[CANCER RESEARCH 55, 2293-2298, June I, 1995]
Dietary Fat, Fiber, and Carcinogen Alter Fecal Diacylglycerol Composition
and Mass1
Jennifer S. Pickering, Joanne R. Lupton, and Robert S. Chapkin2
Faculty of Nutrition, Molecular and Ceil Biology Croup, Texas A&M University, College Station, Texas 77843-247ÃOE
ABSTRACT
Fecal diacylglycerols (DAGs) are known activators of protein kinase C
(PKC), which in turn modulates colonie epithelial cell growth programs
and, therefore, could play a role in the malignant transformation process.
However, the effects of physiological modifiers such as diet and carcinogen
on fecal DAG mass and composition have not been reported. We therefore
designed a 2 x 2 x 2 factorial study (2 fats: corn oil and fish oil; 2 fibers:
pectin and cellulose; with and without carcinogen). Rats were provided
with diets for 5 weeks. Three weeks after the second injection of
azoxymethane, feces were collected from 10 rats/treatment in = 80 total)
and analyzed for DAG mass and fatty acyl composition by combined TLC
and gas chromatography. Dietary fat had a significant effect on the mol %
fatty acyl composition of fecal DAG. Greater amounts of long chain n-3
polyunsaturated fatty acids (20:Sn-3, 22:Sn-3, and 22:6n-3) were detected
in fecal DAG of fish oil-fed animals relative to corn oil (/' < 0.001). In
contrast, corn oil resulted in a higher mol % of 18:2n-6 relative to fish oil
(P < 0.016). The most salient effect of fiber was on total production
(nmol/day) of DAG, which was 2.5 times higher with cellulose than pectin
supplementation. In addition, there was an effect of fiber on both mol %
and concentration of 22:6n-3, with cellulose producing higher amounts
relative to pectin (P < 0.04). A significant interaction between fat and fiber
was observed with nmols of 17:0 excreted in 24 h, with fish oil/cellulose
producing 94.2 nmol as compared to 3.5 seen with corn oil/pectin
(P < 0.02). There was a significant interaction between fat and carcinogen
on all of the DAG n-3 fatty acids, which were elevated with carcinogen/fish
oil treatment. These data show that fat, fiber, and carcinogen can modu
late the fatty acyl composition and mass of fecal DAG. Since the produc
tion of fecal DAG, an activator of PKC, may alter colonie mucosa! cell
proliferation, our data offer insight into a mechanism by which diet may
modify the risk of colon cancer development.
INTRODUCTION
PKC'1 consists of a family of serine/threonine kinases that upon
activation can phosphorylate proteins that regulate short- and long-
term cellular events, including cell proliferation and differentiation. It
is now clear that PKC expression and activation are involved in the
regulation of colonie mucosa! proliferation (1-4). This is noteworthy
because the elevation of colonie cell proliferation has been associated
with the incidence of colon cancer (5).
DAGs link extracellular signals with intracellular responses
through the activation of PKC (6). Intracellular DAG produced from
inositol and choline phospholipid hydrolysis, coupled with increased
Ca2+ levels, can activate PKC to influence cellular processes (7). It is
interesting that several studies have recently shown that rat and human
feces contain appreciable levels of DAG (8-11). This is significant
Received 1/4/95; accepted 4/4/95.
The costs of publication of this article were defrayed in part by the payment of page
charges. This article must therefore be hereby marked advertisement in accordance with
18 U.S.C. Section 1734 solely to indicate this fact.
1 This work was supported in part by grants from the American Institute for Cancer
Research, the Texas A&M Interdisciplinary Research Initiatives Program, and NIH Grants
CA59034 and CA61750.
2 To whom requests for reprints should be addressed, at 442 Kleberg Center, Texas
A&M University, College Station, TX 77843-2471.
3 The abbreviations used are: PKC, protein kinase C; DAG, 1,2-diacyl-JTi-glycerol;
AAG, l-O-alkyl-2-acyl-sn-glycerol; A'AG, l-O-alkenyl-2-acyl-jn-glycerol; ANS,
anilino-1-naphthalene sulphonic acid ammonium salt; AOM, azoxymethane; PUFA,
polyunsaturated fatty acid.
because DAG in the colonie lumen is capable of entering mucosal
cells of the colon (9), where it can activate the PKC pathway (12). In
addition, extracellular DAGs of the chain length found in feces can
enhance the growth of benign colonie tumors and some carcinomas,
while normal cells are not affected (13). These studies suggest that
fecal intraluminal DAG may have implications in the development of
colon cancer.
DAG has been detected in foods at appreciable levels, although
only negligible amounts of dietary DAG reach the colon intact (9).
Sources of DAG in the lumen have not been elucidated, although it
may be derived partly from bacterial action (8). As a result of these
observations, interest has focused recently on the ability of dietary
constituents to modulate intraluminal DAG levels. For example,
Reddy et al. (10) have demonstrated that the type of fiber consumed
can modify fecal DAG mass and composition.
Dietary fat and fiber have interactive effects in the colon (14) and
are capable of influencing colonie PKC isoform expression (15).
However, the combined effects of dietary fat and fiber on fecal DAG
mass and composition have not been examined. Therefore, the present
study was designed to investigate the effects of dietary fat and fiber on
the mass and fatty acyl composition of fecal DAG in the rat experi
mental colon carcinogen model. In addition, fecal diglyceride sub
classes were characterized to determine aliphatic linkage at the sn-\
chemical position.
MATERIALS AND METHODS
Materials. l,2-diheneicosanoyl-.vn-glycero-phosphocholine (21:0-21:0-PC)
was purchased from Avanti Polar Lipids (Alabaster, AL). Phospholipase C (Type
V, Bacillus Cereus) and azoxymethane were from Sigma Chemical Co. (St. Louis,
MO). Silica gel 60 plates (20 x 20 cm, 0.25-mm thickness) for TLC were from
Merck (Darmstadt, Germany). Bakerbond silica gel columns were purchased from
J. T. Baker, Inc. (Phillipsburg, NJ). Dextrose was from HarÃ-anTeklad (Madison,
WI). Cellulose, casein, DL-methionine, choline bitartrate, AIN-76 vitamin, and
AIN-76 mineral mix were purchased from Bio-Serve (Frenchtown, NJ). Corn oil
was kindly provided by Traco Labs (Seymour, IL). Vacuum-deodorized Menha
den fish oil was provided by the NIH Fish Oil Test Material Program, Southeast
Fisheries Center (Charleston, SC). High methoxylated pectin was from Grindsted
(Industrial Airport, KS).
Animals and Diets. The animal use protocol for these experiments was
approved by the University Animal Care Committee at Texas A&M Univer
sity. All animals were treated in accordance with the NIH Guide for the Care
and Use of Laboratory Animals (NRC 1985). Eighty male weanling Spraguc-
Dawley rats (HarÃ-an, Houston, TX) were housed individually in cages in a
temperature- and humidity-controlled facility with a 12-h light/dark cycle.
After a 3-day acclimation period of consuming a nonpurified diet, rats were
assigned randomly to one of 8 treatments (10 rats/treatment) ina2x2x2
factorial design with 2 fats, 2 fibers, with or without carcinogen. The diet
compositions are shown in Table 1. The two fats were fish oil (11.5 g/100 g
diet) and corn oil (15 g/100 g diet). The fish oil diet contained 3.5 g corn
oil/100 g diet to ensure that essential fatty acid requirements were met (14).
Corn oil and fish oil contained identical levels of tert-butyl-hydroquinone
(0.025%) and vitamin E (1.5 mg/g a-tocopherol and 1.0 mg/g y-tocopherol).
The two fibers were pectin and cellulose (6 g/100 g diet). Each group was
divided further into + or - carcinogen treatment. Food and water were
available freely.
Carcinogen Administration. After 1 week of consuming semipurified
diets, the rats were given injections 2 times at 1-week intervals with
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Research.
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