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Institut für Biochemie und Technologie der Fette, H. P. Kaufmann-Institut, BAGKF, D-48147 Münster, Germany
1To whom correspondence should be addressed. E-mail: ibtfett{at}uni-muenster.de.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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-linolenoyl (Ln) moieties, e.g., -linolenoyl-linoleoyl-oleoylglycerols (LnLO) and -linolenoyl-dioleoylglycerols (LnOO) from the rapeseed oil diet were not prominent constituents of rat adipose tissue triacylglycerols, whereas LOP from rapeseed oil and olive oil diets and OOP from rapeseed oil and sunflower oil diets were distinctly enriched in the corresponding adipose tissues. Most of the minor molecular species of the dietary triacylglycerols from all the three diets were distinctly present in the corresponding adipose tissues. Thus, despite numerous biochemical processes involved in the metabolism of dietary triacylglycerols, a substantial proportion of the molecular species of adipose tissue triacylglycerols containing linoleoyl (L), oleoyl (O) and palmitoyl (P) moieties resemble those of dietary triacylglycerols.
KEY WORDS: • rapeseed oil • olive oil • sunflower oil • triacylglycerol molecular species • rats • adipose tissue
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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,2
). Moreover, the actions of adipose tissue lipases on a triacylglycerol molecule seem to depend on the polarity of the molecular triacylglycerol species, i.e., the number of double bonds of the acyl moieties present in an individual triacylglycerol molecule (3
–5
).
Dietary fats affect the fatty acid composition of adipose tissue triacylglycerols of humans (2
,6
,7
), rats (8
,9
) and rabbits (10
); however, very little is known about the effects of dietary fats on the molecular species of adipose tissue triacylglycerols (1
,11
–13
).
In a continuation of our earlier studies on the effects of dietary oils on tissue lipid composition of rats (13
–16
), we report here the effects of dietary canola-type rapeseed oil (RAP), olive oil (OLI) and conventional sunflower oil (SF) on the composition of fatty acids and molecular species of triacylglycerols of subcutaneous, epididymal and perirenal adipose tissues of rats.
The aim of our study was to determine the molecular structure of the various triacylglycerols in adipose tissues after consumption of various plant oils. These data should provide a better understanding of the deposition and mobilization of fatty acids in adipose tissues of obese and nonobese individuals after ingestion of fats and oils with different fatty acid and molecular species composition.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Triacylglycerol and fatty acid methyl ester standards were purchased from Sigma-Aldrich (Deisenhofen, Germany). Analytical grade and HPLC-grade solvents were products of E. Merck (Darmstadt, Germany).
Diets.
Refined, bleached and deodorized rapeseed oil was kindly provided by W. Holtmeier, Noblee & Thörl, Hamburg, Germany. Native olive oil and refined sunflower oil as well as corn oil were purchased from a local supermarket. Isocaloric pelleted diets (metabolizable energy 13.1 kJ/g) containing recommended levels of protein, carbohydrates, vitamins and nutrient minerals (17
) as used in the semipurified Altromin standard diet (Kontrolldiät C 1000) for rats3
and one of the above experimental oils (120 g/kg diet) plus corn oil (20 g/kg diet) were prepared by Altromin International, Lage, Germany.
Animal experiments.
Weaned male Wistar rats (Lippische Versuchstierzucht, Extertal, Germany) weighing 85–90 g were caged individually and divided into groups of 10. The rats were kept in rooms with adequate ventilation at a temperature of 22°C and a relative humidity of 60% with a 12-h light:dark cycle. The rats had free access to food and water at all times until 12 h before they were killed.
Rats were fed for 10 wk. At the end of the feeding, the rats were killed by subjecting them to ether narcosis followed by sectioning of the aorta. All procedures for the rat experiments were approved by the official commission for animal experimentation [Der Regierungspräsident Münster, permission no. 26.0834 (48/90) of November 29, 1990]. Subcutaneous, epididymal and perirenal adipose tissues were rapidly removed and kept frozen at -60°C until the lipids were extracted.
Lipid analysis.
Lipids were extracted from the adipose tissues and feeds according to Bligh and Dyer (18
). Total lipids were fractionated by TLC on Silica Gel H (E. Merck) using hexane/diethyl ether/acetic acid (80:20:1, v/v/v). The fractions of triacylglycerols, which had been identified by cochromatography with a standard, were scraped out, extracted from silica gel with water-saturated diethyl ether, blown with nitrogen until dry and stored in hexane under nitrogen at - 20°C. Aliquots of the triacylglycerol extracts (
1 mg) were treated with 50 µL trimethyl sulfonium hydroxide and 200 µL dichloromethane to prepare methyl esters of their constituent fatty acids. The mixture was shaken vigorously for 1 min and kept at room temperature for 15 min before direct injection onto gas chromatograph (19
).
Methyl esters were analyzed by gas chromatography in a Hewlett-Packard 5890 instrument (Böblingen, Germany) on a 40-m DB-23 (methyl/50%-cyanopropyl silicone, J & W, ASS-Chem, Bad Homburg, Germany) fused silica capillary column (0.18 mm i.d., 0.2-µm film thickness). Hydrogen was used as carrier gas at 20 cm/s linear velocity and a split ratio of 1:10. The temperature was programmed from 170°C (17 min isothermal) at 7°C/min to 225°C (10 min isothermal). Injector and detector temperatures were set at 280°C. Peaks were integrated using a Hewlett-Packard GC ChemStation software.
Aliquots of triacylglycerols from adipose tissues and food were analyzed for their molecular species composition by HPLC (1
,20
) as follows. The HPLC system consisted of a Merck-Hitachi pump L-6200 (E. Merck) equipped with a Kontron (Kontron Instruments, Milan, Italy) UV/Vis HPLC 332 detector (E. Merck) set to a wavelength of 210 nm and an ACS (Applied Chromatography Systems, Macclesfield, UK) mass detector model 750/14 (thermostated to 55°C), which were used in series. UV and mass traces were monitored and evaluated in a KromaSystem 2000 data acquisition unit (Kontron Instruments). Triacylglycerol species were separated isocratically with acetone-acetonitrile (62:38, v/v) on a Merck LiChrospher RP-18 column (250 mm x 4 mm i.d. and precolumn) at 20 and/or 25°C. The flow rate was set at 1 mL/min. Injections (0.2 mg triacylglycerols) were carried out with a Rheodyne 7161 sample injector (Cotati, CA) equipped with a 20-µL sample loop. Synthetic triacylglycerol standards and those isolated from rapeseed oil, olive oil and sunflower oil by argentation TLC were used for comparison.
Statistical analysis.
Statistical evaluation of the data was conducted using a Statgraphics one-way (ANOVA) computer program (STSC, Rockville, MD); a probability value (P) of <0.01 was considered to be significant in the multiple range analysis. Cochran’s C test and Bartlett’s test were used as statistical tests for homogeneity of variance (21
). ANOVA was performed on the homogenous data. If ANOVA was significant, Tukey’s honestly significant differences test (21
) was used for pairwise comparisons between groups using the above computer program.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, show that the major differences between the dietary triacylglycerols were in the levels of oleic acid [18:1(n-9)]4
linoleic acid [18:2(n-6)], and linolenic acid [18:3(n-3)]. Thus, the dietary triacylglycerols of the groups RAP and OLI had much higher proportions of 18:1(n-9) than those of the SF group, whereas the proportion of 18:2(n-6) was substantially higher in the SF group than in the RAP and OLI groups (Table 1)
. Dietary triacylglycerols of the RAP group, as opposed to OLI and SF, contained a large proportion of 18:3(n-3), whereas those of all three groups contained similar proportions of palmitic (16:0) acid (Table 1)
.
|
. Figure 1
shows the tracings of HPLC separations of the molecular species of triacylglycerols of the epididymal adipose tissue of the OLI group in comparison with the triacylglycerols of the corresponding food. In the RAP group, LOO were the most abundant molecular species, followed by OOO, LLO, LnOO and LnLO, whereas in the OLI group, OOO was the predominant species, followed by OOP and LOO (Table 1)
. In the SF group, both LLL and LLO were predominant molecular species, followed by LLP, LOP and LOO (Table 1)
.
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) showed the following. Body weights of the rats fed the different diets did not differ significantly. Food consumption over the 10-wk period for the groups RAP, OLI and SF was 1867, 1900 and 2000 g/rat, respectively. The corresponding weight gains were 36.7, 32.1 and 35.0 g/wk, respectively. Groups did not differ in heart weight or heart lipid content, plasma total cholesterol or plasma triacylglycerols.
In the present experiment, the fatty acid composition of the triacylglycerols of subcutaneous, epididymal and perirenal adipose tissues of the experimental rats (Table 2
) broadly reflected the composition of the dietary oils (Table 1)
. Thus, adipose tissue triacylglycerols of the rats that had consumed the RAP and OLI diets contained 18:1(n-9) as the most abundant constituent acyl moiety, followed by 18:2(n-6), whereas 18:3(n-3) moieties were detected as substantial constituents only in the adipose tissue triacylglycerols of the RAP group (Table 2)
. Linoleic acid, 18:2(n-6), was esterified in the adipose tissue triacylglycerols at significantly higher levels in rats fed the SF diet compared with the groups fed the RAP and OLI diets, whereas the proportion of palmitic acid in the adipose tissue triacylglycerols did not differ among the three groups (Table 2)
. The levels of individual acyl moieties in triacylglycerols of subcutaneous, epididymal, and perirenal adipose tissues within a feeding group (RAP, OLI or SF) did not differ significantly (Table 2)
.
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, 10
) of predominant acyl moieties and molecular species of triacylglycerols in subcutaneous, epididymal and perirenal adipose tissues of rats fed RAP, OLI, and SF diets for 10 wk are given in Table 3
. DI are defined as the ratio of an individual acyl moiety or molecular species of triacylglycerols in the adipose tissues to that in the diets. Consequently, a DI >1 indicates an enrichment of a particular acyl moiety or molecular species of triacylglycerols in adipose tissues with respect to their concentration in the diet, whereas a DI <1 shows a corresponding reduction in the concentration of an acyl moiety or a molecular species. Palmitoyl (16:0) moieties were enriched in the various adipose tissues irrespective of the diet, whereas 18:0 moieties were slightly enriched in rats fed the RAP diet only. The DI of 18:1(n-9) moieties of triacylglycerols were 1 in all three adipose tissues of each group, demonstrating no preferred deposition, whereas the DI of 18:2(n-6) moieties were slightly reduced and those of 18:3(n-3) moieties were distinctly reduced for both RAP and OLI groups (Table 3)
, which is consistent with the literature (2
).
|
. In the RAP group, the triacylglycerol species LOO, which was the most predominant constituent of the dietary oil (Table 1)
, was also the most abundant constituent of the adipose tissue triacylglycerols (Table 4)
. The species OOO and LLO, which were also major constituents of the dietary triacylglycerol of the RAP group (Table 1)
, were present in substantial proportions in the corresponding adipose tissues (Table 4)
. Moreover, the DI for each of the triacylglycerol species, LOO, OOO and LLO, was close to 1 (Table 3)
. However, LnLO and LnOO, two major species of triacylglycerols of the RAP diet, were found in rather small proportions in the corresponding rat adipose tissues, whereas LOP and OOP, two minor constituents of the dietary triacylglycerols, were found to be enriched (DI 3–5) in the adipose tissue triacylglycerols of the RAP group (Tables 1
,3
and 4
). In addition, a few minor dietary triacyglycerol species, e.g., LLL, LnLP, LLP, and LnOP of the RAP diet were also detected in the rat adipose tissues (Tables 1
and 4
).
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2) in the adipose tissues (Tables 1
,3
and 4
). A few minor triacyglycerol species, e.g., LLO, OPP and OOS were detected as minor constituents of the adipose tissue triacylglycerols (Tables 1
and 4
).
Similarly, in the SF group, the major dietary triacylglycerol species, LLL and LLO, were predominant constituents of the adipose tissue triacylglycerols (Tables 1
and 4
), although for each of these molecular species, the DI was <1 (Table 3)
. On the other hand, LLP, LOO and LOP, which are also main molecular species of the SF diet, were obviously enriched (DI 2–4) in the corresponding rat adipose tissues (Tables 1
,3
and 4
). The OOP species, a minor constituent of the dietary triacyglycerols in the SF group (Table 1)
, was detected in substantial proportions in the rat adipose tissue triacylglycerols (Table 4)
with DI as high as 3 (Table 3)
.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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).
It is generally accepted that under normal (nonfasting) dietary conditions, a substantial part of adipose tissue triacylglycerols is derived from triacylglycerols of intestinal mucosa, which, in turn, results from dietary triacylglycerols via lipolysis at the sn-1,3-positions in the intestinal lumen and reacylation of the resulting sn-2-monoacylglycerols in the intestinal mucosa (23
). The acylation of sn-2-monoacylglycerols in intestinal cells is mediated by monoacylglycerol acyltransferase and diacylglycerol acyltransferase (24
). The triacylglycerols of intestinal mucosa are transported to various tissues, including adipose tissue, via chylomicrons (23
). Circulating triacylglycerols are hydrolyzed by tissue-specific lipoprotein lipases (25
) and the fatty acids released enter the adipocytes (26
). The fatty acids are then converted to triacylglycerols of the adipose tissues, possibly via the glycerol-3-phosphate pathway (27
–29
). Together with the transfer of endogenous acyl moieties, this may result in adipose tissue triacylglycerols with a positional distribution of fatty acids different from those of the dietary triacylglycerols. Therefore the composition and stereospecific distribution of acyl moieties of mucosal triacylglycerols, and consequently, of adipose tissue triacylglycerols are determined not only by the composition and positional distribution of acyl moieties in dietary triacylglycerols, but also by the substrate specificity and stereospecificities of the acyltransferases in intestine and adipose tissues as well as the substrate specificitiy of the lipoprotein lipases (23
,24
).
In the present study in rats fed oils with widely varying fatty acid and triacylglycerol compositions, both the composition of the acyl moieties and of the molecular species of triacylglycerols of subcutaneous, epididymal and perirenal adipose tissues broadly reflect those of the dietary triacylglycerols (Tables 1
to 4
). Most of the major molecular species of dietary triacylglycerols (e.g., LOO, OOO, and LLO from rapeseed oil, OOO, OOP and LOO from olive oil, as well as LLL, LLO, LLP, LOO and LOP from sunflower oil) were the predominant molecular species of the corresponding rat adipose tissue triacylglycerols (Tables 1
–4
). However, a few major dietary molecular species containing -linolenoyl moieties, such as LnLO and LnOO of the RAP diet, were present in rather small proportions in the corresponding rat adipose tissues (Tables 1
,3
and 4
). On the other hand, a few minor species of the triacylglycerols, such as LOP and OOP in the RAP diet and LOP in the OLI diet, were distinctly enriched in the adipose tissue triacylglycerols of the corresponding groups (Tables 1
,3
and 4
), which can be attributed to incorporation of endogenous palmitic and oleic acids into adipose tissue triacylglycerols. Moreover, most of the minor constituent molecular species of dietary triacylglycerols were distinctly present as minor constituents of the corresponding rat adipose tissues. These results broadly agree with those reported by Perona et al. (1
) for the fatty acid and molecular species composition of triacylglycerols of subcutaneous and perirenal adipose tissues from rats fed olive and sunflower oil. Some minor differences may be explained by the portion of corn oil added to the various plant oils in our feeding experiments.
It appears from our data that despite alterations by the endogenous fatty acid pool and numerous other physiologic processes occurring during the transport of long-chain triacylglycerols and their derivatives via intestinal mucosa, lymph and blood to adipose tissue, the overall composition of the individual molecular species of the dietary triacylglycerols is broadly reflected by the molecular species composition of the adipose tissue triacylglycerols in rats (Tables 1
–4
). Interestingly, the proportions of several dietary species of triacylglycerols containing linoleoyl and -linolenoyl moieties, such as LLL, LLO, LnLO and LnOO, were distinctly lower in the adipose tissues of the group fed rapeseed oil than in the RAP diet (Tables 1
,3
and 4
) which may be attributed in part to preferential oxidation of the PUFA (30
). This is noteworthy in view of the fact that dietary linoleic and -linolenic acids are precursors of the physiologically important long-chain (n-6) and (n-3) PUFA, respectively, and the corresponding eicosanoids.
A close resemblance between the composition of the acyl moieties and that of the molecular species of triacylglycerols of the three different adipose tissues within the same feeding group (Tables 1
to 4
) was also observed previously in rats fed coriander oil and high oleic sunflower oil (13
). These results suggest that common physiologic and biochemical pathways determine the overall composition of individual molecular species of the triacylglycerols in the three different adipose tissues, which ultimately depends on the fatty acid and molecular species composition of the dietary oils.
In general, our data showed that the molecular species composition of adipose tissue triacylglycerols depends on that of the dietary triacylglycerols, with a reduction of those containing the essential fatty acyl moieties and an enrichment of those containing endogenously synthesized palmitoyl moieties.
Further studies on the stereospecific distribution of fatty acids in dietary triacylglycerols and adipose tissue triacylglycerols should provide evidence about the substrate specificity and stereospecificity of acyltransferases in vivo, which ultimately determine the positioning of individual fatty acids in triacylglycerols, leading to the individual triacylglycerol molecular species.
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FOOTNOTES |
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3 The composition of the semipurified rat standard diet was as follows (per kg diet): crude protein, 170.8 g; disaccharides, 111.4 g; polysaccharides, 151.3 g; crude fiber, 29.9 g; crude ash, 75.8 g; moisture, 53.8 g; p-aminobenzoic acid, 100.0 mg; biotin, 0.20 mg; choline chloride, 1.0 mg; folic acid 10.0 mg; myo-inositol 111.0 mg; nicotinic acid, 50.2 mg; pantothenic acid, 50.1 mg; all-trans retinol, 4.5 mg; thiamin, 20.0 mg; riboflavin, 20.3 mg; pyridoxine hydrochloride, 15.0 mg; cyanocobalamin, 0.04 mg; ascorbic acid, 20.0 mg; cholecalciferol, 0.0125 mg; -tocopherol, 193.6 mg; menadione, 10.0 mg; available phosphorus, 7.16 g; calcium, 9.26 g; chlorine, 3.63 g; cobalt, 0.13 mg; copper, 5.5 mg; fluorine, 4.17 mg; iodine, 0.45 mg; iron, 0.18 g; magnesium, 0.67 g; manganese, 0.10 g; molybdenum, 0.20 mg; potassium, 7.01 g; selenium, 0.32 mg; sodium 2.44 g; sulfur, 2.0 g; zinc, 28.8 mg. In addition, the RAP diet contained 120 g rapeseed oil plus 20 g corn oil/kg diet, the OLI diet 120 g olive oil plus 20 g corn oil/kg diet and the SF diet 120 g sunflower oil plus 20 g corn oil/kg diet.
4 Fatty acids are designated by number of carbon atoms: number of double bonds as well as (n-x) nomenclature giving the position of double bonds, e.g. 18:1(n-9), oleic acid; acyl moieties in triacylglycerols are designated by O, oleoyl; L, linoleoyl; Ln, linolenoyl; P, palmitoyl, S, stearoyl, e.g., LnLO, linolenoyl-linoleoyl-oleoylglycerol.
Manuscript received 2 October 2001. Initial review completed 13 November 2001. Revision accepted 23 December 2001.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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