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*
Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo 113-8657, Japan, and
Nakano Vinegar Co. Ltd., Handa 475-8585, Japan
3To whom correspondence should be addressed.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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-glutamyltranspeptidase) were not affected. To understand
mechanisms underlying the suppression of disaccharidase activity by
acetic acid, Northern and Western analyses of the
sucrase-isomaltase complex were performed. Acetic acid did not
affect the de novo synthesis of this complex at either the
transcriptional or translational levels. The antihyperglycemic effect
of acetic acid may be partially due to the suppression of
disaccharidase activity. This suppression seems to occur during the
post-translational processing.
KEY WORDS: • Caco-2 cells • acetic acid • disaccharidase
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Itoh 1978
,
White 1971
). Dishes in which sourness is required, such
as sushi, pickles and marinated food, contain 10–150 mmol/L of acetic
acid (Bell et al. 1972
, Maruyama et al. 1980
, Rodger et al. 1984
, Seuss and Martin 1993
). When carbohydrates that are indigestible in the
small intestine, such as dietary fiber and resistance starch, are
orally ingested, they are broken down by fermentation in the large
intestine, short-chain fatty acids
(SCFA)6
such as acetic, propionic and butyric acids are produced, and they are
then absorbed from the large intestine (Cummings 1983
).
Pomare et al. (1985)
measured acetic acid appearing in
the venous blood after lactulose (a fermentable carbohydrate) and
acetic acid were orally ingested. The blood level of acetic acid
reached a peak much faster when acetic acid was ingested than when
lactulose was given. Because the absorption of acetic acid from the
stomach is poor, the absorption site of orally ingested acetic acid
seems to be the small intestine (Meyer-Wyss et al. 1991
). Furthermore, Pomare et al. (1985)
have
shown that the acetic acid level in the blood was similar in either
case when lactulose or acetic acid was orally administered. When meals
containing fermentable carbohydrate were orally administered to
experimental animals, the concentration of acetic acid in cecal digesta
reached ~100 mmol/L (Cheng et al. 1987
, Topping et al. 1985
). These studies indicate that when food containing
10–150 mmol/L of acetic acid is eaten, the concentration of acetic
acid possibly reaches the millimolar level in the small intestine. Such
a high concentration of acetic acid may disturb physiological functions
of the intestine. However, only a few studies concerning acetic acid
have been carried out in the small intestine.
Previous in vivo experiments have shown an antihyperglycemic effect of
vinegar. For example, rats were fed for ~30 d a high-sucrose diet
containing 15.4% vinegar (Yonemoto et al. 1995
). Blood
glucose concentration was significantly lower in rats administered
acetic acid. In another study, rats were given diet containing 7%
vinegar for 10 wk and they were then orally loaded 250 mg of glucose
per 100 g body weight. The postprandial blood glucose was
significantly lower in rats fed vinegar (Ebihara and Nakajima 1988
). Carbohydrates are digested by amylase which is present
in saliva and pancreatic juice. Disaccharides are further hydrolyzed by
glycosidases in the brush border membrane of the intestinal epithelium.
Subsequently, resultant monosaccharides are absorbed from the intestine
via specific sugar transport systems. To our knowledge, acetic acid at
the millimolar level does not inhibit amylase. If acetic acid inhibits
transport systems specific to glucose or disaccharidases in the
intestine, glucose absorption from the intestine decreases, resulting
in lowering the blood glucose level. This hypothesis may partially
account for the antihyperglycemic effect of vinegar. Therefore, in this
study we investigated effects of acetic acid on intestinal glucose
transporters and disaccharidases.
To examine if acetic acid affects glucose transport or
disaccharidases, we designed in vitro experiments, using a
human intestinal cell line, Caco-2. This cell line is derived from a
colon carcinoma although it behaves like a small intestinal epithelial
cell after differentiation and polarization (Pinto et al. 1983
). Therefore, this cell line has been used to study
physiological functions of the small intestine (Blais et al. 1987
). Caco-2 cells express glucose transporters as well as
disaccharidases (Howell et al. 1992
, Stein et al. 1996
, Zweibaum 1991
). Furthermore,
post-translational processing of hydrolases, such as
alkalinephosphatase (ALP), aminopeptidase-N (AP-N),
dipeptidylpeptidase-IV (DPP-IV), -glutamyltranspeptidase
(-GTP), angiotensin-I converting enzyme (ACE) and
disaccharidases (sucrase, maltase, trehalase and lactase) has been
studied in this cell line (Danielsen 1992
, Garcia et al. 1993
, Gilbert et al. 1991
, Hauri et al. 1985
, Le Bivic et al. 1990
, Naim 1993
and Sjötrö et al. 1983
,
Stieger et al. 1988
). Therefore, the Caco-2 cell line
was used in the present study.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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A human colonic carcinoma cell line, Caco-2, was obtained from American Type Culture Collection (Rockville, MD). Caco-2 cells were routinely cultured at 37°C in a humidified atmosphere of 95% air-5% CO2. The composition of the medium was Dulbecco’s modified Eagle’s medium (Nissui Pharmaceuticals, Tokyo, Japan) supplemented with 10% heat-inactivated fetal bovine serum (Gibco, Grand Island, NY), 1% nonessential amino acids (Mediatech, Herndon, VA), 4 mmol/L of glutamine and 1 x 105 U/L of penicillin-100 mg/L of streptomycin (Gibco). The pH of the medium was adjusted to 7.4 with sodium bicarbonate. Fresh medium was given every 2 d, and cells were passaged before confluence at a split ratio of 1:2 by their exposure to 0.1% trypsin (Difco Laboratories, Detroit, MI) and 0.02% EDTA in PBS. Cells used were at passages 64–78.
For measurements of enzyme activity, cell growth and cell viability, cells were seeded at a density of 0.14 million cells/well in 24-well plastic microplates (Iwaki Glass, Chiba, Japan). The microplates were precoated with Type-I collagen (Nitta Gelatin, Osaka, Japan). Cells for glucose transport assays were seeded on polycarbonate membranes (Corning Costar, Cambridge, MA). In both cultures for specific experiments, cells were maintained for 1 d using the standard medium after seeding to promote their recovery from damage caused by trypsinization. The medium was then switched to that containing acetic acid or other organic acids. When we cultured cells on polycarbonate membranes, media containing acetic acid or other chemicals were applied to the apical side. The standard medium was always used on the basal side. Because the pH of the medium decreased only by 0.2 unit even when the concentration of acetic acid in the medium was 5 mmol/L (the maximal concentration of acetic acid that we used), the pH was not readjusted. For control experiments, cells were concurrently cultured with the standard medium. Under these culture conditions, Caco-2 cells seeded on the permeable membrane formed a monolayer of cells interconnected with tight junctions by d 15.
Assay of cell proliferation and viability.
Cell proliferation was monitored by serial assays of cellular protein.
The protein was determined by Bradford method (Bradford 1976
). The viability of cells was assessed by their ability
to reduce alamarBlue (Biosource International, Camarillo, CA) and to
maintain lactate dehydrogenase (LDH) inside cells using
LDH-cytotoxic test kit (Wako, Osaka, Japan). The cell viability was
also estimated by cell counting with trypan blue.
Measurement of glucose uptake.
When transport measurements were carried out, medium was removed from the apical and basal sides of cell monolayers cultured on the permeable membrane. The PBS was used to rinse both sides of the monolayer as well as to preincubate at 37°C for 15 min. After PBS was removed, 600 µL of PBS was applied to the basal side and then 300 µL of PBS containing 123 nmol/L of 3-O-[methyl-3H]-D-glucose (3-O-met glucose) (Amersham, Buckinghamshire, United Kingdom) was placed to the apical-side to initiate transport. The 3-O-Met glucose uptake into cells and influx from the apical to the basal side through the cell monolayer were estimated from the radioactivity appearing in the cell lysate and the basal solution, respectively. The uptake was measured for 5 min. To terminate uptake, radioactive glucose was removed from the apical side, and cell monolayers were washed three times with 700 µL of ice-cold PBS containing 0.5 g/L of sodium azide. Subsequently, cells were lysed with 250 µL of 0.1% Triton X-100 and transferred to counting vials. For measurements of 3-O-met glucose influx, 600 µL of PBS were collected from the basal side and transferred to counting vials. The radioactivity was determined by liquid scintillation spectrometry.
Determination of enzyme activity.
The activities of glycosidases, sucrase, maltase, trehalase and
lactase were determined by Dahlqvist’s method (Dahlqvist 1964
). In brief, cell monolayers were rinsed with 700 µL of
PBS, and 400 µL of PBS containing 28 mmol/L of the substrate was
placed on cultured monolayers. Substrates used for sucrase, maltase,
trehalase and lactase assays were sucrose, maltose,
D-(+)-trehalose and D-(+) lactose,
respectively. After cells were incubated with a solution containing the
substrate for a predetermined period at 37°C, the substrate solution
was collected. The amount of glucose released from the substrates was
determined using a kit (Glucose Test #273-13901; Wako). The activity of
ALP was determined by liberation of p-nitrophenol from
p-nitrophenylphosphate (Forstner et al. 1968
). The activity of -GTP was assessed by measuring
nitroanilide released from 3 mmol/L of L-glutamic
-para-nitroanilide (Louvard et al. 1975
).
Glycylglycine was used as the recipient of -glutamine. The
activities of AP-N and DPP-IV were determined using
ala-7-amino-4-methylcoumarin and gly-pro-7-amino-4-methylcoumarin as
substrates, respectively. Released methylcoumarin was assayed by
spectrofluorometry (excitation; 370 nm, emission; 442 nm). The activity
of ACE was determined using benzoyl-gly-his-leu as a substrate by a
method described previously (Stewart et al. 1981
).
Hydrolyzed benzoyl-gly (hippuric acid) was spectrophotometrically
assayed at 228 nm. The activities of hydrolases are expressed as µmol
substrate hydrolyzed/(mg cellular protein · h).
Northern blot analysis.
Cells were cultured in 100-mm dishes and treated with 5 mmol/L of
acetic acid for 15 d. Total RNA was extracted from cells using
Isogen RNA isolation kit (Wako). Total RNA (50 µg) was fractionated
by electrophoresis on a denatured gel and transferred to a nylon
membrane (Amersham). After prehybridization, the membrane was incubated
with a 32P-labeled probe for sucrase-isomaltase (S-I)
complex obtained by reverse transcription-polymerase chain reaction
(RT-PCR) from Caco-2 cells. Primers for PCR were designed from the cDNA
sequence of the human S-I complex (Chantret et al. 1992
): sense, 5'-TAGGTCGACGTGCCAATGGA-3' (nucleotides
1300–1320); antisense, 5'-GCAGGATCCTGATGTTCATATC-3' (nucleotides 2002–2023). The membrane hybridized with the probe was washed, exposed
on an image plate and analyzed with a BAS-2000 II image analyzer (Fuji
Film, Tokyo, Japan). Control hybridization was carried out with human
ß-actin cDNA.
Western blot analysis.
Caco-2 cells cultured in 100-mm dishes (6 million cells per dish) in the presence of 5 mmol/L of acetic acid for 15 d were lysed in 500 µL of a buffer whose composition was 150 mmol/L of NaCl, 1 mmol/L of EDTA and 1% of Nonidet P-40 (NP-40), buffered with 10 mmol/L of Tris/HCl, pH 8.0. The S-I complex was immunoprecipitated with 5 µL of a monoclonal antibody specific to this complex which was generously provided by Dr. H.-P. Hauri, University of Basel (Switzerland). The precipitant was separated by SDS-PAGE and electrophoretically transferred to a nitrocellulose membrane. The location of S-I complex was detected by an ECL method using a kit (Amersham).
Statistical analysis.
Each result is expressed as the means ± SEM for four or seven independent determinations. The number of determinations indicates that of experiments with separate cell monolayers which were performed at each time point or concentration. Differences between experimental and control data were assessed by Student’s t test (Microsoft Excel, Microsoft Corporation, Roselle, IL). The P value (two-tailed) of <0.01 indicates significant difference.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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).The effect of acetic acid on the viability of Caco-2 cells was also
studied. The viability of cells was estimated from their reducing
activity of alamarBlue, retention ability of LDH and excretion ability
of trypan blue. Acetic acid also did not reduce the viability of Caco-2
cells (Table 1
).
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|
).
|
).The influx of 3-O-met glucose was not affected by the
presence of acetic acid during the influx assay (Fig. 3B
).
|
).Thereafter, the sucrase activity greatly increased in control cells
while that activity in cells cultured with acetic acid stayed low. The
activity of sucrase in cells treated with acetic acid was significantly
less than that in control cells on d 7, 11 and 15 (P < 0.01). This decrease in sucrase activity due to acetic acid was not due
to its direct inhibition of sucrase during the assay (0 mmol/L of
acetic acid in the assay mixture, 10.4 ± 0.5; 5 mmol/L of acetic
acid, 11.3 ± 0.2 of µmol · mg
protein-1 · h-1; n = 4).
|
). Even 1 mmol/L of acetic acid inhibited sucrase activity by 30%
(P < 0.01).
|
).
|
). The activities of trehalase and lactase were almost completely
inhibited. The activity of ACE was reduced to 30% of the control by
acetic acid treatment while the activities of ALP, AP-N, DPP-IV and
-GTP were not affected.
|
shows a representative result of Northern blot analysis using a probe
for the S-I complex made by RT-PCR. A band was found at the
size of 6.8 kb as previously reported (Chantret et al. 1992
). Acetic acid treatment did not affect the density ratio
of the S-I complex to ß-actin (control, 0.87 ± 0.04; acetic
acid, 0.99 ± 0.05; P = 0.12, n = 3). We performed a Western blot to examine the change in the amount of
S-I complex due to acetic acid treatment. A monoclonal antibody
specific to the human S-I complex was used to precipitate and
detect the complex. The complex was found at 210 kDa (Fig. 6B
). The treatment of cells with acetic acid did not change
the degree of density of the band at 210 kDa (the density ratio of
acetic acid to control treatments, 1.07 ± 0.14, n
= 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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and Table 1
), showing that 5 mmol/L of acetic acid is not harmful to
the intestinal cells. These results are consistent with those in
previous studies of intestinal cell lines. Gamet et al. (1992)
have shown using HT-29 cells that 30 mmol/L of sodium
acetate did not affect the growth of cells whereas propionate and
butyrate at the same concentration were inhibitory. Even though
propionate and butyrate at 4 mmol/L induced apoptosis in several
colorectal tumor cell lines including Caco-2 and HT-29, the
concentration of acetate required to induce apoptosis was more than 40
mmol/L (Hague et al. 1995
, Marchetti et al. 1997
). Under our microscopic observation, 5 mmol/L of acetic
acid did not induce apoptotic cell death in Caco-2 cells, either. The
mechanisms underlying apoptosis induced by propionate and butyrate in
HT-29 and Caco-2 cells are not clear, although deoxycholate induces
apoptosis in these cells by increasing the intracellular concentration
of Ca2+. Therefore, the reason why among SCFA acetic acid
seems less harmful to intestinal epithelial cells is still unknown.
To determine if acetic acid treatment inhibits glucose transport,
glucose uptake into Caco-2 cells and influx through cell monolayers
were measured using radiolabeled 3-O-met glucose as a
nonmetabolizable substrate. Cells cultured for 15 d in a medium
were studied. The transepithelial electrical resistance (TEER) of
monolayers treated with acetic acid for 15 d was significantly
higher than that of control (control; 715 ± 57
x cm2, acetic acid; 1060 ± 16 x cm2, n = 4, P < 0.01). The
TEER value is an index of the tightness of the intestinal monolayer
barrier. Because the paracellular permeability of substances decreases
as the TEER increases, we assumed less influx of glucose through the
monolayer of Caco-2 cells treated with acetic acid, leading to the
decrease in the glucose concentration. However, the chronic acetic acid
treatment did not change the transepithelial influx of
3-O-met glucose (Fig. 1B)
. The coexistence of acetic acid
during flux measurements also did not inhibit 3-O-met
glucose influx (Fig. 2B)
. We also studied 3-O-met glucose
uptake into the cells. The 3-O-Met glucose uptake was not
different from controls in cells treated with acetic acid (Fig. 1A)
.
The coexistence of acetic acid did not stimulate 3-O-met
glucose uptake (Fig. 2A)
. However, we did not obtain data showing
decreased 3-O-met glucose influx or uptake due to chronic or
acute treatment of acetic acid. Acetic acid does not inactivate glucose
transport in the intestinal cells, which does not explain the
antihyperglycemic effect of acetic acid observed in vivo.
The present study has shown for the first time an inhibitory effect of
acetic acid on the increase of disaccharidase activity during the
growth of Caco-2 intestinal cells (Fig. 4)
. The disaccharidases
inhibited by acetic acid were sucrase, maltase, trehalase and lactase
(Table 3)
. Sucrase and isomaltase are synthesized as a complex
(Traber 1994
). The activity of sucrase increases in the
intestine of rats fed a sucrose-rich diet. This upregulation of
sucrase is due to an increase in the S-I complex mRNA
(Broyart et al. 1990
). Simultaneously, the mRNA level of
sodium-dependent glucose transporter 1 (SGLT1) is also elevated by
a sucrose-rich diet (Miyamoto et al. 1993
). Since
sucrose is hydrolyzed to glucose by sucrase and this glucose is
transported by SGLT1, this is a response of the intestine to enhance
the bioavailability of sucrose. These previous studies indicate that
disaccharidases are susceptible to transcriptional regulation. In this
study, we performed a Northern blot analysis to examine the effect of
chronic acetic acid treatment on the S-I complex mRNA level. Acetic
acid did not affect the S-I complex mRNA, indicating that acetic
acid is not involved in the transcriptional regulation of
disaccharidases (Fig. 6A)
. Furthermore, a Western analysis was
performed, showing that the translation of the S-I complex also is
not negatively regulated by acetic acid (Fig. 6B)
.
A possible explanation for the suppression of disaccharidases
caused by acetic acid is that acetic acid may inhibit such a
post-translational processing step such as intracellular trafficing
of de novo synthesized disaccharidases, their glycosylation or their
sorting into the polarized membrane. Sucrase, maltase, lactase,
AP-N and DPP-IV are classified as transmembrane proteins while
ALP and trehalase are classified as
glycosyl-phosphatidylinositol-anchored proteins (Danielsen 1992
, Garcia et al. 1993
). ALP and sucrase are
delivered directly to the apical membrane while AP-N and DPP-IV
are delivered via the basolateral membrane (Gilbert et al. 1991
, Le Bivic et al. 1990
). In our study,
disaccharidases were suppressed by acetic acid, whereas ALP, AP-N,
DPP-IV and -GTP were not. Therefore, the suppression of
disaccharidases by acetic acid is not explained by these
classifications with regard to membrane sorting or binding of the
hydrolases.
Accumulated data have shown that the transport of peptidases such as
AP-N and DPP-IV from rough-surfaced endoplasmic reticulum
(rER) to trans-Golgi apparatus (tGA) in Caco-2
cells was considerably faster than that of disaccharidases
(Hauri et al. 1985
, Stieger et al. 1988
).
This phenomenon is called the asynchronous transport of intestinal
brush-border hydrolases. ACE is also transported from rER to tGA by
a slower trafficking pathway and its transport kinetics are comparable
to those of disaccharidases (Naim 1993
). Disaccharidases
and ACE do not form homodimers, whereas AP-N and DPP-IV do
(Sjötrö et al. 1983
), suggesting the
hypothesis that brush-border hydrolases utilize different routes
from rER to tGA, according to differences in their structural
maturation. A paper by Quaroni et al. (1993)
supports
this hypothesis because they observed that culturing Caco-2 cells at
42.5°C decreased cell surface delivery of the S-I complex but did
not affect those of DPP-IV or AP-N. A Western analysis in our
experiments showed that acetic acid does not decrease the amount of the
S-I complex (Fig. 6)
, indicating that acetic acid does not affect
the de novo synthesis of the S-I complex until its translation. We
studied the effect of acetic acid treatment (5 mmol/L and 15 d) on
the activity of brush-border hydrolases. The activities of
disaccharidases and ACE were suppressed by this treatment, whereas
those of ALP, AP-N, DPP-IV and -GTP were not (Table 2)
. These
data are well accounted for by the hypothesis, indicating that acetic
acid may interrupt a slow transport pathway from rER to tGA which is
shared by disaccharidases and ACE.
In conclusion, culturing Caco-2 cells with acetic acid suppresses the
increases in disaccharidase activities during cell growth. This
suppression by acetic acid may be due to the interference of
post-translational trafficking of synthesized disaccharidases from
rER to tGA. This seems to be one of the mechanisms underlying the
antihyperglycemic effect of vinegar observed in vivo. However, there
are still cases which cannot be explained by our conclusion obtained in
this study. Nakajima and Ebihara (1988)
have shown that
long-term treatment of rats with acetic acid reduces blood glucose
concentration immediately after the administration of glucose. This
study demonstrates that acetic acid can reduce the glucose level in the
blood even when glucose itself is loaded. Brighenti et al. (1995)
have shown another case in which acetic acid decreases
the blood glucose level even when acetic acid is given with meal,
indicating an acute effect of acetic acid on the blood glucose level.
Acetic acid may change glucose tissue distribution or its utilization
to synthesize glycogen. To understand mechanisms underlying the
antihyperglycemic effects of acetic acid, further experiments are
required.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Ogawa, N., Satsu, H., Watanabe, H., Miyamoto, Y., Fukaya, M., Tsukamoto, Y. & Shimizu, M. (1998) Chronic administration of acetic acid decreases the activity of glycosidases in Caco-2 intestinal epithelial cells. JAACT/ESACT ’98 Meeting Program & Abstracts, pp. 73.
4 Current address: National Food Research Institute, 2-1-2 kannondai, Tsukuba, Ibaraki 305-8642, Japan.
5 Current address: Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, 1-1-1 Bunkyo, Tokyo 113-8657, Japan.
6 Abbreviations used: ACE, angiotensin-I converting enzyme; ALP, alkalinephosphatase; AP-N,
aminopeptidase-N; DPP-IV, dipeptidylpeptidase-IV; ECL, enhanced chemiluminescence; 3-O-met glucose,
3-O-[methyl-3H]-D-glucose; -GTP, -glutamyltranspeptidase; LDH, lactate dehydrogenase; NP-40, Nonidet P-40; rER, rough-surfaced endoplasmic reticulum; RT-PCR, reverse transcription-polymerase chain reaction; SCFA, short-chain fatty acids; SGLT1, sodium-dependent glucose transporter 1; S-I complex, sucrase-isomaltase complex; TEER, transepithelial electrical resistance; tGA, trans-Golgi apparatus.
Manuscript received December 9, 1998. Initial review completed February 18, 1999. Revision accepted November 12, 1999.
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