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1 Northwest Fisheries Science Center, NOAA Fisheries, 2725 Montlake Boulevard East, Seattle, Washington 98112, USA
2 School of Aquatic and Fishery Sciences, University of Washington, Seattle, Washington 98195, USA
3 Graduate School of Fisheries Sciences, Hokkaido University, 3-1–1 Minato, Hakodate, Hokkaido 041-8611, Japan
(Requests for offprints should be addressed to M Shimizu; Email: munetaka.shimizu{at}noaa.gov)
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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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IGF-I and IGFBPs are widely found among vertebrates including teleosts, and they appear to have co-evolved throughout the vertebrate lineage (Reinecke & Collet 1998). Evidence for at least five IGFBP sequences (IGFBP-1 to -5) can be found in zebrafish (Danio rerio) and fugu (Fugu rubripes) genome databases and their sequences show 40–60% homology to mammalian counterparts (Wood et al. 2005a). This conserved nature of IGFBP structure supports the concept that IGFBPs play a crucial role in regulating IGF-I action in vertebrates. In zebrafish, a series of studies based on IGFBP knockdown has shown that IGFBP-1, -2 and -3 regulate developmental rate under hypoxia, formation of the cardiovascular system and formation of the pharyngeal skeleton and inner ear (Kajimura et al. 2005, Li et al. 2005, Wood et al. 2005b). These studies argue for the importance of IGFBPs during development as well as during postnatal growth.
Endocrine IGF-I forms a large pool bound to IGFBPs in the blood. Although an essential role of endocrine IGF-I in the regulation of postnatal growth of mice has been questioned (Le Roith et al. 2001), its contribution to growth and metabolism is a subject of active investigation. Among the six IGFBPs present in the circulation of mammals, IGFBP-1 may be one of the most critical factors regulating the availability of circulating IGF-I to peripheral tissues (Lee et al. 1997). IGFBP-1 generally acts as an inhibitor of IGF-I action, presumably through sequestering free IGF-I. Unlike other IGFBPs, circulating IGFBP-1 shows a diurnal change in response to food intake (Busby et al. 1988, Cotterill et al. 1988). IGFBP-1 levels increase during fasting, and return to basal levels after a meal. This rapid change in IGFBP-1 is primarily due to the suppressive effect of insulin (Snyder & Clemmons 1990). However, amino acids also influence the synthesis of IGFBP-1 in rats (Straus et al. 1993). The increase in IGFBP-1 may be a mechanism by which the action of IGF-I is blocked to redirect energy during malnutrition. Circulating IGFBP-1 is also increased under other catabolic states such as prolonged exercise, stress, hypoxia and critical illness (Lee et al. 1997). These responses of IGFBP-1 may be mediated, at least in part, by glucocorticoids such as cortisol. Glucocorticoid stimulates IGFBP-1 production, but its stimulatory effect is secondary to the suppressive effect of insulin in mammals (Unterman et al. 1991).
Candidates for fish IGFBP-1 have been detected in the circulation of several teleosts (Siharath et al. 1996, Park et al. 2000, Kelley et al. 2001, 2002, Kajimura et al. 2003). Western ligand blotting of fish plasma/serum typically reveals three IGFBP bands at 20–25, 25–30 and 40–50 kDa. The two smaller forms may be fish IGFBP-1 and/or -2 based on their size and response to fasting and stress (Kelley et al. 2001). This is further supported by hormone treatments with insulin and cortisol (Kelley et al. 2001, Kajimura et al. 2003). However, because the exact identity of the lower molecular weight IGFBPs is obscure; it is not known if their physiological response is due to a conserved nature of the same type of IGFBP, or a similar regulation of different types of IGFBPs. In addition, there is no specific assay for fish IGFBP-1 available at present, which makes a detailed quantitative analysis difficult. We have recently purified a 22 kDa IGFBP from Chinook salmon serum, cloned its cDNA and identified it as a homolog of mammalian IGFBP-1 (Shimizu et al. 2005). Salmon IGFBP-1 lacks a PEST (Pro, Glu, Ser, Thr)-rich domain involved in rapid turnover of protein and an RGD (Arg-Gly-Asp) integrin recognition sequence (Shimizu et al. 2005), which might influence kinetics and function of circulating salmon IGFBP-1. Thus, the physiological role of IGFBP-1 in fish is unclear. The present study describes the development of an RIA for salmon IGFBP-1. With this RIA, we measured plasma IGFBP-1 in response to feeding ration and water temperature, and during the parr–smolt transformation; we then compared the IGFBP-1 levels to growth, condition factor, plasma IGF-I and 41 kDa IGFBP.
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Materials and Methods |
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Rearing conditions Yearling Chinook salmon (Oncorhynchus tshawytscha) and coho salmon (O. kisutch) were reared in fresh water at the Northwest Fisheries Science Center in Seattle (WA, USA). They were maintained in recirculated fresh water in circular fiberglass tanks under natural photoperiod; flowrate was 25 l/min and temperature ranged from 10·5 to 13·0°C. Before the fish were used for experiments, they were fed standard rations (0·6–1·0% body weight/day) of a commercial diet (Biodiet Grower; Bioproducts Inc., Warrenton, OR, USA). The experiments were conducted according to the guidelines of the University of Washington Institutional Animal Care and Use Committee.
Blood collection Fish were anesthetized in 0·05% tricane methanesulfonate (MS-222; Argent Chemical Laboratories, Redmond, WA, USA). Blood was withdrawn by cutting the caudal peduncle and letting the blood flow into a heparinized glass tube. Plasma was collected after centrifugation at 700 g for 15 min and stored at –80°C until use.
Effect of fasting Yearling Chinook salmon were fed at 52% of the maximum ration or fasted for 6 weeks (October to December). Blood was collected 6 weeks after treatment as described above.
Effect of feeding ration The detailed experimental design has been described in Beckman et al. (2004a). Briefly, yearling post-smolt coho salmon were individually tagged by passive integrated transponder (PIT) tags (Digital Angel, South St. Paul, MN, USA). From June to September, four groups of fish were fed at 2% (HiFeed) or 1% (MedFeed) body weight/day, and feeding rates were maintained (Constant) through the experiment or decreased to 0·5% body weight/day for 4 weeks and returned to their original feeding rates (Variable). These combinations created four feeding groups: HiFeedConstant, HiFeedVariable, MedFeedConstant and MedFeedVariable. Fish were sampled at 2-week intervals. Instantaneous growth rate was calculated as: growth (%/day)=(ln s2 – ln s1) x (d2 – d1)–1 x 100, where s2 is length or weight on day 2, s1 is length or weight on day 1 and d2 – d1 is the number of days between measurements. Condition factor was calculated as: body weight (g)/body length (cm)3 x 100. Five out of 147 fish were found to be precociously maturing males. IGFBP-1 levels in those fish were not included in the analysis since a disturbance in the relationship among IGF-I, 41 kDa IGFBP and growth rate has been reported in maturing males (Beckman et al. 2004a).
Effects of temperature and feeding ration The detailed experimental design has been described in Beckman et al. (2004b). Briefly, individually tagged 1-year-old coho salmon were reared at 11 °C (Warm) or 7 °C (Cool), and fed at 1·75% (HiFeed), 1·0% (MedFeed) or 0·5% (LowFeed) for 9 weeks (June to August). These combinations created four treatment groups: WarmHiFeed, WarmMedFeed, CoolMedFeed and CoolLowFeed. Fish were sampled at 2- or 3-week intervals.
Parr–smolt transformation One-year-old coho salmon undergoing the parr–smolt transformation were sampled for blood every 2 weeks from March to July as described previously (Shimizu et al. 2003).
Sample analyses
Plasma IGF-I levels were measured by RIA as described in Shimizu et al.(2000). Briefly, IGF-I was first extracted from plasma by acid-ethanol and quantified by the RIA using recombinant salmon IGF-I as standard and tracer, and anti-recombinant barramundi IGF-I as primary antibody (GroPep Pty Ltd, Adelaide, Australia). Plasma 41 kDa IGFBP was quantified by a homologous salmon RIA as described in Shimizu et al.(2003). In this RIA, tracer was prepared from cross-linking purified 41 kDa IGFBP with 125I-labelled IGF-I.
Purification of salmon IGFBP-1
IGFBP-1 was purified from the serum of spawning male Chinook salmon (Shimizu et al. 2005). Briefly, salmon serum was first fractionated by ammonium sulfate precipitation and loaded onto an IGF affinity column. IGFBP-1 was eluted from the column with 0·5 M acetic acid and further purified by reversed-phase HPLC on a Vydac C-4 column (0·46 x 5 cm; Separation Group, Hesperia, CA, USA). Purified IGFBP-1 was quantified with the BCA protein assay kit (Pierce Chemical, Rockford, IL, USA), aliquoted into pre-lubricated microcentrifuge tubes (PGC Scientifcs, Frederick, MD, USA) and stored at –80 °C until use.
Preparation of antiserum
Polyclonal antiserum against purified IGFBP-1 (anti-IGFBP-1) was raised in a rabbit. Immunization of the rabbit was conducted in accordance with the guidelines of the Animal Care Committee of Hokkaido University, Japan. A total of 52 µg purified protein in 1 ml were emulsified in an equal volume of Freund’s complete adjuvant (Iatoron, Tokyo, Japan). The rabbit was first immunized with 24 µg antigen by lymph node injection and this was boosted subcutaneously with 28 µg antigen 3 weeks after the first injection. Two weeks after the boost, blood was withdrawn from the ear vein and antiserum was collected after centrifugation. The antiserum was stored at –30 °C until use.
Preparation of tracers
Purified IGFBP-1 was iodinated with 0·5 mCi Na125I (Amersham) by the chloramine-T method; 5 µg IGFBP-1 in 31 µl were mixed with 41 µl 0·5 M phosphate buffer, pH 7·4. The mixture was reacted with 20 µl of 0·4 mg/ml chloramine-T (Sigma) for 90 s and 20 µl of 0·6 mg/ml metabisulfite was added to stop the reaction. Iodinated IGFBP-1 (125I-labelled IGFBP-1) was separated from free Na125I using Biogel P-6 (1 x 18 cm; BioRad). An aliquot of 125I-labelled IGFBP-1 (1·3 µg) was incubated with 4·3 µg salmon IGF-I (GroPep Pty Ltd, Adelaide, Australia) for 2 h and they were cross-linked by disuccinimidyl suberate (Pierce Chemical) according to manufacturer’s instruction. The 125I-labelled IGFBP-1 cross-linked with salmon IGF-I (125I-labeled IGFBP-1/IGF-I) was separated from non-reacted IGF-I by gel filtration using Sephadex G-50 (1 x 18 cm, superfine; Pharmacia). Specific activity of the tracer estimated by the self-displacement assay was 69·9 µCi/µg.
RIA for salmon IGFBP-1
The RIA was carried out in 12 x 75 mm polystyrene test tubes. Purified IGFBP-1 was used for the standard. Standard (100 µl) or plasma (10–20 µl) diluted in 20 mM phosphate, 150 mM NaCl, pH 7·4 containing 1·0% BSA and 0·05% Triton-X-100 were incubated with 100 µl anti-IGFBP-1 at a dilution of 1:2500 overnight at 4 °C. Approximately 7000 c.p.m. of tracer in 100 µl were added to the tubes and incubated overnight at 4 °C. Free and antibody-bound tracers were separated by the addition of 0·5% Pansorbin (Calbiochem-Novabiochem Corp., La Jolla, CA, USA). After incubating overnight at 4 °C, tubes were centrifuged at 1350 g for 30 min and the supernatant was aspirated. Radioactivity in the pellets was measured by a gamma counter (Packard, Meriden, CT, USA). Standard and plasma samples were run in triplicate and duplicate respectively, unless otherwise indicated.
Statistical analyses
Values of IGFBP-1, IGF-I and body weight were natural-log transformed to improve normality of distribution. Results of the experiments were analyzed by paired Student’s t-test, unpaired t-test or one-way ANOVA followed by the Fisher’s protected least-significant difference (PLSD) test using the Statview 512+ program (Abacus Concepts, Inc., Berkeley, CA, USA). Simple regression was used to assess the relationship of IGFBP-1 to growth and other parameters. Differences between groups were considered to be significant at P < 0·05.
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Results |
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). Adding an excess amount of salmon IGF-I (1:100 molar ratio) to the standard did not alter the curve. The same lack of effect was seen with human IGF-I and IGF-II at various ratios (1:1, 1:10 and 1:100; data not shown). Cross-reactivity of other salmon IGFBPs in the RIA using 125I-labeled IGFBP-1/IGF-I was examined (Fig. 2). The 41 kDa IGFBP had no effect on displacing the binding. The 28 kDa IGFBP showed some displacement at higher concentrations, but its cross-reactivity was less than 0·5%, showing that the RIA is specific to IGFBP-1.
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The effect of IGFs on measured IGFBP-1 was assessed by adding varying concentrations of IGFs to the plasma (Table 1). Salmon IGF-I, human IGF-I and human IGF-II had no effect on IGFBP-1 levels up to 100 ng/ml, whereas 1000 ng/ml human IGFs significantly altered measured IGFBP-1 levels (paired t-test, P < 0·05). However, because circulating IGF levels in salmon rarely exceed 100 ng/ml and because the rank of IGFBP-1 levels in individuals was not altered, the IGF effect is not, in practice, a problem in the assay. Recoveries of purified IGFBP-1 added to plasma with and without salmon IGF-I were 90·3–94·9% and 94·3–103·3% respectively. These data show that IGFs do not interfere with the RIA. The RIA was also biologically validated as fasted fish had higher IGFBP-1 levels than fed fish (21·6 ± 4·6 ng/ml vs 3·0 ± 2·2 ng/ml, n=11–14), which is in agreement with Western blotting analysis (Shimizu et al. 2005).
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). When fish were reared under two different feeding rations (HiFeed and MedFeed), IGFBP-1 levels were higher in MedFeed groups (Fig. 3b). In the HiFeedVariable group, a decrease in feeding ration caused an increase in IGFBP-1 within 2 weeks. A subsequent increase in feeding back to the original amount caused a decrease in IGFBP-1 to the original level. In the MedFeedVariable group, the same trend was seen in response to a decrease in feeding ration except that the elevation in IGFBP-1 took 4 weeks to be significant.
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. For most dates, IGFBP-1 was negatively correlated with body weight, condition factor, growth rates and 41 kDa IGFBP. No significant relation was found between IGFBP-1 and IGF-I on any given date (Table 2, Fig. 4b), whereas a consistent positive relation was evident between 41 kDa IGFBP and IGF-I (Fig. 4a). IGFBP-1 appears to show the strongest negative relationship to condition factor (Table 2, Fig. 4c).
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). Although IGFBP-1 levels fluctuated during the first two sampling dates, they were separated by temperature (Fig. 5b). On the third sampling date, feeding ration became a major factor separating IGFBP-1 levels. Temperature may still have some effect as the differences in IGFBP-1 levels were close to being significant between WarmMedFeed and CoolMedFeed (P=0·0521). At the end of the experiment, IGFBP-1 levels were ranked by feeding ration only.
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). The change in IGFBP-1 was opposite to the change in condition factor (Fig. 6c and d). The inverse relationship between IGFBP-1 and condition factor was best represented by an exponential curve fitting (r2=0·416, P < 0·0001).
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Discussion |
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Elevation of circulating IGFBP-1 during fasting is a well-known response in a wide range of vertebrates including fish (Busby et al. 1988, Siharath et al. 1996). In most experiments, the two extreme nutritional conditions of fasting and feeding ad libitum were compared. On the other hand, much less is known about the response of IGFBP-1 to moderate nutritional change. In humans, caloric restriction of 50% for 6 days resulted in an increase in plasma IGFBP-1 in adults but not in children (Smith et al. 1995). Dietary energy restriction of 42·5 and 56% for 2 weeks had no effect on IGFBP-1 in dogs (Maxwell et al. 1998). Plasma IGFBP-1 levels decreased in guinea pigs fed rations of 70% of ad libitum feeding levels for 80 days (Sohlström et al. 1998). These results indicate that changes in IGFBP-1 in response to moderate feed restriction differ depending on stage and species. In the present study, the effect of ration on circulating IGFBP-1 was assessed in growing coho salmon. When the ration was reduced from 2% to 0·5% body weight per day, IGFBP-1 increased at 2 weeks, whereas reducing the ration from 1% to 0·5% increased IGFBP-1 at 4 weeks. The later response with the more moderate reduction in ration suggests that the relative change in food intake is an important cue for inducing IGFBP-1. Alternatively, the fish fed on the higher ration (2%) may be more sensitive to a reduction in food intake. The response of IGF-I and 41 kDa IGFBP levels to ration reduction was generally opposite to that of IGFBP-1; they declined by 2 weeks after the 2% to 0·5% ration change (Beckman et al. 2004a). However, IGF-I did not decline in response to the 1% to 0·5% ration change, suggesting that IGFBP-1 may be more sensitive than IGF-I to ration change. Overall, the results indicate that IGFBP-1 is quite responsive to moderate ration change in salmon.
Environmental temperature is a crucial factor affecting metabolic rate of poikilotherms and the change in the metabolic setting with temperature, in turn, may alter the endocrine system. In Atlantic salmon (Salmo salar), hormonal changes associated with parr–smolt transformation were limited by lowering temperature (McCormick et al. 2000). A relatively short-term effect of temperature change (1 week) on insulin and IGF-I levels has been reported in coho salmon; a drop of temperature increased insulin and decreased IGF-I respectively (Larsen et al. 2001). Temperature also affects IGFBP in catfish (Ictalurus punctatus) (Johnson et al. 2003). Increasing temperature from 21 to 26 °C resulted in an induction of a 19 kDa IGFBP whereas other IGFBPs remained unchanged. We have previously shown that salmon 41 kDa IGFBP as well as IGF-I was temporally affected by temperature (Beckman et al. 2004b). In the present study, temperature change appeared to disrupt IGFBP-1 levels for at least 6 weeks as feeding level had little relation to plasma IGFBP-1 level until the seventh week of the experiment. After this acclimation period feeding level again appeared to be the primary determinant of IGFBP-1 as fish receiving less feed had higher levels and temperature had no effect on IGFBP-1 at the end of the experiment (9 weeks). These results suggest that it took 9 weeks for fish to adjust IGFBP-1 levels to the different temperature. The response of IGF-I, 41 kDa IGFBP and IGFBP-1 to temperature change appears to differ. Lowering temperature resulted in a decrease in IGF-I and an increase in 41 kDa IGFBP (Beckman et al. 2004b), whereas the IGFBP-1 response occurred in both directions. Gabillard et al.(2003) found that higher environmental temperature increased plasma GH levels in rainbow trout (O. mykiss). These findings suggest that temperature influences the somatotropic axis not simply through changing metabolic rate, which would result in all components of the axis changing similarly, but through specific responses for each component.
We also studied changes in circulating IGFBP-1 levels during smoltification, which is a pre-adaptation to ocean life accompanied by many hormonal changes including IGF-I (Dickhoff et al. 1997). Shimizu et al.(2003) reported that IGF-I levels showed two peaks during the smolting process; one in late March and one in late April. In the present study, plasma IGFBP-1 levels in the same samples used in Shimizu et al.(2003) showed a peak in late April, which corresponds to the second peak in IGF-I. However, IGFBP-1 and IGF-I levels were not correlated (data not shown) similar to the result in the feeding experiment. The increase in IGFBP-1 may be driven by an increase in cortisol, which becomes elevated during smoltification. In contrast, a peak of 41 kDa IGFBP corresponded to the first peak in IGF-I, and their levels were positively correlated. These findings indicate that the IGF-I/IGFBP system changes during smoltification and suggest different roles for IGFBP-1 and 41 kDa IGFBP in this process. The significance of the change in IGF binding proteins during smoltification is unknown.
We analyzed the relationship of IGFBP-1 to growth, fish size, condition factor, IGF-I and 41 kDa IGFBP in individually tagged fish from the feeding experiment. Simple regression analysis revealed a clear trend that circulating IGFBP-1 level is negatively correlated with body weight, condition factor, growth rate and 41 kDa IGFBP. These results support the hypothesis that IGFBP-1 is generally inhibitory to growth. Our findings are in agreement with studies in humans showing that IGFBP-1 is inversely related to anthropometric and endocrine factors (Travers et al. 1998, Voskuil et al. 2001, Wolk et al. 2004). Among the growth and morphometric factors tested in the present study, the strongest and most consistent negative relation was with condition factor (body weight/body length3). The negative relation between IGFBP-1 and condition factor was present in both sets of data analyzed; one from the ration manipulation and the other from the smoltification study. In the experiment where some fish received reduced ration, the decline in condition factor was due to a greater loss in weight relative to growth in length. Growth in length ceased but did not become negative, and some individual fish lost weight due to dietary restriction. The group that went from 2% to 0·5% ration had a significant weight loss by 2 weeks. In the study of smoltification, it is well established that the decline in condition factor is due to a more rapid growth in length relative to growth in weight (Winans & Nishioka 1987). Thus, the inverse relationship between IGFBP-1 and condition factor is present during nutritional restriction and development of growing fish. In humans a strong relationship was observed between IGFBP-1 and body mass index (BMI; body weight/height2), which is similar to the condition factor in fish. The inverse relationship in humans held for early pubertal children (Travers et al. 1998), pre-menopausal women (Voskuil et al. 2001), and middle-aged and elderly men (Wolk et al. 2004). The underlying mechanisms for the relationship of lean body index and high IGFBP-1 in humans and salmon is not known, but invites additional study in other species.
Findings from the present study support different roles of salmon 41 kDa IGFBP and IGFBP-1 in regulating IGF-I activity. The 41 kDa IGFBP is the main carrier of circulating IGF-I as its levels are generally highly correlated with IGF-I levels (Shimizu et al. 2003, Beckman et al. 2004a, b). On the other hand, salmon IGFBP-1 can not be a main carrier of IGF-I because of: (a) the lack of correlation with IGF-I levels and (b) the fact that the molar concentrations of IGFBP-1 in blood are an order of magnitude lower than those of total IGF-I and 41 kDa IGFBP. In mammals, IGFBP-1 is postulated to be an important regulator of free IGF-I levels, which are biologically active and available to bind with IGF receptor (Frystyk et al. 1994). This hypothesis has recently been tested by in vivo infusion of human IGFBP-1 into catheterized rats. Infused human IGFBP-1 did not significantly alter the plasma concentration of total IGF-I, but decreased circulating free IGF-I levels (Lang et al. 2003). Although free IGF-I levels were not measured in the present study, a possible role of salmon IGFBP-1 in the regulation of free IGF-I may explain why IGFBP-1 shows no correlation with total IGF-I despite negative correlation with growth rates.
In conclusion, we developed a specific RIA for salmon IGFBP-1 for the first time and analyzed its regulation by food intake and temperature, and during smoltification. A range of moderate nutritional and temperature manipulations indicate that they are critical factors controlling circulating salmon IGFBP-1 levels. Regression analysis revealed that plasma IGFBP-1 is negatively correlated with growth and condition factor, among other factors. These findings suggest that the growth-inhibitory action of IGFBP-1 is conserved in salmon.
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Acknowledgements |
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Funding |
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This project was supported by a National Research Initiative Competitive Grant (2003–35206–13631) from the USDA Cooperative State Research, Education, and Extension Service, and by Bonneville Power Administration (Projects 2002–003100 and 1993–05600). The authors declare that there is no conflict of interest that would prejudice the impartiality of this scientific work.
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References |
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Received 18 October 2005
Accepted 24 October 2005
Made available online as an Accepted Preprint 15 November 2005
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