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* Centre for Nutrition and Food Safety School of Biological Sciences and ** European Institute of Health and Medical Sciences, University of Surrey, Guildford, Surrey, GU2 5XH, United Kingdom
1To 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: • lipoprotein lipase • fatty acids • fish oils • oxidative stress • rats • maternal nutrition
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Many papers have been published describing the changes in plasma
enzymes and lipid profiles during postnatal development in rats
(Mao and Hamosh 1992
, Planche et al. 1980
, Semenkovich et al. 1989
). High circulating
triglyceride levels occur immediately postpartum which relate to the
low clearing ability of extrahepatic tissues and the sudden high fat
intake as suckling commences. This places the animal into a state where
the pathways for fat clearance are overloaded (Hamosh et al. 1978
). Upon weaning onto a low-fat diet, plasma lipid
levels drop and there is a concomitant fall in intestinal lipase levels
(Deschot-Larkman et al. 1971
, Verger 1984
).
To date, there are few data on the long-term effects of early
dietary fatty acid composition on LPL expression and activity. There is
much interest at present in the mechanisms by which fatty acids may
control gene expression (Gustafsson 1998
). One study
found higher LPL activity in rats from small litter sizes independent
of age (El Habet et al. 1979
) which is
consistent with an early and long-term determination of the enzyme
activity. Reiser and Sidelman (1972)
demonstrated that exposure of
neonatal male rats to high levels of milk cholesterol protected them as
adults from dietary-induced hypercholesterolemia. They suggested
that early exposure to a high-cholesterol diet initiated mechanisms
that maintained serum cholesterol at lower concentrations later in
life, again pointing toward the idea of biological imprinting or
programming. Potential mechanisms of metabolic imprinting were
discussed in a recent review (Waterland and Garza 1999
),
but, as they state, "hypothesis-driven" investigations of possible
mechanisms were scant.
Epidemiological studies in humans have demonstrated association between
disproportionate fetal growth and cardiovascular disease
(Langley-Evans et al. 1998
). However, the paucity of
controlled prospective studies has meant slow progress regarding
mechanistic explanations. It is the apparent early setting or
programming of enzymes, specifically enzymes involved in lipid
metabolism, which the current study set out to investigate further.
Fish oils which are rich in (n-3) PUFA have been postulated to be
beneficial in several disease states including atherosclerosis,
hypertension and arthritis (Clarke et al. 1988
). The
major (n-3) fatty acids found in fish oil are eicosapentaenoic acid
[20:5(n-3)] and docosahexaenoic acid [22:6(n-3)]. Fish oils have
been shown to reduce hepatic lipogenesis and VLDL secretion and
increase post-heparin plasma LPL activity (Daggy et al. 1987
, Zampelas et al. 1994
). There is much
interest in the effects of (n-3) PUFA on the gene expression of many
key enzymes (Simopoulos 1996
). This interest, in
part stems from benefits in later life associated with breast feeding
(which contains long-chain PUFA) over formula-fed infants
(Lanting and Boersma 1996
) and from evolutionary
evidence suggesting benefits of the diet of Paleolithic man where the
ratio of (n-3) to (n-6) PUFA was much higher than present day
(Broadhurst 1997
). However, one of the disadvantages of
fish oil feeding has been linked to increased peroxidation and
possibility of reducing antioxidant status. There is also evidence that
another hepatic microsomal enzyme (
5 desaturase) is affected by
intrauterine diet (Ozanne et al. 1998
) which has been
linked to the development of insulin resistance. To examine these
effects, the activities of the liver enzymes glutathione reductase,
superoxide dismutase and catalase were measured to assess the influence
of the fish oil diet on oxidative status throughout the study.
Our central hypothesis was that the type of fat received in early life
(both in utero and early life) could determine the level of LPL
activity and gene expression which are maintained into later life. In
addition, if enzyme levels were set by diet in early life, these may be
overloaded in later life during periods of dietary excess. It was
proposed that a diet high in (n-3) PUFA would be associated with higher
levels of LPL activity and gene expression, and lower plasma
triglyceride concentrations following a test meal challenge. Plasma
insulin levels were measured since it affects both LPL activity and
gene expression. Plasma glucose-dependent insulinotrophic
polypeptide (GIP) hormone levels were measured because it has been
shown previously that they can be modified by the fat content of the
diet (Hampton et al. 1983
). In addition GIP may be of
importance with respect to effects of dietary fatty acid composition on
LPL activity via both its direct effects on adipose tissue LPL
(Knapper et al. 1995
) and effects on insulin secretion
via the enteroinsular axis (Morgan 1998
).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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and the fatty acid composition of the oils in Table 2
. The oils were obtained from different sources: coconut oil was
obtained from a specialist Indian supermarket, corn and olive oils from
a local supermarket, palm oil from Akisan Enterprises, London, and fish
oil (MaxEPA) was kindly donated by Seven Seas (Kingston-upon-Hull,
United Kingdom). The same batch of each diet was used for the entire
study and was stored at -20°C throughout the trial to avoid
oxidative degradation. On the day after each litter was born, litter
sizes were standardized to six offspring per dam by distribution of the
young among the dams in each dietary group. The pups were weaned at
21 d old onto the same test diet as the dams for 14 d (first
cull), and then the surviving rats were fed nonpurified diet (Beekay
Universal, Humberside, United Kingdom) with the proximate composition:
180 g/kg protein, 25 g/kg oil (containing 6.8 g/kg saturated fatty
acids and 13.7 g/kg unsaturated fatty acids) and 40 g/kg fiber for 7
wk. The offspring were either killed at 5 wk of age (young fish oil
group n = 17; young mixed oil group n = 10) or at 10 wk of age (adult fish oil group n = 18;
adult mixed oil group n = 8). Food was removed during
the day (0900–1700 h) before the kill and all the rats were fed a test
diet during the night containing mixed oil (50 g/kg) (RM1 Special Diet
Services, Essex, Table 1
).
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). Protocols
involving animals were carried out in accordance with the Animals
(Scientific Procedures) Act, 1986, under project license
number PPL90/306. Measurement of LPL activity.
LPL activity was measured in explants of omental adipose tissue by a
method described by Knapper et al. (1995
). Briefly
explants were cut under a dissecting microscope from the adipose tissue
and following resting in medium 199 for 90 min at 37°C, heparin (2U)
was added and following a further 40 min incubation the medium was
collected for the measurement of heparin-releasable LPL activity.
The LPL activity assay used was as described by Nilsson-Ehle and Schotz (1976)
using the detection of liberated labeled free fatty acids
from a tritiated triolein substrate emulsion. The interassay
coefficient of variation was 4.9% at 0.73 and 5.6% at 2.7 pmol oleate
released/(min(-) . g adipose tissue) at 37°C.
Measurement of LPL mRNA.
Total RNA was extracted from epididymal fat pads by a single step
isolation using an acid guanidinium thiocyanate/phenol/chloroform
mixture (Chomczynski and Sacchi 1987
). RNA content of
the product was measured by absorption at 260 nm. Total RNA (10 µg)
was separated on a denaturing agarose gel (20 g/L) containing 10 mmol/L
3-[N-morpholino] propanesulphonic acid and
formaldehyde (0.3 mol/L), visualized with ethidium bromide and blotted
onto Hybond N+ (Amersham, Herts, UK) membrane using 10x
standard sodium citrate (150 mmol/L of sodium citrate, 1.5 mol/L of
NaCl; pH 7.0). Blots were crosslinked under UV light for 3 min and
baked at 80°C for 2 h. Blots were probed with a subclone of the
LPL recombinant supplied by Oka (Gotoda et al. 1989
) labeled with (32P-dCTP using a
"Megaprime" oligolabelling kit (Amersham). Prehybridization and
hybridization were carried out at 65°C in a rolling oven using
solutions modified from Church and Gilbert (1984)
containing 1 mmol/L
of EDTA, 0.5 mol/L NaHPO4 (pH 7.2) and SDS (70 g/L).
Two 30-min posthybridization washes were carried out at 65°C with a
solution containing 1 mmol/L of EDTA, 40 mmol/L of NaHPO4
(pH 7.2) and SDS (50 g/L).
The bands were visualized by autoradiography and LPL mRNA quantified by densitometric scanning at 550 nm. Normalization of the results was achieved by expression of the results against a second probe for the constitutively expressed protein, ß-actin. The intraassay coefficient of variation for this method was 14% at a ratio of LPL/actin of 91.
Measurement of plasma triglyceride, total cholesterol, glucose, insulin and GIP.
Plasma triglyceride, total cholesterol and glucose concentrations were
assayed spectrophotometrically using colorimetric kits (Unimate 5 Trig,
Unimate 5 Chol and Unimate 5 Gluc HK, respectively) supplied by Roche
Diagnostics (Welwyn Garden City, Herts, United Kingdom). The intraassay
coefficients of variation were 2.4% at 2.38 mmol/L of triglyceride,
1.2% at 7.8 mmol/L of total cholesterol and 0.5% at 4.0 mmol/L of
glucose, respectively. Immunoreactive insulin and GIP were measured in
plasma by radioimmunoassays according to Albano et al. (1972)
and
Morgan et al. (1978)
. The intraassay coefficients of variation were
9.0% at 35 pmol/L insulin and 3.4% at 297 pmol/L GIP.
Measurements of liver enzyme activities.
Rat livers were washed, minced with scissors and homogenized in
potassium chloride solution (11.5 g/L, KCl) on ice. The homogenates
were diluted 1 in 4 with KCl and transferred into sterile centrifuge
tubes and centrifuged at 9,000 x g at 4°C for 20
min. The resultant supernatant was decanted and stored at -20°C.
Superoxide dismutase activity was determined using a method by Salin and McCord (1974)
, catalase by a method described by Baudhuin (1974)
and glutathione reductase by a method described by Carlberg and Mannervick (1975)
. Activity was expressed in U/mg of protein where the
protein content was determined by the Lowry procedure (Lowry et al. 1951
).
Statistical analyses.
Statistical differences were determined using two-way (age X diet) ANOVA followed by a Scheffé post-hoc test to identify the differences using Statistica (version 5) Stat Soft Inc. (Tulsa, OK). Data where the variances were not equal included the insulin, GIP, LPL activity, and gene expression results were log-transformed prior to analysis. Pearson’s Correlations were determined for plasma triglyceride and GIP levels. Differences of P < 0.05 were considered significant. Data are reported as means ± SD unless otherwise stated.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Levels were significantly higher in the fish-oil fed young
compared to the mixed oil-fed young (P < 0.001), but there were no differences between the adult diet groups.
Plasma triglyceride concentrations were higher in the young compared to
the adults in those fed the fish oil diet (P < 0.001). There were significant age (P < 0.05) and
dietary effects (P < 0.001) on the cholesterol
levels but no interaction between diet and age. Plasma total
cholesterol levels did not differ between the diet groups however, as
with the triglycerides values, levels were significantly higher in both
the young groups compared to the adult groups (P < 0.001).
|
There were significant effects of diet, age and an interaction between
diet and age in the epididymal fat LPL mRNA levels (P
< 0.001); gene expression was much higher in the mixed
oil-fed adult rats than in the other groups (Fig. 1
). Omental adipose tissue LPL activity, however, was highest in the fish
oil-fed young rats (P < 0.001), but there were
no significant diet effects nor an interaction between diet and age
(Fig. 2
).
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), but there was no effect of diet. Liver superoxide dismutase activity
was also higher in the young rats fed fish oil than all other groups
(P < 0.05), and there was a significant dietary
effect (P < 0.02) but no interaction between age
and diet (Fig. 4
.). Liver catalase activities were significantly affected by age
(P < 0.001) and diet (P < 0.001), and there was a significant interaction between age and diet
(P < 0.001, Fig. 5
). Activity was lower in the young rats fed fish oils compared to the
adults fed fish oil and the fish oil-fed groups had significantly
higher liver catalase activities than the mixed oil-fed groups of
the same age (P < 0.05).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Although it has been shown that GIP secretion is affected by diet
(Elliott et al. 1993
, Kwasowski et al. 1985
) no significant differences were seen between the two
dietary groups in this study. However, plasma GIP levels were very high
in the young rats compared to those in adulthood and at both ages were
much higher than adult human levels of the hormones. The pattern of
results may have been a result of low levels of intestinal lipase in
the adult animals in the same way as the triglyceride levels with the
GIP levels reflecting slower fat absorption in the adult animals. The
mean GIP levels found in young and adult groups are consistent with its
putative role in activating LPL.
Although the heparin-releasable LPL activities in omental adipose
tissue did not differ between the two dietary groups, there were clear
trends depicted, with higher LPL activity in the fish oil-fed young
rats and adults (P < 0.06). The lack of significance
is in part due to the large variation in LPL values found in the young
group and this may be a reflection of the rapid changes in development
occurring when the young samples were obtained. Higher LPL activity in
response to feeding (n-3) PUFA is consistent with previous work which
has shown that fish oils increase epididymal adipose tissue LPL
activity (Benhizia et al. 1994
, Murphy et al. 1993
).
The extremely high LPL mRNA levels in the mixed oil-fed adult group
were unexpected; previous work by Semenkovich et al. (1989)
compared
LPL mRNA levels in epididymal fat pads taken from rats aged 24 d
with those from adult rats and found similar levels of expression at
the two ages. However, a pronounced increase in rate of cell growth
(cell size and number) occurs in epididymal tissue after 21 d
(Cryer and Jones 1978
). The finding that LPL expression
was so much higher in response to the same test meal in mixed
oil-fed adult rats compared to those fed the fish oil, despite the
groups having similar plasma triglyceride levels, may suggest that the
mixed oil-fed rats are under metabolic controls that keep plasma
triglyceride levels at normal levels. Adipose tissue LPL mRNA and
activity did not follow similar patterns during this study, but they
were measured in different tissues due to the small size of epididymal
fat pads in the young rats. Adipose tissue LPL activity and mRNA have
previously been shown to vary between anatomical sites within one
animal (Cryer et al. 1978
) and in humans
(Ranganathan et al. 1995
).
There were no significant differences in plasma insulin and
nonesterified fatty acid levels in response to changes in early diet.
The only difference in plasma glucose concentrations was a
significantly greater glucose level in young compared to adult rats, in
the fish oil fed group. Previous studies have shown lower plasma
insulin levels following the consumption of a high fish oil diet in
rats (Baltzell et al. 1991
), but as they did not pair
feed the rats, the differences seen could have been due to changes in
actual quantities of food intake.
Cholesterol levels were high in the young rats, suggesting that the
levels had not dropped during the 2 wk after the high-fat diet
exposure during suckling. Reiser and Sidelman (1972)
suggested that
early exposure of rats to a high-cholesterol diet initiated
mechanisms that maintained serum cholesterol at lower concentrations
later in life. The high cholesterol levels in the young rats and those
on in the fish oil-fed groups supports previous findings
(D’Aquino et al. 1991
, L’Abbé et al. 1991
).
Catalase activities previously have been reported to increase in
response to fish-oil feeding (Yamazaki et al. 1987
).
In this study, the elevated catalase activities seen in the young
animals fed fish oil continued into adulthood. This suggests that these
rats remained under oxidative stress despite the cessation of
fish-oil feeding after 5 wk of age. We also found raised superoxide
dismutase activity in the fish oil-fed young, in contrast to
previous studies on (n-3) PUFA that have shown either reduced activity
(L’Abbé et al. 1991
) or no significant difference
(D’Aquino et al. 1991
). However, the absence of a
dietary effect on glutathione reductase activity confirms the findings
of L’Abbé et al. (1991)
who found no effect of fish-oil
feeding.
In conclusion, the majority of differences shown in this study were
between the two age groups rather than between the two diet groups at
each age. This suggests that changes in the postprandial handling of a
standard test meal are more affected by age than by early dietary fatty
acid composition. However, early diet did affect LPL expression and
catalase activity later in life, which may indicate important
biological imprinting mechanisms for these fatty acids, especially in
the areas of the control of gene expression and in the handling of
oxidative stress. Oxidative load, in particular, has been associated
with premature aging and has been suggested by Van Assche et al. (1998)
as a possible link between dietary insufficiency in fetal life and
adverse consequences in later life.
Future studies are required to elucidate the mechanisms of these effects. If, through changes in dietary availability or formulation, potentially beneficial alterations in gene expression can be shown in rodents and other animal models, there would be grounds on which to explore the effects of modifying diet in pregnant women and possibly formula composition for infants.
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FOOTNOTES |
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Manuscript received February 17, 1999. Initial review completed May 18, 1999. Revision accepted October 22, 1999.
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
1. Albano J. D. M., Ekins R. P., Maritz G., Turner R. C. A sensitive, precise radioimmunoassay of serum insulin relying on charcoal separation of bound and free hormone moieties. Acta Endocinol 1972;70:487-509
2. Baltzell J. K., Wooten J. T., Otto D. A. Lipoprotein lipase in rats fed fish oil: apparent relationship to plasma insulin levels. Lipids 1991;26:289-294[Medline]
3. Baudhuin P. Isolation of rat liver peroxisomes. Meth. Enzymol. 1974;31:356-368[Medline]
4.
Benhizia F., Hainault I., Serouge C., Lagrange D., Hajduch E., Guichard C., Malewiak M.-I., Quignard-Bolangé A., Lavau M., Griglio S. Effects of a fish oil-lard diet on rat plasma lipoproteins, liver FAS, and lipolytic enzymes. Am. J. Physiol. 1994;267:E975-E982
5. Broadhurst C. L. Balanced intakes of natural triglycerides for optimum nutrition: an evolutionary and phytochemical perspective. Med. Hypoth. 1997;49:247-261[Medline]
6.
Carlberg I., Mannervick B. Purification and characterisation of the flavoenzyme glutathione reductase from rat liver. J. Biol. Chem. 1975;250:5475-5480
7. Chomczynski P., Sacchi N. Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987;162:156-169[Medline]
8.
Church G. M., Gilbert W. Genomic sequencing. Proc. Nat. Acad. Sci. (USA) 1984;81:1991-1995
9.
Clarke S. D., Benjamin L., Bell L., Phinney S. D. Fetal growth and fetal lung phospholipid content in rats fed safflower oil, menhaden oil, or hydrogenated coconut oil. Am. J. Clin. Nutr. 1988;47:828-835
10. Cryer A., Jones H. M. Changes in lipoprotein lipase (clearing factor lipase) activity of white adipose tissue during development of the rat. Biochem. J. 1978;172:319-325[Medline]
11. Cryer A., Kirtland J., Jones H. M., Gurr M. I. Lipoprotein lipase activity in the tissue of guinea pigs exposed to different fats from conception to three months of age. Biochem. J. 1978;170:169-172[Medline]
12. Daggy B., Arost C., Bensadoun A. Dietary fish oil decreases VLDL production rates. Biochim. Biophys. Acta 1987;920:292-300
13. D’Aquino M., Benedetti P. C., Di Felice M., Gentili V., Tommassi G., Maiorino M., Ursini F. Effect of fish oil and coconut oil on the antioxidant defence system and lipid peroxidation in rat liver. Free Rad. Res. Com. 1991;12/ 13:147-152
14. Deschot-Larkman M., Robberecht P., Camus J., Christophe J. Short term adaption of pancreatic hydrolases to nutritional and physiological stimuli in adult rats. Biochimie 1971;53:789-796[Medline]
15. El Habet A., Aust L., Noack R. The influence of postnatal nutrition on lipoprotein lipase activity and hormone sensitive lipolysis in vitro of rat adipose tissue. Acta Biol. Med. Germanica 1979;38:601-609
16.
Elliott R. M., Morgan L. M., Tredger J. A., Deacon S., Wright J., Marks V. Glucagon-like peptide-1 (7–36) amide and glucose dependent insulinotropic polypeptide secretion in response to nutrient ingestion in man: acute post-prandial and 24-h secretion patterns. J. Endocrinol. 1993;138:159-166
17.
Gotoda T., Senda M., Gamou T., Furuchi Y., Oka K. Nucleotide sequence of human cDNA coding for a Lipoprotein lipase (LPL) cloned from placental cDNA library. Nuc. Acid. Res. 1989;17:2351
18. Gustafsson J. A. Fatty acids in control of gene expression. Nutr Rev. 1998;56:s20-1-s54-75[Medline]
19. Hamosh M., Simon M. R., Canter H., Hamosh P. Lipoprotein lipase activity and blood triglyceride levels in fetal and newborn rats. Paediatr. Res. 1978;12:1132-1136[Medline]
20. Hampton S. M., Kwasowski P., Tan K., Morgan L. M., Marks V. Effects of pretreatment with a high fat diet on the gastric inhibitory polypeptide (GIP) and insulin responses to oral triolein and glucose in rats. Diabetogoia 1983;24:278-281
21. Knapper J. M. E., Puddicombe S. M, Morgan L. M., Fletcher J. M., Marks V. Investigations into the actions of GIP & GLP-1 (7–36) amide on LPL activity in explants of rat adipose tissue. J. Nutr. 1995;125:183-388
22. Kwasowski P., Flatt P. R., Bailey C. J., Marks V. Effects of fatty acid chain length and saturation on gastric inhibitory polypeptide release in obese hypertriglycaemic (ob/ob) mice. Biosci. Reports 1985;5:701-705[Medline]
23. L’Abbé M. R., Trick K. D., Beare-Rogers J. L. Dietary (n-3) fatty acids affect heart, liver and aortic protective enzyme activities and lipid peroxidation. J. Nutr. 1991;121:1331-1340
24. Langley-Evans S. C., Gardner D. S., Welham S. J. Intrauterine programming of cardiovascular disease by maternal nutritional status. Nutr 1998;14:39-47
25. Lanting C. I., Boersma E. R. Lipids in infant nutrition and their impact on later development. Cur. Opinion Lipid. 1996;7:43-47
26.
Lowry O. H., Roseborough N. H., Farr A. L., Randall R. J. Protein measurements with the Folin phenol reagent. J. Biol. Chem. 1951;193:265-275
27. Mao J., Hamosh M. Postnatal development of plasma-lipid-clearing enzymes (lipoprotein lipase, hepatic lipase and lecithin: cholesterol acyl transferase) and lipid profiles in suckling rats. Biol. Neonate 1992;62:1-9[Medline]
28. Morgan L. M. The role of gastro-intestinal hormones in carbohydrate and lipid metabolism and homeostasis: effects of GIP and GLP-1. Biocem. Soc. Trans. 1998;26:216-222
29. Morgan L. M., Morris B. A., Marks V. Radioimmunoassay for gastric inhibitory polypeptide. Ann. Clin. Biochem. 1978;15:172-177[Medline]
30. Murphy M. C., Zampelas A., Puddicombe S. M., Furlonger N. P., Morgan L. M., Williams C. M. Pre-Translational regulation of the expression of the lipoprotein lipase gene by dietary fatty acids in the rat. Br. J. Nutr. 1993;70:727-736[Medline]
31. Nilsson-Ehle P., Schotz M. C. A stable, radioactive substrate emulsion for assay of lipoprotein lipase. J. Lipid Res 1976;17:536-541[Abstract]
32. Ozanne S. E., Martensz N. D., Petry C. J., Loizou C. L., Hales C. N. Maternal low protein diet in rats programmes fatty acid desaturase activities in the offspring. Diabetologia 1998;41:1337-1342[Medline]
33.
Planche E., Boulange A., De Gasquet P., Tonnu N. T. Importance of muscle lipoprotein lipase in rats during suckling. Am. J. Physiol. 1980;238:E511-E517
34.
Ranganathan G., Ong J. M., Yukht A., Saghizadeh M., Simsolo R. B., Pauer A., Kern P. A. Tissue specific expression of human lipoprotein lipase. J. Biol. Chem. 1995;270:7149-7155
35. Reiser R., Sidelman J. Control of cholesterol homeostasis by cholesterol in the milk of the suckling rat. J. Nutr. 1972;102:1002-1016
36. Salin M. L., McCord J. M. Superoxide dismutase in polymorphonuclear leukocytes. J. Clin. Invest. 1974;54:1005-1009
37. Semenkovich C. L., Chen S.-H., Wims M., Luo C.-C., Li W.-H., Chan L. Lipoprotein lipase and hepatic lipase mRNA tissue specific expression, developmental regulation, and evolution. J. Lipid Res 1989;30:423-431[Abstract]
38. Simopoulos A. P. The role of fatty acids in gene expression: Health implications. Ann. Nutr. Metab. 1996;40:303-311[Medline]
39. Van Assche F. A., Holemans K., Aerts L. Fetal growth and consequences for later life. J. Perinatal Med. 1998;26:337-346[Medline]
40. Verger R. Pancreatic Lipase. Borgstrom B. Brockman H.L. eds. Lipases 1984:151-183 Elsevier Amsterdam
41.
Waterland R. A., Garza C. Potential mechanisms of metabolic imprinting that leads to chronic disease. Am. J. Clin. Nutr. 1999;69:179-197
42. Yamazaki R. K., Shen T., Scade G. B. A diet rich in (n-3) fatty acids increases peroxisomal ß-oxidation activity and lowers plasma triacylglycerols without inhibiting glutathione-dependent detoxification activities in the rat liver. Biochim. Biophys. Acta 1987;920:62-67[Medline]
43. Zampelas A., Murphy M. C., Morgan L. M., Williams C. M. Postprandial lipoprotein lipase, insulin and gastroinhibitory polypeptide responses to test meals of different fatty acid composition: comparison of saturated, (n-6) and (n-3) polyunsaturated fatty acids. Eur. J. Clin. Nutr. 1994;48:21-30
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