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Laboratory of Nutrition Chemistry, Faculty of Home Economics, Kobe Women’s University, Suma-ku, Kobe 654-8585, Japan and * Riken Chemical Industry Limited Company, Fushimi-ku, Kyoto 612-8404, Japan
1To whom correspondence should be addressed. E-mail: oi{at}suma.kobe-wu.ac.jp.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • garlic • diallyldisulfide • testosterone • corticosterone • rats
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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2
3
4
5
6)
. However, the effects of
garlic supplementation on protein metabolism have not been fully
clarified. In our previous work, we reported that the supplementation
of garlic powder at 0.8 g/100 g to a high fat diet and the
administration of diallyldisulfide, a major volatile
sulfur-containing compound in garlic, enhanced triglyceride
catabolism and growth of interscapular brown adipose tissue
(IBAT)2
by increasing noradrenaline secretion in rats (7
,8)
.
Recently, we reported that allyl-containing sulfides in garlic
increase the uncoupling protein (UCP) content in brown adipose tissue,
and noradrenaline and adrenaline secretion in rats (9)
. We
speculated that garlic may affect whole-body protein metabolism by
the stimulation of hormone secretion and that dietary supplementation
of garlic may enhance hormone-regulated protein anabolism.
Testosterone plays a major role in protein anabolism
(10
,11)
. In contrast, glucocorticoid, which is secreted
mainly as corticosterone, affects protein catabolism in rats
(10)
. The present study was conducted to investigate the
effects of garlic supplementation on protein metabolism in rats. In
particular, we wanted to determine whether garlic supplementation
stimulates protein anabolism via regulation by steroid hormones with
counterregulatory effects on both protein anabolism and catabolism,
i.e., the protein anabolic hormone, testosterone, and the protein
catabolic hormone, corticosterone. Furthermore, to better understand
the effects of garlic supplementation on protein metabolism, we
investigated in anesthetized rats the effects of diallyldisulfide on
the secretion of luteinizing hormone (LH) from the pituitary gland,
which regulates testosterone production in the testis
(12
,13)
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Male Sprague-Dawley rats (Japan SLC, Shizuoka, Japan) were housed
individually in stainless steel wire-bottom cages in a room
maintained at 22–24°C and 
50% relative humidity. The room was
lit from 0700 to 1900 h. Tap water was freely available. Rats, 4
and 7 wk old, were purchased for use in Experiments 1 and 2,
respectively. In Experiment 1, rats were fed a commercial diet (CE-2,
Japan, Clea, Tokyo, Japan) for 3 d before starting the
experiments, and in Experiment 2, rats were given the commercial diet
before starting the experiments. This study was approved by the
Institutional Animal Care and Use Committee of Kobe Women’s
University, Faculty of Home Economics.
Experiment 1.
The experimental diets were normal fat (5 g/100 g fat) diets with three
different protein levels (40, 25 or 10 g/100 g casein), as shown in
Table 1
. Rats in the control group were fed 40, 25 or 10% casein (control
diet), whereas rats in the garlic group were fed one of these diets
supplemented with 8 g of garlic powder/kg diet (garlic diet). The
garlic powder was prepared from fresh garlic bulb (Riken Chemical
Industry, Kyoto, Japan), which was heat-dried at 60–70°C, and
then ground by a mill. Volatile compounds in the garlic powder were
analyzed by gas chromatography using diallyldisulfide as a standard
(14
,15)
; their concentrations were determined as
diallyldisulfide equivalents (Table 1)
. Rats (n = 39)
weighing 80–90 g were separated into six groups (control groups, 6
rats; garlic groups, 7 rats) and were fed for 28 d one of the
following experimental diets: 40, 25 or 10% casein diets with or
without garlic powder. Each group was fed the appropriate diet in
amounts such that the six groups consumed an equal amount of
metabolizable energy during the experimental period, and that food
consumption of each of the six groups was approximately equivalent to
the maximal amount (food intake was sufficient for the rats) that rats
can consume under these conditions. At the end of the 28 d, the
rats were transferred to individual metabolic cages and urine and feces
were collected separately for 1 d. To each urine sample obtained
during the collection was added 1 mL of 6 mol/L HCl solution to prevent
its degradation. After the collection, urinary and fecal nitrogen
contents and the nitrogen content in each experimental diet were
determined by the semimicro Kjeldahl method, and nitrogen intake was
calculated on the basis of the nitrogen content of each experimental
diet from the total amount of food consumed. Urinary creatinine content
was measured using the method of Clark and Thompson (16)
.
Urinary 17-ketosteroid (urinary excretion of total amounts of
androsterone, etiocholanone, dehydroepiandrosterone,
11-ketoandrosterone, 11-ketoetiocholanone, 11-OH androsterone and 11-OH
etiocholanorone) content was determined by the Zimmerman reaction
(17)
.
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-chloralose and urethane
(18)
, which were purchased from Wako Chemical (Osaka,
Japan) and Tokyo Chemical (Tokyo, Japan), respectively. After feeding
(at the end of d 29), rats were anesthetized by intraperitoneal
injection of -chrolarose and urethane (75 and 750 mg/kg,
respectively). Blood samples were collected from the abdominal aorta,
and plasma was separated after centrifugation (3000 x g for 15 min) and stored at -40°C until analyzed. After
collection of the blood sample, the liver, kidney, perirenal adipose
tissues and epididymal fat pad were immediately excised, weighed and
stored at -40°C for further analyses. Arginase activity in the liver
was determined using the method of Schimke (19
,20)
. Plasma
corticosterone concentration was determined using the method of Sagara
et al. (21)
, i.e., the plasma sample was analyzed by HPLC
after the extraction of steroids, as described below. To extract free
steroids in the plasma, 10 mL of 0.05% methanol-chloroform and 0.2
mL of 1 mol/L NaOH were added to 1 mL of plasma sample, and the mixture
was shaken gently for 20 min. Then, 9 mL of the methanol-chloroform
layer was removed without contamination of the emulsion layer. The
extract was washed twice with distilled water (2 mL); 8 mL of the
methanol-chloroform layer was obtained and evaporated to dryness in
a rotary evaporator under continuous suction. The residue was dissolved
in absolute methanol. An aliquot of the solution was injected into a
chromatograph [Irica HPLC system; detection, UV at 245 nm;
flow rate, 0.5 mL/min; column, ODS column RP-18T, 250 x 4.6 mm;
mobile phase, H2O/methanol/tetrahydrofuran
(36:55:9)]. Each rat testis was homogenized with 1 mL of distilled
water and centrifuged at 12,000 x g at 4°C for 30 min
(22)
. Then the supernatant was separated and steroids were
extracted using the same method as in the case of plasma
corticosterone. After steroid extraction, the testicular testosterone
content was analyzed by HPLC as described above.
In a preliminary experiment concerning the effects of different
cholesterol concentrations in two different fats, testosterone content
in the testis was compared in rats fed high fat diets (21.21 MJ/kg)
containing 30% shortening (0% cholesterol) or lard (0.1%
cholesterol). The composition of the shortening and lard diets was
described previously (9)
. We examined the effects of
garlic supplementation (8 g/kg diet) on testicular testosterone content
in rats fed these diets for 28 d. Each group of rats was offered
the appropriate diet in amounts such that the four groups consumed
equal metabolizable energy during the experimental period, and food
consumption in all four groups was approximately equivalent to the
maximum (food intake was sufficient for the rats) that rats can consume
under these conditions. Testicular testosterone content was determined
by the same method as in Experiment 1 described above.
Experiment 2.
Rats weighing 250 g were anesthetized as described above; their
rectal temperature was maintained between 36.5 and 37.5°C using a
direct-current heating pad. Rats (n = 6–7)
were used to evaluate the effects of diallyldisulfide in comparison
with rats that received vehicle alone (9 g/L NaCl solution containing
2% ethanol and 10% Tween 80). We determined the dose-dependent
response with respect to plasma LH concentration after the
administration of diallyldisulfide. Diallyldisulfide [88.9%; the
remaining compounds were diallylmonosulfide (5.4%) and
diallyltrisulfide (5.3%)] was purchased from Tokyo Chemical. For
dose-response measurements, each rat received 1 mL of the vehicle
containing 10 mmol/L (1.46 mg), 20 mmol/L (2.92 mg) or 30 mmol/L (4.28
mg) diallyldisulfide via injection into the right femoral vein over 1
min. Blood samples were collected from the abdominal aorta after 30
min. In a preliminary experiment, we confirmed that plasma LH
concentrations were maximal 30 min after administration. Accordingly,
we performed the dose-response measurements and determined plasma
LH concentration 30 min after diallyldisulfide administration. Plasma
LH concentration was assayed using an enzyme immunoassay kit (rat LH
enzyme immunoassay system, Amersham Pharmacia, UK).
In another preliminary experiment concerning the effects of noradrenaline on plasma LH concentration, plasma LH concentration in rats after administration of 5, 10 or 50 mg noradrenaline was examined as described above.
Statistical analysis.
All data are presented as means ± SEM. Statistical analyses were done using Statistical Package for Social Sciences (SPSS10.0 for Windows; SPSS, Chicago, IL). In Experiment 1, treatment effects (dietary protein levels and garlic supplementation) were analyzed using two-way ANOVA, and the differences between means were tested using Duncan’s multiple range post-hoc test. In Experiment 2, data were analyzed using one-way ANOVA, and significant differences between means were evaluated by the Bonferroni post-hoc test. The correlations between the data of plasma LH concentrations and the administration of diallyldisulfide or noradrenaline for dose response measurements were tested by regression analysis. Differences with P < 0.05 were considered significant.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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After 28 d of dietary treatment, no significant differences due to
garlic were found on body, liver, kidney, testis, perirenal adipose
tissue and epididymal fat pad weights, or urinary creatinine
(Table 2
). Urinary nitrogen was significantly lower in the garlic-40% casein
diet group than in the control-40% casein diet group (Table 3
). No differences were observed among groups in fecal nitrogen content
(Table 3)
. Nitrogen balance was significantly higher in the
garlic-40% casein diet group than in the control-40% casein diet
group, whereas there were no significant differences between the
control diet groups and the garlic diet groups fed 10 and 25%
casein diets (Table 3)
. Similarly, arginase activity in the liver was
significantly higher in the garlic-40% casein diet group than
in the control-40% casein diet group, whereas there were no
significant differences between the control diet groups and the garlic
diet groups fed 10 and 25% casein diets (Table 4
). Plasma corticosterone concentrations in rats fed all levels of casein
were significantly lower in those supplemented with garlic (Fig. 1
). Testosterone contents in the testis of rats fed either 40 or 25%
casein diets were significantly greater in rats supplemented with
garlic, whereas there were no significant differences between the
control diet group and the garlic diet group fed the 10% casein diet
(Fig. 2
). Urinary 17-ketosteroid levels in rats fed 40% casein diets were
significantly greater in those consuming garlic (Fig. 3
). Furthermore, urinary 17-ketosteroid excretion in rats in the
garlic-40% casein diet group was significantly higher than that in the
garlic-10% casein diet group (Fig. 3)
.
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). Further investigation is necessary to elucidate the different effects
of garlic supplementation, in relation to dietary cholesterol, on
steroid hormone production.
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Plasma LH concentrations were significantly higher in rats that
received 20 or 30 mmol/L diallyldisulfide than in those that
received vehicle alone (Table 5
). The increase was dose dependent, and there was a positive correlation
(P < 0.01, r = 0.552) between plasma
LH concentration and the dose of diallyldisulfide.
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).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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. This technique allows the rates of whole-body
protein synthesis and breakdown to be estimated together with amino
acid oxidation and the fractional synthetic rates of mixed muscle
protein or of single plasma proteins (10
,23)
. Protein
synthesis rates of tissues (e.g., plasma, tibialis anterior, soleus or
liver) in rats in vivo were measured by the flooding dose method, which
reduces uncertainty over the labeling of the tracer amino acid in the
precursor pool for the protein synthesis (24
25
26)
. Broadly
speaking, isotopic methods fall into two groups, i.e., those methods
based on uptake of isotope into protein which yield information about
the rate of protein synthesis and those based on isotope loss from
which the rates of both synthesis and breakdown can be determined
(27)
. For instance, enzymes must have a fast turnover rate
so that their concentrations can be rapidly changed by factors that
modulate their rates of synthesis or degradation. Among the potential
factors that play a role in the regulation of protein metabolism are a
number of substrates and hormones. Hormones, by affecting the turnover
rates of key proteins, can modulate cell differentiation and growth and
direct the flux of substrates through specific metabolic pathways
(10
,23)
. Our previous papers indicated that the
allyl-containing polysulfides in garlic are responsible for the
enhancement of noradrenaline and adrenaline secretion and the increased
thermogenesis indicated by the increased UCP content in IBAT
(9)
. We speculated that garlic may be involved in hormonal
secretion. Thus, garlic administration may affect whole-body
protein metabolism due to hormonal regulation by stimulating hormone
secretion, and dietary supplementation of garlic may affect protein
metabolism by enhancing protein anabolism. The present study was
conducted to investigate the effects of garlic on protein metabolism,
particularly to determine the effects of garlic supplementation on the
hormonal regulation of protein metabolism by measuring the levels of
steroid hormones, i.e., testosterone and corticosterone. The following
hormones have been suggested to affect protein metabolism: insulin,
growth hormone, insulin-like growth factor I, adrenaline, androgen,
estrogen, progesterone, glucagon, glucocorticoid and thyroid hormone
(10)
. On the basis of their net effects on protein balance
(protein synthesis minus protein breakdown) in the entire body,
hormones can be classified into two groups as follows: those having a
prevalent anabolic action, i.e., insulin, growth hormone,
insulin-like growth factor I, adrenaline and androgen
(testosterone), and those with a prevalent catabolic action, i.e.,
glucocorticoids (corticosterone), glucagon and thyroid hormone.
Therefore, in the present study, we investigated the effects of garlic
administration on testosterone as a protein anabolic hormone and
corticosterone as a protein catabolic hormone. In Experiment 1, the effects of garlic powder supplementation on protein metabolism in rats fed the experimental diet containing different casein levels (40, 25 or 10% casein diet) were investigated. Testicular testosterone content, urinary 17-ketosteroid content, arginase activity in the liver and nitrogen balance were significantly increased in rats after garlic supplementation to the 40% casein diet, whereas plasma corticosterone concentration was significantly decreased in rats after garlic supplementation to the 40 or 25% casein diet. Based on urinary excretion of creatinine data, body muscle mass was not affected by garlic supplementation. However, nitrogen balance data suggested that nitrogen retention in the body was enhanced by garlic supplementation in rats fed a high protein diet. Similarly, hepatic arginase activity data suggested that protein synthesis in the liver was enhanced by garlic supplementation in rats fed a high protein diet. Urinary 17-ketosteroid is an index of steroid hormone secretion, which is derived almost completely from testosterone secretion in the whole body (i.e., an index of testosterone secretion in testis). These results suggest that protein anabolism occurs in rats fed the high protein diet supplemented with garlic. Concerning the effects of garlic on protein metabolism, the different responses to garlic supplementation in rats fed normal-fat diets with different protein levels suggest that protein anabolic effects were induced by the high protein diet (40% casein diet), but not by the low protein diet (10% casein diet). The present study suggests that to induce the protein anabolic effect of garlic supplementation, the protein content in the diet should be high. Therefore, our findings suggest that protein anabolic effects were induced to a greater extent by garlic supplementation in rats fed the high protein experimental diet.
Steroid hormones are produced from cholesterol in mammals. The experimental diets in the present study were normal-fat diets containing 5% corn oil, which is cholesterol free. The testosterone contents in rats fed the 40, 25 or 10% casein diet were not significantly different, whereas the testosterone contents in rats fed the 40% casein diet were significantly increased by garlic supplementation. We speculate that testicular testosterone was derived from the de novo synthesis of cholesterol in the body. Therefore, our data indicate that garlic supplementation enhanced testosterone production in the testis.
LH is a glycoprotein with a molecular weight of 36,000; it is
comprised of two subunits ( and ß). LH is termed gonadotrophin and
is secreted by basophilic cells of the anterior pituitary gland, called
gonadotrophs. It has been reported that LH stimulates Leydig cells in
the testis to produce testosterone (12
,13
,28)
. In
Experiment 2, to confirm the protein anabolic effects of garlic, the
effects of diallyldisulfide on the secretion of LH from the pituitary
gland, which regulates testosterone production in the testis, were
investigated in anesthetized rats. In this experiment, plasma LH
concentration was directly affected by diallyldisulfides and the
intravenous administration of diallyldisulfide corresponded to garlic
absorption in blood after oral consumption. The dose of
diallyldisulfide (10 mmol/L, 1.46 mg) corresponded to approximately
twice the total average amount of garlic consumed per day per rat in
Experiment 1; thus, it is considered to be equivalent to the
physiologic level of garlic in rats. Therefore, we evaluated the
effects of diallyldisulfide on plasma LH concentration to determine
specifically the dose-dependent response of plasma LH
concentration after diallyldisulfide administration. Diallyldisulfide
increased plasma LH concentration, and plasma LH concentration
was affected by diallyldisulfide in a dose-dependent manner. These
results suggest that garlic administration increases testosterone
production in the testis due to the enhancement of LH secretion from
the pituitary gland. Previously, we reported that
allyl-containing sulfides in garlic increased noradrenaline and
adrenaline secretion levels (7
8
9)
. Noradrenaline and
adrenaline, which are involved in the secretion of various hormones,
play important roles in stimulating hormone secretion. Our results
(Table 6
) suggest that increasing noradrenaline secretion via
stimulation by allyl-containing sulfides in garlic enhances LH
secretion from the pituitary gland. Therefore, we contend that
allyl-containing sulfides in garlic are responsible for the
enhancement of LH secretion via stimulation of the pituitary gland by
noradrenaline. Garlic supplementation likely increases testicular
testosterone content due to the stimulation of LH secretion from the
pituitary gland by the increased plasma noradrenaline concentration.
The present study suggests that garlic supplementation enhances protein
anabolism and suppresses protein catabolism due to hormonal regulation
by the stimulation of steroid hormones, leading to greater testis
testosterone content and lower plasma corticosterone concentration in
rats fed a high protein diet.
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FOOTNOTES |
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Manuscript received November 27, 2000. Initial review completed January 4, 2001. Revision accepted May 11, 2001.
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