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Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan
3To whom correspondence should be addressed. E-mail: noguchi{at}bio.m.u-tokyo.ac.jp
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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6-fold
greater in the AA- group. Differences in plasma IGFBP-1
concentration under these conditions could be explained by differences
in hepatic IGFBP-1 mRNA contents. Based on these results, we conclude
that restriction of single EAA does not affect IGFBP-1 synthesis in
vivo, although the deprivation of a single EAA has been reported to
increase IGFBP-1 production in hepatocyte cultures. Our results also
indicated that a single EAA restriction decreased IGF-I production
but did not affect IGFBP-1 production. The present study suggests that
not only plasma IGF-I, but also IGFBP-1, affects the magnitude of
growth retardation in vivo.
KEY WORDS: • essential amino acid • insulin-like growth factor–binding protein-1 • mRNA • rats
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). This hormone is
complexed with several specific IGF binding proteins (IGFBP) in plasma.
At least six distinct IGFBP (IGFBP-1 through -6) have been
characterized, and these IGFBP have been suggested to modify the
biologic activity of IGF-I (Jones and Clemmons 1995
,
Rajaram et al. 1997
, Zapf 1995
).
Previous studies showed that plasma concentration and liver mRNA
content of IGFBP-1 are regulated by nutritional factors such as
fasting, restriction of energy intake and protein intake (Busby et al. 1988
, Ooi et al. 1990
, Murphy et al. 1990
, Straus et al. 1993
, Lemozy et al. 1994
, Takenaka et al. 1996
). Hepatic IGFBP-1
mRNA content increases during protein deprivation, and this is
attributed to the higher transcription rate of its gene (Miura et al. 1993
, Takenaka et al. 1996
, Tseng et al. 1992
). Although rats fed a protein-free diet had
greater mRNA content of IGFBP-1 [11-fold compared with those fed a
control (Con) diet], rats fed a diet containing 12% gluten, which was
deficient in Lys and Thr, had same IGFBP-1 mRNA level as the Con group
(Takenaka et al. 1993
).
By contrast, the effect of EAA starvation on IGFBP-1 synthesis in vitro
has been reported using hepatoma cell lines and primary cultured rat
hepatocytes (Arany et al. 1993
, Jousse et al. 1998
, Pao et al. 1993
, Straus et al. 1993
, Thissen et al. 1994
), and it was revealed
that the deprivation of a single essential amino acid (EAA) greatly
increased IGFBP-1 gene expression (Jousse et al. 1998
,
Straus et al. 1993
). There is a discrepancy between the
conclusions from in vivo and in vitro systems.
In the present study, we performed animal experiments to investigate the effect of the restriction of a single EAA on plasma concentrations of IGF-I and IGFBP-1 and on liver content of IGFBP-1 mRNA, as well as the effect on animal growth, and showed that the response of IGFBP-1 synthesis in vivo may be different from that in cultured liver cells.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Recombinant human IGF-I and anti-human IGF-I polyclonal
antibody were kindly donated by Fujisawa Pharmaceutical (Osaka, Japan).
Anti-rabbit 
-globulin polyclonal antibody and rabbit serum were
purchased from Daiichi Radioisotope Labs (Chiba, Japan). Labeled sodium
iodide (Na-125I) and 5'-[
-32P]dCTP
were obtained from Amersham Life Science (Buckinghamshire, U.K.). Other
chemicals were of reagent grade and available commercially. Rat IGFBP-1
was purified from the cell culture medium of H4IIE rat hepatoma cells.
IGFBP-1 antiserum was obtained by immunization of adult female rabbit
with the purified rat IGFBP-1 protein.
Diets.
The experimental diets contained different nitrogen sources. The Con
diet contained the complete amino acid (AA) mixture recommended by the
National Research Council (1978).
The diets deficient in
one EAA (Leu-, Lys-, Met- or
Thr-) contained an AA mixture in which the single EAA was
reduced to 20% of the level of the Con diet; the AA-free diet
(AA-) contained no AA. The compositions of the diets are
shown in Table 1
. Toeliminate the effect of reduced food intake in rats fed the
AA-deficient diets, the food intake of rats fed diets restricted in
a single EAA and of rats fed the Con diet (Con/paired) was restricted
to that of rats fed the AA- diet. One group was
fed the Con diet ad libitum (Con/ad libitum).
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Male rats of the Wistar strain with a mean body weight of 120 g (6
wk old) were purchased from Charles River Japan (Kanagawa, Japan). The
rats were housed under constant conditions of temperature (22
± 1°C) and light (on at 0800 h, off at 2000h), with free
access to water. After the rats were fed a Con diet from 1000 to
1800 h for 4 d, they were divided into seven experimental
groups (n = 5) and were fed the experimental diets
from 1000 to 1800 h for 7 d. On d 8 at 1130 h, the rats
were killed under pentobarbital anesthesia (50 mg of pentobarbital/kg
of body weight). The livers were removed, quickly frozen in liquid
nitrogen and kept at -70°C until the time of analysis. Blood
was collected in tubes containing 10 mg EDTA on ice. Samples were
centrifuged, and the plasma was kept at -20°C until assayed.
Body weight changes, food intake and plasma IGF-I concentrations of
the rats are shown in Table 2
. The procedures for animal research were approved by the Committee on
Laboratory Animal Care, Graduate School of Agricultural and Life
Sciences, The University of Tokyo.
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Acid gel chromatography was used as described previously
(Crawford et al. 1992
, Uchijima et al. 1995
) to eliminate the effect of IGFBP. RIA for IGF-I was
performed as described previously (Higashi et al. 1998
).
RIA of plasma IGFBP-1.
An excess amount of IGF-I was added to the RIA reaction to
eliminate the endogenous IGF-I in plasma, because binding of
125I–IGFBP-1 to the antibody was affected by IGF-I
(Lewitt et al. 1992
). Two hundred µL of plasma or the
standard solution (3.3 x 10-13 to 6.6 x 10-11 mol IGFBP-1/L) was added to 100 mL of 6.5
x 10-3 g IGF-I/L, 10,000 dpm of
125I–IGFBP-1 and 100 mL of 1000x diluted anti–IGFBP-1
antiserum and reacted in RIA buffer (2.5 g bovine serum albumin,
0.1 g Triton X-100, 0.2 g sodium azide and 0.1 mol phosphate
buffer, pH 6.5, per L) for 18 h at 4°C. Then, 10 mL of 10x
diluted anti-rabbit immunoglobulin antiserum and 100 mL of 40x
diluted normal rabbit serum were added, and incubation was conducted
for 30 min at 4°C. After the 30-min incubation with 1 mL of
polyethylene glycol (PEG) solution [60 g PEG 6000 and 1.5 g NaCl
per L], the samples were centrifuged at 1000 x g
for 20 min, and the radioactivity of the precipitant was measured with
a -counter.
Rat IGFBP-1 was purified from the cell culture medium of H4IIE rat
hepatoma cells by ammonium sulfate precipitation,
phenyl-Toyopearl and DEAE-Toyopearl chromatography (Tosoh,
Tokyo, Japan) and C4 reverse phase HPLC. Purified rat IGFBP-1 was used
as the standard and for the preparation of 125I-IGFBP-1.
IGFBP-1 was labeled using Na-125I and chloramine-T (as
described by Iwaki, Takahashi and Noguchi, unpublished). Anti–IGFBP-1
antiserum was prepared by immunization of female New Zealand White
rabbits with the purified IGFBP-1. Purified rat IGFBP-1 (100 mg) was
dissolved in 1 mL of phosphate-buffered saline, homogenized with an
equal volume of Freund’s complete adjuvant and injected subcutaneously
into female rabbit. At 2 and 5 wk after the first injection, a second
and a third injection were carried out using Freund’s incomplete
adjuvant. Blood was collected 2 wk after the third injection, and this
serum was used as an antiserum for rat IGFBP-1 (as described in Iwaki,
Takahashi and Noguchi, unpublished). Cross-reactivity of the
antiserum against other IGFBP and the parallel displacement curve of
IGFBP-1 standard and serum was evaluated (Iwaki et al. unpublished).
Our replacement curve confirmed the results reported by Lewitt et al. (1992).
Preparation of total RNA from rat liver followed by Northern blot analysis of IGFBP-1.
Total RNA was prepared from liver according to the modified method of
acid guanidinium thiocyanate-phenol-chloroform extraction
(Chomczynski and Sacchi 1987
, Puissant and Houdebine 1990
), as described previously (Miura et al. 1992
).
Northern blot analysis was performed as described previously
(Miura et al. 1992
). The cDNAs of rat IGFBP-1 were used
as probes, as described previously (Takenaka et al. 1991
). The intensity of each band obtained from a Northern blot
was quantified with the Fujix BAS 2000 or 3000 system (Fuji Film,
Tokyo, Japan).
Statistics.
Data were statistically analyzed by Duncan’s multiple range test
(Duncan 1955
) after one-way ANOVA. Liver IGFBP-1
mRNA content and plasma IGFBP-1 concentrations were compared using the
Mann-Whitney test for nonparametric data. Differences were
considered significant at P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Food intake was reduced to 58.9% (P < 0.01) and body
weight gain was reduced to 18.8% (P < 0.01) in the
Con/paired group compared with the Con/ad libitum group (Table 2)
. The
body weights of all groups fed EAA-restricted diets
(Leu-, Lys-,
Met- or Thr-) or the diet
devoid of AA (AA-) were lower than that of the
groups fed the Con diet, and the loss of body weight was significantly
greater in the AA- group than in groups fed
diets with a single EAA restriction (Table 2)
.
Plasma IGF-I concentration.
The reduced food intake did not affect plasma IGF-I
concentration. Plasma IGF-I concentration was significantly lower
than that of the Con group in the groups fed the EAA-restricted
diets and the AA- diet (P < 0.05). These groups did not differ from each another (Table 2)
.
Plasma IGFBP-1 concentration and liver IGFBP-1 mRNA content.
The hepatic content of IGFBP-1 mRNA did not differ significantly in the
rats fed diets with a single EAA restriction compared with the two Con
groups, whereas the level of the AA- group was
25-fold greater than that of the Con groups (Fig. 1A
). The plasma IGFBP-1 concentration was not significantly
affected by single EAA restrictions, except for that of Met
(P < 0.01); however, it was 6-fold greater in the
AA-deprived rats (AA-) than in the Con rats
(Fig. 1B
).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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) and a higher liver IGFBP-1 mRNA
content and plasma IGFBP-1 concentration (Takenaka et al. 1993
, Umezawa et al. 1991
). We have also shown
in vivo that feeding rats a 12% gluten diet, which was marginally
deficient in lysine and threonine, did not affect the hepatic IGFBP-1
mRNA content or the transcription rate of the IGFBP-1 gene compared
with that of the rats fed a 12% casein diet (Miura et al. 1993
, Takenaka et al. 1993
). The plasma
concentration of IGFBP-1 determined by specific RIA did not differ in
the rats fed the gluten diet and was 5- to 10-fold greater in rats
fed protein-free diets (Iwaki, Takahashi and Noguchi, unpublished
data). These studies indicate that deficiencies of lysine and threonine
did not affect IGFBP-1 synthesis in vivo.
On the other hand, in previous reports using the rat hepatoma cell line
H4IIE, IGFBP-1 mRNA was higher after deprivation of a single EAA from
the experimental medium, which was explained by the greater
transcription of the IGFBP-1 gene (Straus et al. 1993
).
A recent study by Jousse et al. (1998)
demonstrated that
when HEP G2 cells are deprived of each EAA from the medium, the IGFBP-1
mRNA content was higher than in the cells with control medium. These
studies suggested that the effect of EAA deficiency on hepatic IGFBP-1
synthesis may be different in cultured liver cells and rat liver in
vivo.
To investigate the effect of single AA deficiency on hepatic
IGFBP-1 synthesis in vivo, in the present study we prepared four
EAA-restricted diets (Leu-,
Lys-, Met- or
Thr-) that contained AA mixtures with each EAA
restricted to 20% of the level of the complete AA mixture recommended
by the National Research Council. In a series of studies, we used
casein, gluten and soy proteins, which are marginally deficient in
methionine, lysine and threonine, and methionine, respectively, as
nitrogen sources (Miura et al. 1992
). Therefore, we
selected these AA to be restricted in the present study. Leucine was
selected because its regulatory effect on IGFBP-1 mRNA content has been
well studied in hepatocyte cultures (Jousse et al. 1998
,
Straus et al. 1993
). We restricted the EAA to only 20%
to avoid energy malnutrition, which usually occurs in rats fed a diet
devoid of each EAA. As a result, we found that feeding rats each of
these diets restricted in one of the four AA did not affect the hepatic
IGFBP-1 mRNA level or plasma IGFBP-1 concentration except Met
-. Because deprivation of each of these four AA
had an effect to elevate IGFBP-1 mRNA content in cell culture system
(Jousse et al. 1998
), we concluded that the effect of a
single EAA deficiency on IGFBP-1 synthesis differs between in vivo and
cell culture systems. We could not rule out the possibility that the
restriction condition in the present study may not be sufficient to
induce IGFBP-1 synthesis. However, the effects of dietary AA deficiency
was sufficient to affect IGF-I system in the present study because
plasma IGF-I concentration of rats fed a diet with a single EAA
restriction was comparable to that of total AA deprivation.
The intracellular pool of each AA in organs is thought to be affected
by AA concentrations in plasma and the supply of AA degraded from
endogenous proteins. Intracellular levels of each AA are one of the
most likely candidates to modulate IGFBP-1 gene transcription
(Takenaka et al. 2000
). Accordingly, differences in
intracellular pools of each EAA between liver in vivo and cultured
hepatocytes may in part explain the difference between the effect of AA
restriction on IGFBP-1 mRNA content in vivo and in hepatocyte culture
systems.
Rats fed protein-free diets had a higher IGFBP-1 mRNA content, as
well as transcription rate of the IGFBP-1 gene (Miura et al. 1993
). In addition, we found that the 5' upstream region of
IGFBP-1 plays some role in increasing IGFBP-1 mRNA in response to AA
deprivation in human hepatocyte cultures (Takenaka et al. 2000
). These results suggest that transcription of the IGFBP-1
gene was greater in dietary AA-deprived condition and imply that
transcription regulation in response to single EAA deficiency is
different between liver in vivo and hepatocytes cultures.
In contrast to IGFBP-1, rats fed diets with a single EAA restriction
had a dramatically lower plasma IGF-I concentration to the level of
that of rats totally deprived of AA (Table 2)
. We have shown that the
AA deficiency lowered hepatic IGF-I mRNA (Miura et al. 1992
). Because the AA deficiency did not significantly affect
the transcription rate of the IGF-I gene in liver in vivo, we
concluded that AA deficiency lowers the stability of IGF-I mRNA
(Miura et al. 1993
). Because plasma IGF-I
concentrations of single EAA-restricted rats were comparable to
that the rats fed protein-free diets (Table 2)
, the restriction of
a single EAA could be monitored by an unknown system and is sufficient
to provide signals to destabilize IGF-I mRNA. In the case of
IGF-I regulation, similar results were obtained in liver in vivo
and in cell culture systems. All of these results indicate that the
synthesis of IGF-I is suppressed posttranscriptionally, but
transcription of IGFBP-1 gene is greater under dietary AA-deprived
conditions. The different molecular mechanisms of the transmission of
signals of AA deficiency to the machinery for IGF-I or IGFBP-1
synthesis may explain the different effects of the single EAA
restriction on plasma concentrations of IGF-I and IGFBP-1 in the
present study.
We reported that the levels of plasma IGF-I concentrations
correlated well with growth rate when rats were fed diets with
different protein contents (Takahashi et al. 1990
).
However, we show in the present study that in rats fed diets without
AA, body weight loss was more severe than in a single
EAA-restricted groups, despite the fact that there was no
significant difference in plasma IGF-I concentration. The different
responses of IGFBP-1 synthesis to restriction of a single EAA and total
AA deprivation may explain this discrepancy between the body weight
change and the plasma IGF-I concentration. IGFBP-1 has been shown
to transport IGF-I from the vascular space or to suppress activity
of serum IGF-I, resulting in a lower plasma concentration of total
IGF-I or free IGF-I. We presume that with a single EAA
restriction, the elevated plasma IGFBP-1 concentration suppresses the
IGF-I activity. Plasma concentrations of IGFBP-3 and -4 did not
differ between single AA-restricted groups and the total
AA-deprived group (data not shown). On the other hand, results of
immunoblotting showed that IGFBP-2 in plasma was higher in rats fed a
protein-free diet, but this increase was much smaller than that of
IGFBP-1 (Takenaka et al. 1996
). Taken together, our
results suggest that both low plasma IGF-I concentration and high
plasma IGFBP-1 concentration may cause the most severe weight loss in
rats fed AA-free diet.
In summary, we conclude that the effect of a single EAA deficiency on IGFBP-1 synthesis was different in rat liver in vivo from that in cell culture systems. Our results also indicated that a single EAA restriction suppressed IGF-I production but did not affect IGFBP-1 production. The present results suggest that not only plasma IGF-I but also IGFBP-1 plays an important roles in determining the magnitude of growth retardation in vivo.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Present address: Department of Animal Sciences,
Graduate School of Agricultural and Life Sciences, The University of
Tokyo, Bunkyo-ku, Tokyo 113-8567, Japan.
4 Abbreviations used: AA, amino acid; Con,
control; EAA, essential amino acid; IGFBP-1, insulin-like growth
factor–binding protein-1; IGF-I, insulin-like growth factor-I;
PEG, polyethylene glycol; RIA, radioimmunoassay.
Manuscript received June 5, 2000. Initial review completed July 17, 2000. Revision accepted September 5, 2000.
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