been detected in connective tissue instead of muscle fibers (Jennische & Hall 2000), our observations suggest that the transitory increase of IGFBP-4 mRNA does not participate in myogenesis resumption.
IGFBP-5, IGFBP-rP1, and IGF-I exhibited similar responses to fasting and refeeding. Their expression profiles involved a decrease of mRNA abundance after starvation, and refeeding induced a first peak of expression at day 2, a second at day 7, and a complete restoration from day 15. Moreover, the mRNA abundance of these genes was highly correlated (r = 0.6 – 0.8; P < 0.0001). Therefore, our observation indicates that IGFBP-5, IGFBP-rP1, and IGF-I are coordinately regulated during refeeding. In this experiment and others by Chauvigné et al.(2003), we observed a peak of IGF-I mRNA expression, which was accompanied by a peak of myogenin. Given that myogenin is involved in the differentiation of myoblast (Florini et al. 1996), it is likely that the peak of IGF-I expression is associated with the resumption of myogenesis. Likewise, IGFBP-5 expression, which is upregulated by IGF-I in mammals (Duan et al. 1999b), is also stimulated during myoblast differentiation (James et al. 1993). Moreover, it has been shown that after injury IGFBP-5 expression is restricted to the regenerating muscle cell (Jennische & Hall 2000). In contrast, IGFBP-rP1 is upregulated in proliferative myoblast and downregulated in differentiating myoblast (Damon et al. 1997). Therefore, the elevation of IGFBP-5 mRNA would arise from differentiating myoblasts, whereas IGFBP-rP1 mRNA would arise from proliferating myoblasts. Together, our observations strongly suggest that the expression profiles of IGF-I, IGFBP-5, and IGF-rP1 are a signature of the resumption of myogenic activity.
In conclusion, the rapid return to a control value of the plasma GH and liver GHR1 expression is the first step of the restoration of GH/IGF system activity after starvation. Plasma IGF-I levels are restored after plasma GH levels, which does not support the present model according to which the elevation of plasma GH would result from the decrease of plasma IGF-I. Given the precocious restoration of plasma IGF-II levels, our study suggests a role of IGF-II instead of IGF-I in plasma GH level restoration. In muscle, our observations indicate that fasting and refeeding induced a coordinated regulation of IGF-I, IGFBP-5, and IGFBP-rP1 all of which are probably involved in a strong myogenesis resumption. Nevertheless, the functional analysis of IGFBP-5 and IGFBP-rP1 remains to be performed to fully understand their role in myogenesis.
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Acknowledgements |
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References |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Received 15 March 2006
Received in final form 7 June 2006
Accepted 20 June 2006
Made available online as an Accepted Preprint 14 July 2006
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