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Unit of Pharmacokinetics, Metabolism, Nutrition and Toxicology PMNT 7369 Université Catholique de Louvain, B-1200 Brussels, Belgium and * Department of Biochemistry and General Physiology, Liège University, B-4000 Liege, Belgium
2To whom correspondence should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • polyamine • oligofructose • cecum • intestinal microflora • rats
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Löser et al. 1999
), glucose transport (Johnson et al. 1995
), intestinal motility (Fioramonti et al. 1994
) and regulation of disaccharidase activities
(Deloyer et al. 1996
). Enterocytes respond to luminal
nutrients with large increases in polyamine synthesis, under the
control of ornithine decarboxylase
(ODC)3
activity, even though they are mature, nonproliferating cells
(Johnson et al. 1995
). In addition to the endogenous
synthesis of polyamines inside the cell, exogenous sources of
polyamines seem to be essential for small intestinal and colonic
mucosal growth and development (Löser et al. 1999
). Several sources of "exogenous polyamines"
reaching the intestine are available. Polyamines may be absorbed per se
as food components. Their absorption occurs mainly in the upper part of
the gut, where they are involved in enterocyte maturation and
metabolism (Bardocz et al. 1998
). Polyamines found in
the intestinal lumen may also be provided by pancreatic and biliary
secretions, through desquamation or via their active secretion by
intestinal cells (Benamouzig et al. 1997
, Osborne and Seidel 1990
). Some probiotics such as yeast can exert
trophic effects on the small intestine by mediating the endoluminal
release of spermine and spermidine (Buts et al. 1994
).
Moreover, as suggested by recent studies in humans and animals,
polyamines may be synthesized from dietary fermentable substrates such
as pectin or guar gum by bacteria in lower parts of the gut (cecocolon)
(Noack et al. 1998
, Satink et al. 1989
).
Inulin-type fructans are natural components of the diet that escape
hydrolysis by mammalian digestive enzymes, but are largely fermented by
colonic bacteria to produce a wide variety of compounds that may affect
gut as well as systemic physiology, in both humans and rats
(Roberfroid and Delzenne 1998
, Van Loo et al. 1999
).
End products of carbohydrate fermentation are represented primarily by
a limited number of carboxylic acids, especially short-chain fatty
acids (SCFA) such as acetate, propionate and butyrate, which can have
noticeable biological effects in tissues exposed to large
concentrations including the colonic epithelium and, to a lesser
extent, the liver. In the colon, the role of butyrate as a major energy
fuel and control factor of cell proliferation has been established
(Demigné et al. 1999
, Koruda et al. 1990
).
Fructans are completely fermented in the cecocolon by several bacterial
strains; some of these bacteria such as bifidobacteria are able to
acquire a proliferative advantage over other strains, as demonstrated
in vitro in mixed bath culture and in vivo in humans (Gibson et al. 1995
, Gibson and Roberfroid 1995
). Several
physiologic effects inside the gut may be related to the extensive
fermentation of fructans by endogenous bacteria, i.e., a decrease in pH
due to the production of short-chain carboxylic acids, an increase
in calcium and magnesium absorption and a displacement of nitrogen
excretion (Campbell et al. 1997
, Delzenne et al. 1995
, Rémésy et al. 1993
). Moreover,
feeding rats inulin-type fructans leads to cecal, but not colonic
hyperplasia and to an increase in ODC activity in cecal wall cells
(Rémésy et al. 1993
).
In this study, we analyzed the influence of supplementing a diet with oligofructose (OFS), a fructan obtained by enzymatic hydrolysis of chicory inulin, on polyamine concentrations in the cecum, portal vein and liver of rats.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Male Wistar rats (n = 12;
Iffa Credo, France), weighing 200 g at the beginning of the
experiment were given either a standard diet (controls), commercially
available (AO4, Villemoisson sur Orge, France), or the same diet
enriched with 10% OFS (Raftilose P95, Orafti, Belgium) for 4 wk. The
complete composition of the diets was described previously
(Daubioul et al. 2000
). The rats were anesthetized with
pentobarbital (60 mg/kg). After laparotomy, blood from the portal vein
was collected in sodium citrate solution and centrifuged at 1200
x g for 10 min at 4°C. The plasma and RBC were
washed three times in 9 g/L NaCl to remove lymphocytes and monocytes
and kept at -70°C until use. The liver was excised. The full cecum
was weighed; the cecal contents were diluted with 2 mL of 9g/L NaCl,
then centrifuged at 9000 x g for 10 min. The
supernatant was frozen at -70°C and kept for further polyamine
analysis. The cecum and liver were weighed and then clamped in liquid
nitrogen. Liver (fourfold dilution) and cecum (sixfold dilution)
homogenates were prepared in sterile water using a Potter homogenizer.
The protein level was measured in cecal and liver homogenates by using
the method of Lowry et al. (1951)
.
Polyamine content in the samples was measured by HPLC (Bontemps et al. 1984
). All samples had been stored under the same
conditions before polyamine analysis, (-70°C; maximum 3 mo). Such
storage did not modify polyamine content in pig RBC (data not shown).
The tissue homogenate and cecal contents supernatant were treated using
a procedure described previously (Kaouass et al. 1997
).
The polyamines from the blood samples were extracted using the method
of Moulinoux et al. (1991)
. After dansylchloride
derivatization, polyamines were separated on a reverse-phase column
(Lichrocart RP-18, Merck, Darmstadt, Germany).
Statistical analysis.
Data are presented as means ± SEM. Student’s t test was applied to compare unpaired means. Statview512 + (BrainPower, Calabasas, CA) was used as software. The level of significance was set at P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). OFS treatment significantly increased the cecal contents and cecal
tissue weight by 
80%. Histologic examination of cecal tissue
samples did not reveal any differences in the histologic pattern (cell
proliferation, crypt depth, villous height) of cecal mucosa in
OFS-fed and control rats.
|
5% of the total polyamine concentration estimated in the cecal
contents (Fig. 1
). Treatment with OFS almost doubled the level of putrescine in the
cecal contents but did not significantly modify the concentration of
spermidine or spermine. In the cecal tissue, spermidine and spermine
represented the major fractions (Fig. 2
). Both of these polyamines as well as putrescine were significantly
greater in the cecal tissue of OFS-fed rats.
|
|
). Polyamine concentrations in RBC were not affected by OFS treatment,
but plasma spermidine concentration was significantly lower in
OFS-fed rats. The concentration of spermine in the portal plasma
was measured in all of the samples. In OFS-fed rats, it was 0.33
nmol/mL in one rat; in the other five rats, its concentration was below
the limit of quantification (corresponding to 0.2 µmol/L)
(see Table 2
). Spermine concentration was measurable in all of the
plasma samples from the control group. The hepatic concentration of the
three polyamines was not modified by dietary OFS (Figure 3
). In the liver, spermidine and spermine were the most abundant
polyamines, whereas putrescine represented only 10% of the total
polyamines measured.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Morita et al. 1999
, Roberfroid and Delzenne 1998
,
Slavin 1999
). This fermentation leads to the
production of (SCFA), which have been proposed to be mediators of the
systemic effect of such nondigestible/fermentable nutrients
(Demigné et al. 1999
). Could other metabolic
by-products, namely, polyamines, play a role in the physiologic
effects of nondigestible carbohydrates? In this study, OFS, an
inulin-derived fructan, was added to the standard diet of rats for
4 wk. This treatment significantly decreased body weight after 4 wk,
but food intake, measured weekly, was not significantly different
between groups. However, the total energy intake was lower in
OFS-fed than in control rats. This effect could be attributed to
the lower energy value of the OFS-containing diet (13.23 kJ/g for
OFS-containing diet vs. 14 kJ/g for control diet), using an
estimated energy value for OFS of 6.3 kJ/g (Roberfroid et al. 1993
). At the end of treatment, macroscopic analysis of the
organs revealed cecal enlargement in OFS-fed rats, as previously
described (Delzenne et al. 1995
, Roberfroid and Delzenne 1998
). The increase in the cecal contents reflects a
huge proliferation of bacteria. Fructans may be metabolized by several
types of bacteria, e.g., most species of bifidobacteria are able to use
fructans as substrates (Gibson et al. 1995
). An increase
in the concentration of short-chain carboxylic acids, primarily
acetate, but also propionate, butyrate and lactate was found in the
cecum of rats fed inulin-type fructans (Campbell et al. 1997
, Roberfroid et al. 1993
, Van Loo et al. 1999
). Among the polyamines tested, only the putrescine
concentration was significantly greater in the cecal contents of
OFS-fed rats. Noack et al. (1998)
compared the
influence of pectin, a fermentable dietary fiber, on cecal polyamine
production in germfree and conventional rats. They showed that
putrescine is the main endogenous polyamine secreted into the gut lumen
from the gut mucosal cells (Noack et al. 1998
). Our
study did not provide any data relative to polyamine secretion by
intestinal or cecal cells, and the involvement of such a mechanism
would require further studies. Feeding rats fermentable dietary fiber
increased the desquamation of intestinal and/or cecal cells, a
phenomenon that could contribute to the release of putrescine in the
gut lumen (Noack et al. 1998
). Another source could
result from a modified enterohepatic circulation of polyamines, leading
to an increase in their pancreatic or biliary secretion (Osborne and Seidel 1990
). Finally, the involvement of the intestinal
flora in the modulation of polyamine concentration in the cecum must be
questioned. Inulin-type fructans such as OFS are fermented mainly
in mixed culture, and in human fecal samples in anaerobic batch
cultures, by bifidobacteria, which predominate over the other strains;
moreover, the addition of OFS (15g/d) in the diet significantly reduced
the count of bacteroides, fusobacteria and clostridia populations in
adult humans (Gibson et al. 1995
). Do OFS reduce the
number of bacterial strains able to metabolize polyamines, and/or do
they promote the strains producing putrescine? The question remains
open. The bacteria that induce putrescine production are
gram-positive anaerobic cocci and fusobacteria, whereas members of
the genus Bacteroides are considered spermidine producers
(Noack et al. 1998
). Testing the ability of
bifidobacteria to produce polyamines could be an interesting way to
determine their role in the modulation of polyamine cecal production by
dietary fructans. The predominance of bacteroides in the cecal flora of
conventional rats would explain why spermidine was the major polyamine
found in the lumen of the cecum of rats from both groups in our study.
The slight decrease (P = 0.07) in spermidine
observed in the cecal contents of OFS-fed rats could be attributed
to the decreased number of bacteroides.
In the cecal tissue, spermidine was the major polyamine, and its
concentration was significantly higher in OFS-fed rats than in
controls. The fact that all three polyamines were increased in the
cecal wall of OFS-fed rats suggests a greater endogenous synthesis,
rather than greater uptakes of polyamines of bacterial origin.
Increased activity of ODC, a key enzyme in polyamine synthesis, in the
cecal tissue of fructan-fed rats has already been described
(Rémésy et al. 1993
) and could be linked to
the cecal tissue hyperplasia observed in those rats; crypt cell
proliferation in the cecum is stimulated by butyrate, as well as by
propionate, albeit to a smaller extent (Demigné et al. 1999
). In this study, we were unable to show histologically any
increase in cell proliferation, even in the deepest zone of the crypts,
where butyrate has been shown to promote DNA synthesis
(Demigné et al. 1999
).
In addition to its effect on the gastrointestinal tract, OFS exerts
systemic effects on protein and lipid metabolism. Fructans reduce
plasma urea in normal and nephrectomized rats, by enhancing urea N
transfer into the large intestine with incorporation of this nitrogen
into bacterial protein (Levrat et al. 1993
,
Younes et al. 1995
). The addition of fructans to the
diet of male Wistar rats for at least 3 wk has been shown to decrease
fatty acid synthesis and esterification in the liver, thus reducing
serum and hepatic triglyceride concentration (Delzenne and Kok 1999
, Kok et al. 1996
). SCFA (mainly propionate)
have been proposed as the putative mediators of the "antilipogenic"
effect of dietary fructans (Demigné et al. 1999
).
In view of the results obtained in this study, we propose that the
decrease in spermine and spermidine concentrations in the plasma of the
portal vein of OFS-treated rats could also participate in lowering
hepatic triglyceride. In fact, spermine was shown to promote fatty acid
esterification by increasing phosphatidate phosphohydrolase
translocation from the cytosol toward the microsomal fraction. It also
stimulates mitochondrial and microsomal glycerol-3-phosphate acyl
transferase activities (Bates and Sagerson 1981
,
Martin-Sanz et al. 1985
, Pittner et al. 1986
). The influence of polyamines on lipogenesis was shown
only in adipose tissue and has never been studied in hepatic cells
(Borland et al. 1994
).
An accumulation of putrescine was observed in the cecum of OFS-fed
rats. Even if this polyamine acts as a growth factor in the gut, its
exact function in some aspects of cellular metabolism in the cecocolon
is still in question. Could it act, like butyrate, as a source of
instant energy in the cecocolon, as recently shown in the small
intestine of rats (Bardocz et al. 1998
)? The low content
of putrescine in the cecal contents (0.1 µmol/cecum in
OFS-fed rats) compared with the content of butyrate (50
µmol/cecum) (Demigné et al. 1999)
favors a prominent role for butyrate vs. putrescine as an "energy
provider" to cecal wall cells.
Would putrescine participate, as suggested for SCFA produced
through OFS fermentation, as a stimulator of differentiation and
apoptosis (Goodlad et al. 1989
)? Benamouzig et al. (1999)
showed recently that some food components such as
soy protein induced significant changes in lumenal polyamines in the
colon, without affecting cell proliferation in the colonic mucosa.
Finally, could the slight decrease in energy intake observed in
OFS-treated rats be involved in the modulation of putrescine
metabolism? This question is addressed in the recent studies of
Bardocz et al. (1998)
who showed that putrescine uptake
by the small bowel mucosa from the systemic circulation was doubled in
food-deprived rats compared with rats eating ad libitum. The
present study opens the door to a new field of research relative to the
gastrointestinal effect of fermentable nutrients, namely, fructans,
which are already considered "functional food" as a result of their
pleiotropic gastrointestinal and systemic effects in both animals and
humans.
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FOOTNOTES |
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3 Abbreviations used: ODC, ornithine decarboxylase; OFS, oligofructose; SCFA, short-chain fatty acids.
Manuscript received January 20, 2000. Initial review completed February 20, 2000. Revision accepted July 11, 2000.
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