Role of fatty acids in adipocyte growth and development

M. J. Azain

J ANIM SCI 2004, 82:916-924.

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 Role of fatty acids in adipocyte growth and development1,2
M. J. Azain3
Animal and Dairy Science Department, University of Georgia, Athens 30602
ABSTRACT: Fat is typically added to diets as a
source of energy. The alternative aspects considered
here are the use of specific fats to alter the fatty acid
profile of adipose tissue toward creation of value-added
products and the potential for individual fatty acids to
alter gene expression and control adipose tissue devel-
opment. Emphasis is placed on the omega-3 fatty acids,
such as those found in fish oil, and on CLA. The most
common association of fatty acids with adipose tissue
is related to their storage as triglycerides in mature
adipocytes and the consequences of excess accumula-
tion in obesity. Fatty acids and their derivatives also
can have hormone-like effects and have been be shown
to regulate gene expression in preadipocytes, which ul-
timately effects their proliferation and differentiation.
Long-chain, saturated, and polyunsaturated fatty acids
have been shown to regulate transcription factors, such
as CCAAT/enhancer binding protein, peroxisome prolif-
Key Words: Adipocytes, Conjugated Linoleic Acid, Gene Expression, Omega-3 Fatty Acids
2004 American Society of Animal Science. All rights reserved.
Introduction
Conventional reasons to add fat to animal diets in-
clude: use as an energy source, to control dust and
improve palatability of the diet, and in rare cases, as
a source of essential fatty acids. Alternative reasons
for fat supplementation are the focus of this discus-
sion, and these include 1) alteration of the fatty acid
profile of a particular product and thus creation of
“value-added” products and 2) alteration of adipose
development via fatty acid effects on gene expression.
The effects of dietary fat on tissue fatty acid profile
and on adipocyte development have been investigated
1
Publication of this symposium paper is supported by USDA/ARS.
2
Presented at the ASAS Symposium: Alternative Aspects of Adipo-
cyte Function, Phoenix, AZ. The author wishes to express his appreci-
ation to S. Duckett, G. Hausman, H. Mersmann, and S. Poulos for
their input and assistance in the preparation of this manuscript.
3
Correspondence—phone: 706-542-0963; fax: 706-542-0399; e-
mail: mazain@arches.uga.edu.
Received July 10, 2003.
Accepted October 11, 2003.
916
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erator activated receptor, and other adipose-specific
genes, very early in adipocyte development. These ef-
fects have the potential to affect fat cell number at
maturity. Specifically, there is evidence that the fatty
acids in fish oil, such as docosahexaenoic and eicosopen-
taenoic acids, and fatty acids in the CLA series, de-
crease preadipocyte proliferation in cell lines and re-
duce adiposity in rodents. There is little direct evidence
of the ability of fatty acids to manipulate adipocyte
development in non-rodent species. The genetic, nutri-
tional, and pharmacological manipulation of adipose
tissue in meat animals has long been of interest to
animal scientists. An understanding of the ability of
fatty acids to regulate factors such as adipocyte size
and number, particularly in meat animals, would be of
great interest. The evidence for regulatory roles of fatty
acids in development from rodent and in vitro studies
and their potential application to meat animals are re-
viewed.
J. Anim. Sci. 2004. 82:916–924
in both ruminants and nonruminants. Biohydrogena-
tion of dietary fatty acids in the rumen makes manipu-
lation of tissue fatty acids more difficult in ruminant
species (Wood and Enser, 1997). Thus, most of the
emphasis will be on studies in nonruminant species.
Use of Dietary Fat to Create Value-Added
Products with Altered Fatty Acid Profiles
Elevated intakes of saturated fatty acids are associ-
ated with an increased incidence of heart disease, as
well as other human health issues. Because much of
the intake of saturated fat has been associated with
intake of animal products, there has been considerable
interest in reducing total carcass fat and in altering
the profile of fatty acids toward a more unsaturated
pattern. Genetic selection and pharmacological agents
have been used to reduce carcass fat. Dietary fat ma-
nipulation has been used to alter fatty acid profile.
Beginning in the 1980s and 1990s, there was interest
in increasing n-3 fatty acids, whereas recently, the
focus has changed to incorporation of CLA isomers.
Manipulation of muscle or adipose tissue fatty acid
 Fatty acids and adipocytes
profile in non-ruminants by dietary alteration is well
documented. In pigs, there is a linear relationship
(r2 = 0.70) between dietary linoleic acid intake and
percentage of 18:2 in the carcass (Averette-Gatlin et
al., 2002b). Similarly, dose-dependent increases in tis-
sue levels of the long-chain, highly unsaturated fatty
acids found in fish oil are observed in response to their
addition to the diet (Overland et al., 1996).
Omega-3 Fatty Acids
The primary omega-3 fatty acids that have been of
interest are a-linolenic (ALA, 18:3⌬9, 12, 15), eicosapen-
taenoic (EPA, 20:5⌬5, 8, 11, 14, 17), and docosahexaenoic
(DHA, 22:6 ⌬7, 10, 13, 16, 19) acids. This series of fatty acids
are metabolized to the Group 3 series of eicosanoids. In
contrast, n-6 fatty acids, which include linoleic (18:2⌬9,
12
) and arachidonic acids (20:4⌬5, 8, 11, 14), are metabo-
lized to the Group 1 and 2 series of eicosanoids (Chap-
kin, 2000). Interest in increasing the intake of n-3
fatty acids is associated with health benefits of these
compounds or their metabolites (Chapkin, 2000). In
general, the eicosanoids produced from n-3 fatty acids,
particularly EPA and DHA, are less inflammatory,
cause vasodilation, and inhibit platelet aggregation,
compared with those produced from n-6 fatty acids.
Rodents fed fish oil have reduced adipose tissue mass,
although these effects may be gender and strain spe-
cific (Belzung et al., 1993; Fickova et al., 2002).
Studies of primitive diets indicate that humans
likely evolved eating a diet with an n-6:n-3 ratio of
1:1 to 4:1 (Eaton et al., 1996). Due to the high intake
of corn and soy oil, the current diet ratio in developed
countries is greater than 10:1. Thus, future dietary
guidelines in the US will likely not only have recom-
mendations for total fat and polyunsaturated:satu-
rated ratio, but also a recommendation for an n-6:n-
3 ratio. Such guidelines exist in the United Kingdom
(Scollan et al., 2001b).
α-Linolenic acid can be elongated and further desa-
turated to give rise to EPA and DHA and is particu-
larly abundant in linseed oil (ALA, 53%; n-6:n-3 ratio =
0.26). Feeding linseed oil or full-fat flaxseed results
in increased tissue content of ALA in pigs (Romans et
al., 1995a,b; Van Oeckel et al., 1996) and cattle (Scol-
lan et al., 2001a,b). Canola or rapeseed oil contains
approximately 9% ALA and has an n-6:n-3 ratio of
2.5) and also increases the ALA content of pork when
fed to pigs (Leskanich, et al., 1997). Feeding 10% flax-
seed (37% crude fat in seed) for 25 d before slaughter,
resulted in increased ALA (control = 0.19, 15% flax-
seed = 0.75 mg of ALA/g of tissue) and EPA (control =
0.033, 15% flaxseed = 0.055 mg of EPA/g of tissue), but
no change in DHA in muscle (Romans et al., 1995a).
Because EPA and DHA are more direct precursors
for the Group 3 eicosanoids, it would seem more effi-
cient to feed them directly rather than depending on
conversion of ALA. In general, EPA and DHA account
for 15 to 20% of the fatty acids in most fish oils. Feed-
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917
ing fish oil to nonruminants results in increased tissue
content of these fatty acids. Irie and Sakimoto (1992)
reported that feeding diets with 6% fish oil to pigs for
4 wk resulted in a fivefold increase in EPA and a 10-
fold increase in DHA content of pork.
There are, however, potential negative effects asso-
ciated with an increase in n-3 fatty acid content. Be-
cause n-3 fatty acids are liquid at room temperature,
one of the common observations in products enriched
with these fatty acids is that they are oily and often
unacceptable to consumers. Although not observed in
all studies, there is potential for reduced product shelf
life and increased susceptibility to oxidative damage
(Wood and Enser, 1997). Some studies report in-
creased off-flavors in n-3-enriched products. These ef-
fects are less likely with ALA than with the fish oils.
However, it is estimated that the conversion of ALA
to EPA is only 15% efficient (Nettleton, 1991; Winters
et al., 1994). In a study in cattle comparing the effects
of linseed oil and fish oil with a control group, feeding
linseed oil resulted in a twofold increase in the ALA
content of muscle phospholipids and a 50% increase
in EPA (no significant change in DHA). In contrast,
feeding fish oil increases ALA by approximately 30%,
and increases EPA and DHA by 150 and 112%, respec-
tively (Scollan et al., 2001b).
Thus, although it is possible to alter the fatty acid
profile of animal products to enrich their n-3 content,
negative effects, such as decreased firmness, reduced
shelf life, and off flavors, are likely (Wood and Enser,
1997). There are also considerable inefficiencies in the
conversion of these fatty acids from the diet to product.
Feeding a diet with 6% fish oil (approximately 1% EPA
+ DHA) resulted in pork containing approximately 2
mg of EPA and DHA per 100 mg of total fat (Irie and
Sakimoto, 1993). A 100-g serving of pork containing
3 to 5% fat would contribute 60 to 100 mg of these
fatty acids. Although this is significant, the current
recommendations are for an average daily intake of 1
to 4 g. Assuming a feed intake of 3 kg/d, the pig would
have consumed approximately 5 kg of fish oil over the
4-wk period. Finally, the costs associated with keeping
these potentially value-added carcasses segregated
from other product during processing are a further
consideration. Direct consumption of fish is probably
the most efficient way for humans to increase their
intake of EPA and DHA.
Fatty acid profile of poultry products can also be
influenced by diet. Sanz et al (1999a) reported that
whereas feeding polyunsaturated fats resulted in
marked changes in the consistency of abdominal fat
consistency, it resulted in only moderately higher sus-
ceptibility to lipid oxidation as compared to fat from
birds fed more saturated fat sources. Zollitsch et al.
(1997) reported that feeding polyunsaturated fatty
acids (soy or rapeseed oil) improved growth perfor-
mance without negative effects on carcass characteris-
tics. They attributed this effect to improved nutrient
digestibility with unsaturated fatty acids relative to
918
more saturated forms. Although this is a possibility,
it does not explain the reduced fat pad weights that
a number of investigators report with dietary PUFA
in birds (e.g., Newman et al., 2002).
It is much more difficult to manipulate the tissue
fatty acid profile of ruminant animals (Wood and En-
ser, 1997). Scollan et al (2001b) examined diets con-
taining approximately 6% oil from a saturated source,
linseed oil, fish oil, or a combination of linseed and
fish oil. They reported that whereas EPA and DHA
contents doubled with fish oil feeding relative to the
control group, the contribution as a dietary source of
n-3 fatty acids was small (control = 13 mg; fish oil,
20:5 + 22:6 = 28 mg from a 100-g serving of beef).
Hydrogenation rates for EPA and DHA were approxi-
mately 90% (Scollan et al., 2001a). Management sys-
tems seem to have the potential to change fatty acid
composition of beef more than dietary fat source. For
example, grass-fed beef contains significantly more n-
3 fatty acids than would be found in products from
animals fed concentrate or feed lot diets (Duckett et
al., 1993).
Conjugated Linoleic Acid
Conjugated linoleic acid represents a group of posi-
tional and geometric isomers of linoleic acid. There
are a number of reviews that summarize the history
of CLA and its potential mechanism of action (Pariza,
1997; Pariza et al., 2001; Belury, 2002). Conjugated
linoleic acid is formed under anaerobic conditions in
the rumen and large intestine by anaerobic bacteria
(Ha et al., 1989). The predominant isomer in these
natural sources is the cis-9, trans-11 version, which
has anticarcinogenic properties (Ip et al., 1994). Syn-
thetic forms of CLA are produced from oils high in
linoleic acid oils, such as safflower oil, and these con-
tain predominantly the cis-9, trans-11 and trans-10,
cis-12 isomers. With the availability of the synthetic
forms of CLA came the observation that CLA also had
antiobesity effects (Park et al., 1997). It has subse-
quently been shown that these can be attributed to
the trans-10, cis-12 isomer (Park et al., 1999).
The potential health benefits of CLA have contrib-
uted to an interest in identifying means to increase
dietary intake. Developing animal products with in-
creased amounts of CLA represents one means by
which to accomplish this goal. Meat products from
nonruminant animals contain low concentrations of
CLA, primarily the cis-9, trans-11 isomer (Chin et al.,
1992). Numerous studies in pigs and poultry demon-
strate that feeding synthetic forms of CLA results in
increased tissue content (see Azain, 2003). For exam-
ple, feeding 1.25% CLA to growing-finishing pigs for
29 d prior to slaughter resulted in an increase in the
CLA content of loin muscle from undetectable levels
in the control to 5.8 mg/g of fatty acid (Wiegand et al.,
2002). A 100-g serving of pork (assume 3 to 5% fat)
from a pig fed CLA would provide 15 to 25 mg of CLA.
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Azain
In younger pigs fed CLA, the relative percentages in-
corporated into muscle were in the range of 2 to 5%
of the fatty acids (Ramsay et al., 2001). This would
extrapolate to dietary levels of 60 to 250 mg/100-g
serving. Based on extrapolation from rodent studies,
a daily intake of 3 to 5 g of CLA would be needed
to result in dietary levels similar to those that have
anticarcinogenic and antiobesity effects in lab ani-
mals. Thus, as with n-3 fatty acids, it is possible to
increase CLA content, but the cost effectiveness and
practicality of doing so must be questioned.
Unlike n-3 fatty acids, feeding CLA does not have
negative effects on carcass quality. One of the meta-
bolic effects of CLA is that it inhibits ⌬-9 desaturase
(Lee et al., 1998), the enzyme responsible for con-
verting palmitate and stearate to palmitoleic and oleic
acids, respectively. The net effect of this inhibition
is an increase in saturated fatty acid content and a
reduction in iodine value (Averette-Gatlin et al,
2002a), which results in firmer carcass fat characteris-
tics. Although an increase in saturation is contrary to
current dietary recommendations, it should be pointed
out that the calculated atherogenic index (Ulbricht
and Southgate, 1991) of CLA-enriched pork remains
less than that of milk. A decrease in the degree of
unsaturation in animal products due to CLA feeding
also has the potential to increase product shelf life,
although this has yet to be consistently demonstrated.
At least two groups have reported that marbling is
increased in CLA-fed pigs (Averette-Gatlin, 2002a;
Wiegand et al., 2002). This has not been consistently
observed, however (Dugan et al., 1997; Eggert et al.,
2001; Tischendorf et al., 2002).
Dietary Fat and Adipose Tissue Development
The discussion of the effects of dietary fat on adipose
tissue development can be divided into effects on cell
size and those on cell number. Using the pig as a point
of reference, the latter generally occurs postweaning,
whereas the former is associated with late gestation
and the preweaning period (Hausman, 1985). Al-
though it is possible to recruit new adipocytes at any-
time, it is generally agreed that cell number is largely
determined prior to weaning and that increases in
body fat in the growing animal after weaning are ac-
counted for by preexisting cells filling with lipid
(Van, 1985).
Effects of Dietary Fat on Cell Number
Preadipocytes represent a pool of cells that have
the potential to either proliferate or differentiate into
adipocytes. Differentiation is characterized by expres-
sion of adipocyte specific proteins such as lipoprotein
lipase (Cornelius et al., 1994) and is regulated by tran-
scription factors such as CCAATT/enhancer binding
protein-α (C/EBP-α) and peroxisome proliferator ac-
tivated receptor-γ (PPAR-γ; MacDougald and Lane,
 Fatty acids and adipocytes
1995; Shao and Lazar, 1997). Studies in cell culture
systems clearly show the effects that fatty acids have
on proliferation and differentiation of these cells
(Amri et al., 1994). The mechanism by which this oc-
curs involves the fatty acids or their metabolites
(Duplus et al., 2000, 2001). In cases where gene ex-
pression is affected, it is likely that fatty acids are
working through transcription factors such as the per-
oxisome proliferator activated receptors or PPAR.
There are numerous reviews that demonstrate that
the fatty acids or their metabolites such as the prosta-
glandins are ligands for PPAR (Kliewer et al., 1997;
Hertzel and Bernlohr, 1998; Sessler and Ntambi,
1998). In rodents, PPAR-γ is highly expressed in liver,
kidney, heart, and brown adipose tissue, but is not
detected in white adipose tissue (Schoonjans et al.,
1996). Stimulation of PPAR-γ by fatty acids or specific
ligands such as the fibrates, results in increased fatty
acid oxidation ( Kliewer et al., 1997; Wolfrum et al.,
2001). PPAR-γ2 is highly expressed in white adipose
tissue (and at low or undetectable levels in liver) and
its stimulation by fatty acids or specific ligands such
as the thiazolidinediones results in expression of
markers associated with preadipocyte differentiation
(Tontonoz et al., 1994; Schoonjans et al., 1996a,b; Gre-
goire et al., 1998; Thuilier et al., 1998).
In contrast to what has been well documented in the
rodent, both PPAR-α and -γ are expressed in porcine
adipose tissue (Houseknecht et al., 1998; Ding et al.,
2001b; Spurlock et al., 2002). The significance of this
is not yet clear, but emphasizes the danger in extrapo-
lating data from rodent or cell culture systems to large
animals. Similarly, both isoforms (γ-1 and γ-2) of
PPAR-γ are expressed in bovine adipose tissue (Sund-
vold et al., 1997). Expression of PPAR-α has not been
reported in the bovine. However, Kawada et al. (1998)
reported that Wy14,643, a selective ligand for PPAR-
α, stimulated differentiation of bovine fibroblast-like
cells into adipocytes in vivo. This response was less
potent than that seen with the thiazolidinediones,
which are selective for PPAR-γ, suggesting a more
important role for this isoform in differentiation.
In porcine preadipocyte cultures, fatty acids have
been shown to regulate gene expression of both tran-
scription factors and markers of adipocyte differentia-
tion (Ding et al., 2001a,b). However, a clear relation-
ship of fatty acids and transcription factor expression
in relation to adiposity in vivo has not been estab-
lished (Spurlock et al., 2000, 2002; Ding et al., 2003).
Based on patterns of transcription factor and adipo-
cyte specific protein, McNeel et al. (2000) concluded
that use of cell culture systems with porcine stromal
vascular cells as a source of preadipocytes was a valid
method for investigation of adipose development in
the pig. However, they also noted that the relative
pattern and magnitude of change for various tran-
scripts differed from the in vivo situation. Recently,
this group (Ding et al., 2003) reported that despite
strong in vitro effects of fatty acids on transcription,
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919
there were no changes in vivo in response to feeding
fat. This may be due to the presence of mixed cell
populations in vivo, competing fatty acid metabolism,
time of sampling, or various other factors.
Effects of CLA on Adipocyte Differentiation
The CLA isomers are also ligands for PPAR (Belury
et al., 2002; Ding et al., 2000) and have been shown
to affect adipose development and gene expression in
vitro. In vitro, CLA has been shown to inhibit prolifer-
ation of 3T3-L1 cells, a cell line commonly used for the
study of adipocyte development (Brodie et al., 1999;
Satory and Smith, 1999). A potential application of
this observation is that exposure of an animal to CLA
at the time when fat cell number is being determined
might ultimately allow for control of adiposity. We
have tested this possibility in both the pig and rat. In
the rat study (Poulos et al., 2001), pregnant females
were fed diets containing 0 or 0.5% CLA beginning
on d 7 of gestation and continuing through d 21 of
lactation. Progeny were monitored at 11 wk of age.
There was no effect of maternal diet on adipocyte size
or number. It should be noted that whereas it was our
expectation that feeding CLA during gestation would
result in accumulation in the fetus, we were unable
to detect CLA in the pups at birth. CLA was detected
at 11 and 21 d of age, so it is likely that it is transferred
in milk.
In the pig study (Poulos et al., 2000), sows were fed
0 or 0.5% CLA beginning on d 40 or 70 of gestation
and continuing through d 21 of lactation (weaning).
Carcass composition of selected progeny was deter-
mined by ultrasound at 100 kg of BW. As in the rat
study (Poulos et al., 2001), there was no influence of
maternal diet on body composition at market weight
and we were unable to detect CLA in pigs at birth.
Sow milk samples collected on d 7 and 21 of lactation
showed significant increases in CLA in response to
feeding. Conjugated linoleic acid also caused a depres-
sion in milk fat.
These studies fail to confirm that CLA can affect fat
cell number as was reported in vitro (Brodie et al.,
1999; Satory and Smith, 1999). In many cases, effects
of CLA in culture have been investigated with CLA
as the only lipid in the media. This is not physiological.
There is a need to conduct additional work with mixed
fatty acids as would be typical in vivo.
Effects of Dietary Fat on Cell Size.
In comparison with diets with no added fat, there
are characteristic changes in performance associated
with diets supplemented with fat. In the pig, as well
as in other livestock, these include reduced intake,
improved gain and feed efficiency, and increased car-
cass fat. The increase in carcass fat is most likely the
result of increased fat cell size (Steffen et al., 1978).
Addition of fat to the diet results in an increase in the
920
energy density of the diet, which reduces intake (NRC,
1987). The improved growth performance is likely a
combination of the effects of dietary fat on reducing
gut passage rate and increasing digestibility of other
nutrients, and the metabolic effects that result in in-
creased net energy availability. Pettigrew and Moser
(1991) summarized the effects of dietary fat on perfor-
mance and carcass characteristics from over 90 stud-
ies and concluded that the increase in carcass fat was
independent of whether the calorie:protein ratio in
the diet was maintained. Earlier work (Allee, 1985)
had suggested that the effects of dietary fat can be
offset if the calorie:protein ratio is maintained. How-
ever, the extra-caloric and extra-metabolic effects of
dietary fat result in greater efficiency of digestion and
energy retention, which most likely account for the
increased carcass fat despite this adjustment.
When fat is included in the diet, there is an inhibi-
tion of de novo lipogenesis, and the fatty acids that
are deposited in adipose tissue switch from being of
endogenous origin to that characteristic of the exoge-
nous fat source. There are important species differ-
ences in the primary site of lipogenesis and in the
effect of exogenous fatty acids on the rate of lipogen-
esis. In rodents, lipogenesis occurs in both liver and
adipose tissue, whereas in pigs and ruminants it is
primarily in adipose tissue. The liver is the main site
of lipogenesis in the bird (Allee et al., 1971a,b, 1972;
Steffen et al., 1978; Donaldson, 1985).
The literature on the effects of the type of dietary
fat on lipogenesis is dominated by studies in rodent
liver tissue demonstrating the effects of the degree of
unsaturation on inhibition of fatty acid synthase (e.g.,
Clarke, 2001). In fact, the effects of degree of unsatu-
ration are specific to liver. There is no difference in
the degree of inhibition by saturated and unsaturated
fatty acids in rodent adipose tissue (Shillabeer et al.,
1990). This suggests that the promoter regions of fatty
acid synthase differ between tissues.
Lipogenic enzyme activity and overall lipogenesis
are low in the liver of pigs (Lee et al., 2000; Ding et
al., 2001; Gondret et al., 2001). There are reports from
three independent laboratories that inhibition of lipo-
genesis in adipose tissue of the pig is stronger with
saturated fat sources than with unsaturated sources
(Allee et al., 1972; Camara et al., 1996, Smith et al.,
1996). Dietary fat inhibits lipogenesis in ruminants
(Deeth and Christie, 1979; Emery, 1979; Page et al.,
1997), but it is not clear if there are differences in
potency for different degrees of unsaturation.
Several studies report that feeding polyunsaturated
fatty acids to chickens results in reduced abdominal
and total carcass fat as compared to that in birds
fed saturated fatty acid sources (Sanz et al., 1999a,b,
2000; Crespo and Esteve-Garcia, 2002a,b; Newman et
al., 2002). The calculated contribution of endogenous
synthesis of fat to depot fat indicated that there was
less endogenous contribution when birds were fed sat-
urated fat (Crespo and Esteve-Garcia, 2002b). This
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Azain
was unexpected given that other investigators re-
ported that, as with rodents, lipogenesis was inhibited
to a greater extent in chicken hepatocytes with unsat-
urated vs. saturated fatty acids (Lien et al., 2000; Sanz
et al., 2000.).
It seems that in species where the liver is the pri-
mary site of lipogenesis, unsaturated fatty acids are
more inhibitory than saturated ones. Such is the case
in rodents and poultry. In species where adipose tissue
is the primary site of lipogenesis, saturated fatty acids
are equivalent (or more potent) than unsaturated. The
regulation of hepatic expression of lipogenic enzymes
such as fatty acid synthase has been well character-
ized, but there has been little investigation of the regu-
lation of the gene in adipose tissue in rodents or other
species. In particular, there is a need to characterize
the potential differences in the promoter regions of
these genes in various tissues. Such a characterization
may help to explain species and depot differences in
the anti-lipogenic response to unsaturated fatty acids.
There are limited studies on the specific effects of
n-3 fatty acids on fat cell size in livestock or poultry.
In rats, there is evidence that animals fed fish oil have
reduced cell size and reduced fat pad weights (Belzung
et al., 1993; Su and Jones, 1993; Fickova et al., 2002).
This effect seems to be depot, gender, and strain de-
pendent, and there are no corresponding observations
in livestock. At least part of these effects may be ac-
counted for by the potent effects of fish oil fatty acids
on lipogenesis in the liver (Herzberg and Rogerson,
1988).
Effects of CLA on Cell Size
With reports of the antiobesity effects of CLA in
rodents, there was interest in the potential to use CLA
as a repartitioning agent in meat animals. In rats
fed CLA, the antiobesity effect is accounted for by
decreased lipid filling of adipocytes, and thus, de-
creased cell size (Azain et al., 2000). In livestock, the
effects of dietary CLA on body fat have been less than
that observed in rodents and have been inconsistent.
The effects dietary CLA in finishing pigs has recently
been reviewed (Azain, 2003). Two factors that appear
to account for the variation in carcass fat response to
dietary CLA are the level of fat in the diet and the
amount of carcass fat in the control group. Conjugated
linoleic acid decreases subcutaneous fat thickness
when there is little or no other fat added to the diet
and when the level of 10th-rib fat in the control group
is greater than 23 mm. The relevance of fat thickness
is confounded by gender, in that barrows are generally
fatter than gilts. There are a few specific studies with
appropriate controls that support this explanation for
the variation in response.
When CLA was added to diets with 2% added fat,
there was an 11% (P < 0.05) decrease in subcutaneous
fat thickness. However, at 5% added fat, there was no
significant CLA effect (Dugan et al, 2001). The gender
 Fatty acids and adipocytes
Table 1. Comparison of key aspects of adipose development and metabolism in rodents, pigs, and cattlea
Item Rodent
Fate of dietary fatty acids Absorbed without major
modification
PPAR expression in adipose tissueb
PPAR-α expressed in liver, but not
in adipose tissue
PPAR γ-1 in liver only
PPAR γ-2 highly expressed in
adipose tissue
Effect of exogenous fatty acids on lipogenesis
In liver Fatty acids inhibit lipogenesis and
unsaturated are more inhibitory than
saturated
In adipose tissue No effect of degree of unsaturation
on lipogenesis
a
See text for references.
b
PPAR = peroxisome proliferator activated receptor.
and fat thickness interaction is illustrated in another
study (Tischendorf et al., 2002). In barrows, the con-
trol group had 26 mm of 10th-rib fat thickness and
CLA reduced fat thickness 11% (P < 0.01). In this same
study (Tischendorf et al., 2002), however, there was
no effect of CLA in gilts that had 20 mm of fat. To
further illustrate this point, Averette-Gatlin et al.
(2002) examined the effects of CLA on barrows and
gilts with and without 4% added fat. They observed
no effect of CLA in any of the groups. The key here is
that both barrows and gilts had less than 15 mm of
fat, well below the proposed threshold of 23 mm. Thus,
studies in rodents suggesting that the effects of CLA
are independent of diet and background level of car-
cass fat (Park et al., 1997; DeLany et al., 1999) are
not necessarily applicable to other species. It would
appear that other than alterations in fatty acid profile,
which results in increased carcass or belly firmness,
there is not a consistent advantage to feeding CLA
to pigs.
Summary and Future Direction
Two aspects of the relationship between dietary fat
and adipose tissue have been reviewed: 1) the ability
to modify fatty acid profiles as a means to create val-
ued-added products with increased n-3 or CLA content
and 2) the ability of dietary fat to affect adipose cell
development. Although it is clearly possible to modify
fatty acid profile in nonruminant animals, the nega-
tive effects on carcass quality (in the case of n-3 fatty
acids) and the inefficiency associated with feeding the
desired oil to animals in order to increase human di-
etary intake raises issues about the practicality of
this approach.
Cell culture studies clearly demonstrate that fatty
acids can modify gene expression and affect adipose
development. In vivo studies are less clear. The lack
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921
Pig Cattle
Absorbed without major Majority biohydrogenated to
modification saturated forms
PPAR-α, γ-1, and γ-2 PPAR-α expression not
expressed in adipose tissue reported
PPAR γ-1 and γ-2 expressed
in adipose tissue
Not a major site of lipogenesis Not major site of lipogenesis
Fatty acids inhibit lipogenesis; Limited data, but several
several studies suggest that studies show that fatty acids
saturated fatty acids are more inhibit lipogenesis
inhibitory than unsaturated
of confirmation of in vitro results may be due to the
artificial environments used in cell culture studies or
to complexities of in vivo systems. Much of what is
known about fatty acid metabolism and effects on gene
regulation is based on information gathered in experi-
ments with laboratory animals and from cell lines in
culture. There are important species differences that
must be considered in applying this information to
livestock and poultry (Table 1). In many cases, species-
specific details for nonlaboratory animals are not
known. There is a need for investigation of the differ-
ences in the regulation of key enzymes and expression
of regulatory proteins such as PPAR. The emphasis
over the last few decades on reduction of the total
amount of adipose tissue needs to be refocused on
identification of factors that allow control over the
development of specific adipose depots, such as be-
tween subcutaneous and intramuscular sites.
Implications
Despite improvements in lean:fat ratio in meat ani-
mals, there is continued interest in defining ways to
regulate fat deposition. Dietary fat can substantially
alter the tissue fatty acid profile in nonruminants,
and to a lesser extent in ruminants, but there is little
evidence that adipose tissue development is changed.
There is a need for better understanding of species
differences in the regulation of adipose tissue gene ex-
pression.
Literature Cited
Ackman, R. G. 2000. Fatty acids in fish and shellfish. Pages 153–
174 in Fatty Acids in Foods and Their Health Implications.
2nd ed. C. K. Chow, ed. Marcel Dekker, Inc., New York.
Allee, G. L. 1985. The interaction of dietary protein and energy on
swine performance. Pages 136–141 in Proc. of the Georgia
Nutr. Conf. for the Feed Industry, Atlanta.
922
Allee, G. L., D. H. Baker, and G. A. Leveille. 1971a. Influence of
dietary protein and fat on lipogenesis and enzymatic activity
in pig adipose tissue. J. Nutr. 101:869–878.
Allee, G. L., D. H. Baker, and G. A. Leveille. 1971b. Influence of
level of dietary fat on adipose tissue lipogenesis and enzymatic
activity in the pig. J. Anim. Sci. 33:1248–1254.
Allee, G. L., D. R. Romsos, G. A. Leveille, and D. H. Baker. 1972.
Lipogenesis and enzymatic activity in pig adipose tissue as
influenced by source of dietary fat. J. Anim. Sci. 35:41–47.
Amri, E., G. Ailhaud, and P. A. Grimaldi. 1994. Fatty acids as
signaling molecules: Involvement in the differentiation of pre-
adipose to adipose cells. J. Lipid Res. 35:930–937.
Averette Gatlin, L., M. T. See, D. K. Larick, X. Lin, and J. Odle.
2002a. Conjugated linoleic acid in combination with supple-
mental dietary fat alters pork quality. J. Nutr. 132:3105–3112.
Averette Gatlin, L., M. T. See, J. A. Hansen, D. Sutton, and J. Odle.
2002b. The effects of dietary fat sources, levels, and feeding
intervals on pork fatty acid composition. J. Anim. Sci.
80:1606–1615.
Azain, M. J., D. B. Hausman, M. B. Sisk, W. P. Flatt, and D. E.
Jewell. 2000. Dietary conjugated linoleic acid reduces rat adi-
pose tissue cell size. J. Nutr. 130:1548–1554.
Belury, M. A. 2002. Dietary conjugated linoleic acid in health: Physi-
ological effects and mechanisms of action. Ann. Rev. Nutr. 22:
505–531.
Belury, M. A., S. Y. Moya-Camarenab, M. Lub, L. Shib, L. M. Lees-
nitzerc and S. G. Blanchard. 2002. Conjugated linoleic acid is
an activator and ligand for peroxisome proliferator-activated
receptor-gamma (PPAR-γ). Nutr. Res. 22:817–824.
Belzung, F., T. Raclot, and R. Groscolas. 1993. Fish oil n-3 fatty
acids selectively limit the hypertrophy of abdominal fat depots
in growing rats fed high-fat diets. Am. J. Physiol.
264:R1111– R1118.
Brodie, A. E., V. A. Manning, K. R. Ferguson, D. E. Jewell, and C.
Y. Hu. 1999. Conjugated linoleic acid inhibits differentiation
of pre- and post-confluent 3T3-L1 preadipocytes but inhibits
cell proliferation only in preconfluent cells. J. Nutr.
129:602–606.
Camara, M., J. Mourot, and C. Fevrier. 1996. Influence of two dairy
fats on lipid synthesis in the pig: Comparative study of liver,
muscle and the two backfat layers. Ann. Nutr. Metab.
40:287–295.
Chapkin, R. S. 2000. Reappraisal of the essential fatty acids. Pages
557–568 in Fatty Acids in Foods and Their Health Implications.
2nd ed. C. K. Chow, ed. Marcel Dekker, Inc., New York.
Chin, S. F., W. Lui, J. M. Storkson, Y. L. Ha, and M. W. Pariza.
1992. Dietary sources of conjugated diene isomers of linoleic
acid, a newly recognized class of anticarcinogens. J. Food Com-
pos. Anal. 5:185–197.
Clarke, S. D. 2001. Polyunsaturated fatty acid regulation of gene
transcription: A molecular mechanism to improve the meta-
bolic syndrome. J. Nutr. 131:1129–1132.
Cornelius, P., O. A. MacDougald, and M. D. Lane. 1994. Regulation
of adipocyte development. Annu. Rev. Nutr. 14:99–129.
Crespo, N., and E. Esteve-Garcia. 2002a. Dietary polyunsaturated
fatty acids decrease fat deposition in separable fat depots but
not in the remainder carcass. Poult. Sci. 81:512–518.
Crespo, N., and E. Esteve-Garcia. 2002b. Nutrient and fatty acid
deposition in broilers fed different dietary fatty acid profiles.
Poult. Sci. 81:1533–1542.
Deeth, H. C., and W. W. Christie. 1979. Biosynthesis of triacylglyc-
erols in ovine adipose tissue in vitro. Int. J. Biochem.
10:577–582.
DeLany, J. P., F. Blohm, A. A. Truett, J. A. Scimeca, and D. B.
West. 1999. Conjugated linoleic acid rapidly reduces body fat
content in mice without affecting energy intake. Am. J. Physiol.
276:R1172–R1179.
Ding, S.-T., A. Lapillonne, W. C. Heird, and H. J. Mersmann. 2003.
Dietary fat has minimal effects on fatty acid metabolism tran-
script concentrations in pigs. J. Anim. Sci. 81:423–431.
Downloaded from jas.fass.org by guest on July 24, 2011
Azain
Ding, S. T., R. L. McNeel, and H. J. Mersmann, 2000. Conjugated
linoleic acid increases the differentiation of porcine adipocytes
in vitro. Nutr. Res. 20:1569–1580.
Ding, S. T., and H. J. Mersmann. 2001a. Fatty acids modulate
porcine adipocyte differentiation and transcripts for transcrip-
tion factors and adipoycte-characteristic proteins. J. Nutr. Bio-
chem. 12:101–108.
Ding, S. T., A. P. Shinckel, T. E. Weber, and H. J. Mersmann. 2001b.
Expression of porcine transcription factors and genes related
to fatty acid metabolism in different tissues and genetic popula-
tions. J. Anim. Sci. 78:2127–2134.
Donaldson, W. E. 1985. Lipogenesis and body fat in chicks: Effects of
calorie-protein ratio and dietary fat. Poult. Sci. 64:1199–1204.
Duckett, S. K., D. G. Wagner, L. D. Yates, H. G. Dolezal, and S. G.
May. 1993. Effects of time on feed on beef nutrient composition.
J. Anim. Sci. 71:2079–2088.
Dugan, M. E. R., J. L. Aalus, K. A. Lien, A. L. Schaefer, and J. K.
G. Kramer. 1997. The effect of conjugated linoleic acid on fat
to lean repartitioning and feed conversion in pigs. Can. J. Anim.
Sci. 77:723–725.
Dugan, M. E. R., J. L. Aalus, K. A. Lien, A. L. Schaefer, and J. K. G.
Kramer. 2001. Effects of feeding different levels of conjugated
linoleic acid and total oil to pigs on live animal performance
and carcass composition. Can. J. Anim. Sci. 81:505–510.
Duplus, E., M. Glorian, and C. Forest. 2000. Fatty Acid Regulation
of Gene Transcription. J. Biol. Chem. 275:30749–30752.
Duplus, E., M. Glorian, and C. Forest. 2001. Fatty acid regulation
of gene expression in adipogenesis and adipocyte metabolism.
Pages 11–16 in New Avenues of Research in Fatty Acid Oxida-
tion and Ketone Body Metabolism. S. Eaton and P. A. Quant,
ed. FAOXK Press, London.
Eaton, S. B., S. B. Eaton, III, M. J. Konner, and M. Shostak. 1996. An
evolutionary perspective enhances understanding of human
nutritional requirements. J. Nutr. 126:1732–1740.
Eggert J. M., M. A. Belury, A. Kempa-Steczko, S. E. Mills, and A.
P. Schinkel. 2001. Effects of conjugated linoleic acid on the
belly firmness and fatty acid composition of genetically lean
pigs. J. Anim. Sci. 79:2866–2872.
Emery, R. S. 1979. Deposition, secretion, transport and oxidation
of fat in ruminants. J. Anim. Sci. 48:1530–1537.
Fickova, M., P. Hubert, G. Cremel, and C. Leray. 2002. Dietary (n-
3) and (n-6) polyunsaturated fatty acids rapidly modify fatty
acid composition and insulin effects in rat adipocytes. J. Nutr.
128:512–519.
Gondret, F., P. Fere, and I. Dugail. 2001. ADD-1/SREBP-1 is a
major determinant of tissue differential lipogenic capacity in
mammalian and avian species. J. Lipid Res. 42:106–113.
Gregoire, F. M., C. M. Smas, and H. S. Sul. 1998. Understanding
adipocyte differentiation Physiol. Rev. 78:783–809.
Ha, Y. L., N. K. Grimm, and M. W. Pariza. 1989. Newly recognized
anticarcinogenic fatty acids: identification and quantification
in natural and processed chesses. J. Agr. Food Chem. 37:75–81.
Hausman, G. J. 1985. The comparative anatomy of adipose tissue.
Pages 1–21 in New Perspectives in adipose tissue: Structure,
function and development. A. Cryer and R. L. R. Van, ed. But-
terworths Publishing, London, U.K.
Hertzel, A. V., and D. A. Bernlohr. 1998. Regulation of adipocyte
gene expression by polyunsaturated fatty acids. Mol. Cel. Bio-
chem. 188:33–39.
Herzberg, G. R., and M. Rogerson. 1988. Hepatic fatty acid synthesis
and triglyceride secretion in rats fed fructose- or glucose-based
diets containing corn oil, tallow or marine oil. J. Nutr.
118:1061–1067.
Houseknecht, K. L., C. A. Bidwell, C. P. Portocarrero, and M. E.
Spurlock. 1998. Expression and DNA cloning of porcine peroxi-
some proliferator-activated receptor gamma (PPARγ). Gene
225:89–96.
Ip, C., J. A. Scimeca, and H. J. Thompson. 1994. Conjugated linoleic
acid: A powerful anticarcinogen from animal sources. Cancer
74(Suppl.):1050–1054.
 Fatty acids and adipocytes
Irie, M., and M. Sakimoto. 1992. Fat characteristics of pigs fed fish
oil containing eicosapentaenoic and docosahjexaenoic acids. J.
Anim. Sci. 70:470–477.
Kliewer, S. A., S. S. Sundseth, S. A. Jones, P. J. Brown, G. B.
Wisely, C. S. Koble, P. Devchand, W. Wahli, T. M. Willson, J.
M. Lenhard, and J. M. Lehmann. 1997. Fatty acids and eicosa-
noids regulate gene expression through direct interactions
with peroxisome proliferator-activated receptors alpha and
gamma. Proc. Natl. Acad. Sci. USA 94:4318–4332.
Lee, K. N., M. W. Pariza and J. M. Ntambi. 1998. Conjugated linoleic
acid decreases hepatic stearoyl-CoA desaturase mRNA expres-
sion. Bioch. Biophys. Res. Commun. 248:817–821.
Lee, K. C., M. J. Azain, D. B. Hausman, and T. G. Ramsay. 2000.
Somatotropin and adipose tissue metabolism: Substrate and
temporal effects. J. Anim. Sci. 78:1236–1246.
Leskanich, C. O., K. R. Matthews, C. C. Warkup, R. C. Noble, and
M. Hazzledine. 1997. The effect of dietary oil containing (n-3)
fatty acids on the fatty acid, physiochemical, and organoleptic
characteristics of pig meat and fat. J. Anim. Sci. 75:673–683.
Lien, T. F., C. P. Wu, K. L. Chen, and K. H. Yang. 2000. Effects of
different fatty acids and levels on the lipogenic capacity and
lipolysis rate of broilers in vitro. Asian-Australas. J. Anim Sci.
13:1285–1289.
MacDougald, O. A., and M. D. Lane. 1995. Transcriptional regula-
tion of gene expression during adipocyte differentiation. Ann.
Rev. Biochem. 64:345–373.
McNeel, R. L., S. T. Ding, E. O’Brian Smith, and H. J. Mersmann.
2000. Expression of porcine adipocyte transcripts during differ-
entiation in vitro and in vivo. Comp. Biochem. Physiol. B
126:291–302.
Mourot, J., and D. Hermier. 2001. Lipids in monogastric animal
meat. Reprod. Nutr. Dev. 41:109–118.
Nettleton, J. A. 1991. 4-3 Fatty acids. Comparison of plant and
animal sources in human nutrition. J. Amer. Diatetic Assoc.
91:331–337.
Newman, R. E., W. L. Bryden, E. Fleck, J. R. Ashes, W. A. Buttemer,
L. H. Storlien, and J. A. Downing. 2002. Dietary n-3 and n-6
fatty acids alter avian metabolism: Metabolism and abdominal
fat deposition. Br. J. Nutr. 88:11–18.
NRC. 1987. Predicting feed intake of food-producing animals. Natl.
Acad. Press, Washington, DC.
Overland, M., O. Taugbol, A. Haug, and E. Sundstol. 1996. Effect
of fish-oil on growth performance, carcass characteristics, sen-
sory parameters, and fatty acid composition in pigs. Acta Agric.
Scand. 46:11–17.
Page, A. M., C. A. Sturdivant, D. K. Lunt, and S. B. Smith. 1997.
Dietary whole cottonseed depresses lipogenesis but has no ef-
fect on stearoyl coenzyme desaturease activity in bovine subcu-
taneous adipose tissue. Comp. Biochem. Physiol. B 118:79–84.
Pariza, M. W. 1997. Animal studies: Summary, gaps, and future
research. Am. J. Clin. Nutr. 66:1539–1540.
Pariza, M. W., Y. Park, and M. E Cook. 2001. The biologically active
isomers of conjugated linoleic acid. Prog. Lipid Res. 40:283–
298.
Park, Y., K. L. Albright, W. Liu, J. M. Storkson, M. E. Cook, and
M. W. Pariza. 1997. Effect of conjugated linoleic acid on body
composition in mice. Lipids 32:853–858.
Park, Y., J. M. Storkson, K. J. Albright, W. Liu, and M. W. Pariza.
1999. Evidence that the trans-10, cis-12 isomer of conjugated
linoleic acid induces body composition changes in mice. Lipids
34:235–241.
Pettigrew, J. E., and R. L. Moser. 1991. Fat in Swine Nutrition.
Pages 133–145 in Swine Nutrition. E. R. Miller, D. E. Ullrey,
and A. J. Lewis, ed. Butterworth-Heineman, Stoneham, MA.
Poulos, S. P., M. Azain, and G. J. Hausman. 2000. In utero dietary
conjugated linoleic acid alters body composition and growth
rate of newborn pigs. J. Anim. Sci. 78:(Suppl. 1)136.
Poulos, S. P., M. Sisk, D. B. Hausman, M. J. Azain, N. S. G. J.
Hausman. 2001. Pre- and post-natal dietary conjugated linoleic
acid (CLA) alters adipose tissue development, body weight gain
Downloaded from jas.fass.org by guest on July 24, 2011
923
and body composition in Sprague-Dawley rats. J. Nutr.
131:2722–2731.
Ramsay, T. G., C. M. Evock-Clover, N. C. Steele, and M. J. Azain.
2001 Dietary conjugated linoleic acid alters fatty acid composi-
tion of pig skeletal muscle and fat. J. Anim. Sci. 79:2152–2161.
Romans, J. R., R. C. Johnson, D. M. Wolf, G. W. Libal, and W. J.
Costello. 1995a. Effects of ground flaxseed in swine diets on
pig performance and on physical and sensory characteristics
and omega-3 fatty acid content of pork: I. Dietary level of
flaxseed. J. Anim. Sci. 73:1982.
Romans, J. R., D. M. Wolf, R. C. Johnson, G. W. Libal, and W. J.
Costello. 1995b. Effects of ground flaxseed in swine diets on
pig performance and on physical and sensory characteristics
and omega-3 fatty acid content of pork: II. Duration of 15%
dietary flaxseed. J. Anim. Sci. 73:1987.
Sanz, M. J. 2003. Conjugated linoleic acid and its effects on animal
products and health in monogastric animals. Proc. Nutr. Soc.
62:319–328.
Sanz, M., A. Flores, P., and C. J. Lopez-Bote. 1999a. Effect of fatty
acid saturation in broiler diets on abdominal fat and breast
muscle fatty acid composition and susceptibility to lipid oxida-
tion. Poult. Sci. 78: 378–382.
Sanz, M., A. Flores, P. Perez-de Ayala, and C. J. Lopez-Bote. 1999b.
Higher lipid accumulation in broilers fed on saturated fats
than in those fed on unsaturated fats. Br. Poult. Sci. 40:95–101.
Sanz, M., C. J. Lopez-Bote, D. Menoyo, and J. M. Bautista. 2000.
Abdominal fat deposition and fatty acid synthesis are lower
and -oxidation is higher in broiler chickens fed diets containing
unsaturated rather than saturated fat. J. Nutr. 130:3034–
3037.
Satory, D., and S. B. Smith. 1999. Conjugated linoleic acid inhibits
proliferation but stimulates lipid filling of murine 3T3-L1 pre-
adipocytes. J. Nutr. 129:92–97.
Schoonjans, K., J. Peinadoonsurbe, A. M. Lefebvre, R. A. Heyman,
M. Briggs, S. Deeb, B. Staels, and J. Auwerx. 1996a. PPAR-
alpha and PPAR-gamma activators direct a distinct tissue-
specific transcriptional response via a PPRE in the lipoprotein
lipase gene. EMBO J. 15:5336–5348.
Schoonjans, K., B. Staels, and J. Auwerx. 1996b. The peroxisome
proliferation activated receptors (PPARs) and their effects on
lipid metabolism and adipocyte differentiation. Biochim. Bio-
phys. Acta. 1302:93–109.
Scollan, N. D., M. S. Dhanoa, N. J. Choi, W. J. Maeng, M. Enser,
and J. D. Wood. 2001a. Biohydrogenation and digestion of long
chain fatty acids in steers fed on different sources of lipid. J.
Agric. Sci. 136:345–355.
Scollan, N. D., N. J. Choi, E. Kurt, A. V. Fisher, M. Enser, and J.
D. Wood. 2001b. Manipulating the fatty acid composition of
muscle and adipose tissue in beef cattle. Br. J. Nutr.
85:115–124.
Sessler A. M., and J. M. Ntambi. 1998. Polyunsaturated fatty acid
regulation of gene expression. J. Nutr. 128:923–926.
Shao, D., and M. A. Lazar. 1997. Peroxisome proliferation activated
receptor, CCAAT/enhancer-binding protein, and cell cycle sta-
tus regulate the commitment to adipocyte differentiation. J.
Biol. Chem. 272:21473–21478.
Shillabeer, G., J. Hornford, J. M. Forden, N. C. W. Wong, and D.
C. Lau. 1990. Hepatic and adipose tissue lipogenic enzyme
mRNA levels are suppressed by high fat diets in the rat. J.
Lipid Res. 31:623–631.
Smith, D. R., D. A. Knabe, and S. B. Smith. 1996. Depression of
lipogenesis in swine adipose tissue by specific dietary fatty
acids. J. Anim. Sci. 74:975.
Spurlock, M. E., C. A. Bidwell, K. L. Houseknecht, J. L. Kuske, C.
Camacho-Rea, G. R. Frank, and G. M. Willis. 2002. Nutri-
tionally induced adipose hypertrophy in young pigs is transient
and independent of changes in the expression of the obese
and peroxisome proliferation activated receptor genes. J. Nutr.
Biochem. 13:112–120.
Spurlock, M. E., K. L. Houseknecht, C. P. Portocarrero, S. G. Corne-
lius, G. M. Willis, and C. A. Bidwell. 2000. Regulation of PPARγ
924
but not obese gene expression by dietary fat supplementation.
J. Nutr. Biochem. 11:260–266.
Steffen, D. G., E. Y. Chai, L. L. Brown, and H. J. Mersmann. 1978.
Effects of diet on swine glyceride lipid metabolism. J. Nutr.
108:911–918.
Su, W., and P. J. H. Jones. 1993. Dietary fatty acid composition
influences energy accretion in rats. J. Nutr. 123:2109–2114.
Sundvold, H., A. Brzozowska, and S. Lien. 1997. Characterisation
of bovine peroxisome proliferator-activated receptors γ1 and
γ2: Genetic mapping and differential expression of the two
isoforms. Biochem. Biophys. Res. Commun. 239:857–861.
Thuillier, P., R. Bailliea, X. Shaa, and S. D. Clarke. 1998. Cytosolic
and nuclear distribution of PPAR2 in differentiating 3T3-L1
preadipocytes. J. Lipid Res. 39:2329–2338.
Tischendorf, F., F. Schone, U. Kirchheim, and G. Jarhreis. 2002.
Influence of a conjugated linoleic acid mixture on growth, organ
weights, carcass traits and meat quality in growing pigs. J.
Anim. Physiol. Anim. Nutr. 86:117–128.
Tontonoz, P., E. Hu, R. A. Graves, A. I. Budavari, and B. M. Spiegel-
man. 1994. mPPAR gamma 2: tissue-specific regulator of an
adipocyte enhancer. Genes Devel. 8:1224–1234.
Torii, S. I., T. Kawada, K. Matsuda, T. Matsui, T. Ishihara, and H.
Yano. 1998. Thiazolidinedione induces the adipose differentia-
tion of fibroblast-like cells resident within bovine skeletal mus-
cle. Cell Biol. Int. 22:421–427.
Ulbricht, T. L. V., and D. A. T. Southgate. 1991. Coronary heart
disease: Seven dietary factors. Lancet 338:985–992.
Van, R. L. R. 1985. The adipocyte precursor cell. Pages 353–382 in
New Perspectives in Adipose Tissue: Structure, Function and
Downloaded from jas.fass.org by guest on July 24, 2011
Azain
Development. A. Cryer and R. L. R. Van, ed. Butterworths
Publishing, London, U. K.
Van Oeckel, M. J., M. Casteels, N. Warnants, L. Van Damme, and
Ch. V. Boucque. 1996. Omega-3 fatty acids in pig nutrition:
Implications for the intrinsic and sensory quality of the meat.
Meat Sci. 44:55–63.
Wiegand, B. R., J. C. Sparks, F. C. Parrish, and D. R. Zimmerman.
2002. Duration of feeding conjugated linoleic acid influences
growth performance, carcass traits, and meat quality of finish-
ing barrows. J. Anim. Sci. 80:637–643.
Winters, B. L., S. M. Yeh, and Y. Y. Yeh. 1994. Linoleic acid provides
a source of docosahexaenoic acid for artificially reared rat pups.
J. Nutr. 124:1654–1659.
Wolfrum, C., C. M. Borrmann, T. Borchers, and F. Spener. 2001.
Fatty acids and hypolipidemic drugs regulate peroxisome pro-
liferator-activated receptors α- and γ-mediated gene expres-
sion via liver fatty acid binding protein: A signaling path to
the nucleus. Proc. Natl. Acad. Sci. USA 98:2323–2328.
Wood, J. D., and M. Enser. 1997. Factors influencing fatty acids in
meat and the role of antioxidants in improving meat quality.
Br. J. Nutr. 78:s49–s60.
Wright, H. M., C. B. Clish, T. Mikami, S. Hauser, K. Yanagi, R.
Hiramatsu, C. N. Serhan, and B. M. Spiegelman. 2000. A syn-
thetic antagonist for the peroxisome proliferator-activated re-
ceptor gamma inhibits adipocyte differentiation. J. Biol. Chem.
275:1873–1877.
Zollitsch, W., W. Kraus, F. Aichinger, and F. Lettner. 1997. Effects
of different dietary fat sources on performance and carcass
characteristics of broilers. Anim. Feed Sci. Technol. 66:63–73.
References This article cites 75 articles, 35 of which you can access for free at:
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