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Department of Animal Science and Center for Animal Biotechnology, Institute of Bioscience and Technology, Texas A&M University, College Station, TX 77843–2471
2To 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: • amino acids • fetus • pregnancy • pigs
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). They serve as
essential precursors for syntheses of proteins and other biologically
important substances such as peptides, hormones, neurotransmitters,
purine and pyrimidine nucleotides, creatine, carnitine, porphyrins,
polyamines and nitric oxide (Reeds and Hutchens 1994
,
Wu and Morris 1998
). Amino acid malnutrition not only
retards fetal growth and development (Pond 1973
,
Pond et al. 1969
), but also permanently alters the
structure and function of key organs postnatally (Desai et al. 1996
, Ozanne 1997
). Epidemiologic
studies indicate that fetal nutrition may be an important factor
contributing to diseases such as diabetes, hypertension and coronary
heart disease later in life (Barker 1998
). Thus,
understanding fetal amino acid nutrition and metabolism is of enormous
importance for optimizing growth and health of the fetus, neonate and
adult. However, little is known about this aspect of fetal nutrition
(Hay 1998
). To date, only a few studies have determined
amino acid concentrations and accretion in fetuses of the guinea pig
(Sparks et al. 1985
), sheep (Meier et al. 1981
), rat (Southgate 1971
), and human
(Widdowson et al. 1979
). In these studies, not all amino
acids were quantified. Although the pig has been proposed as an animal
model for studying amino acid nutrition and metabolism in the human
preterm neonate and infant (Ball et al. 1996
), there is
no published information regarding amino acid composition or accretion
in the fetal pig.
As part of our long-term goal of quantifying fetal amino acid
metabolism, we reported amino acid concentrations in plasma, allantoic
and amniotic fluids of fetal pigs (Wu et al. 1995 and 1996
) and in porcine placenta and endometrium (Wu et al. 1998a
), and their alterations during maternal protein
malnutrition (Wu et al. 1998a and 1998b
). To further
characterize the fetal pig model, it is important that amino acid
composition of the fetus be quantified. Such information provides a
critical data base for future studies of amino acid metabolism in the
fetal pig, defining fetal amino acid requirements, and elucidating
mechanisms responsible for intrauterine growth retardation and
life-threatening derangements of nitrogen metabolism in preterm
neonates.
The objective of this study was to determine amino acid composition and accretion in fetal pigs at various gestational ages. Our results demonstrated the following: 1) amino acid nitrogen represented 83–88% of total nitrogen, and arginine was the most abundant nitrogen carrier in the fetal pig; 2) amino acid composition in the fetal pig was similar to that for the human fetus and changed with gestation, particularly for glycine and hydroxyproline; and 3) uterine uptake of arginine and proline plus hydroxyproline met requirements for fetal amino acid accretion only marginally during late gestation.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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HPLC-grade methanol and water were purchased from Fisher Scientific (Fair Lawn, NJ). Amino acid standards and other chemicals were obtained from Sigma Chemical (St. Louis, MO).
Pigs.
Pigs were F1 crosses of Yorkshire x Landrace sows and Duroc
x Hampshire boars, and were maintained at Texas A&M University's
Veterinary Research Park. Gilts were mated when detected in estrus and
12 and 24 h later, and were assigned randomly to be
hysterectomized on d 40, 60, 90, 110 or 114 of gestation. Pregnant
gilts had free access to water and a sorghum-soybean meal–based
diet that met NRC requirements (Wu et al. 1995
). Dietary
contents of metabolizable energy, protein and lysine were 13240 kJ/kg,
13.9% and 0.61%, respectively. On the assigned day of gestation,
gilts were hysterectomized as previously described (Wu et al. 1996
). Briefly, pigs received intramuscular administration of
Telazol (2.2 mg/kg body weight) to induce anesthesia, which was
maintained throughout surgery with halothane (1–5%) and oxygen via a
snout mask and a closed circuit anesthesia machine. A mid-ventral
laparotomy was performed, and the reproductive tract was exposed.
Uterine arterial and venous blood samples (3 mL) were withdrawn into
heparinized tubes. Then the uterine vessels of each uterine horn, the
ovarian pedicle and the cervix were ligated with umbilical tape. Two
fetal pigs were obtained from each gilt, weighed and stored at
-80°C. This study was approved by Texas A&M
University's Institutional Animal Care and Use Committee.
Analyses of chemical composition in fetal pigs.
The whole fetal pig was ground in a meat grinder and then homogenized
by using a standard laboratory size blender. A portion of the
homogenate (3 g) was used for determining the content of water, dry
matter, ash (minerals) and lipids with the use of standard methods
(AOAC 1980
). A portion of the homogenate (1 g) was used
for analysis of total nitrogen content with the Kjeldahl procedure
(AOAC 1980
). For measuring amino acids (except
tryptophan), 0.5 g of the homogenate was hydrolyzed in 100 mL of 6
mol/L HCl at 110°C for 24 h under N2, and amino
acids in hydrolysates were measured by HPLC as previously described
(Wu et al. 1995
). For tryptophan analysis by HPLC,
0.5 g of the homogenate was hydrolyzed at 110°C for 20 h in
10 mL of 4.2 mol/L NaOH plus 0.1 mL of thiodiglycol (an antioxidant,
25% aqueous solution), as previously described (Wu et al. 1997
). Because acid hydrolysis converts glutamine and
asparagine to glutamate and aspartate, respectively, nitrogen content
of glutamine, glutamate, asparagine and aspartate in fetal homogenates
was estimated on the basis of frequency of occurrence of their residues
(4.0, 6.2, 4.4 and 5.3%, respectively) in primary structures of 1021
unrelated proteins of known sequence (Creighton 1993
,
McCaldon and Argos 1988
). These ratios of
glutamine/glutamate (0.645:1) and asparagine/aspartate (0.830:1) are
similar to those in major muscle proteins of known sequence (e.g.,
0.650:1 for glutamine/glutamate and 0.782:1 for asparagine/aspartate)
in cardiac, skeletal and smooth muscle myosin heavy chain
(Matsuoka et al. 1991
).
Plasma amino acid analysis.
Blood samples were centrifuged for 15 min at 3000 x g and 4°C.
Plasma (1 mL) was acidified with 1 mL of 1.5 mol/L HClO4
and then neutralized with 0.5 mL of 2 mol/L
K2CO3. The supernatant was used for amino acid
analysis by HPLC as previously described (Wu et al. 1995 and 1997
). Uterine arteriovenous (A-V) differences in
concentrations of amino acids were used to estimate uterine uptake of
amino acids on the basis of uterine blood flow [243 mL/(min ·
fetus)] (Ford et al. 1984
) and hematocrit (0.32)
(Caton and Bazer 1978
) in pregnant swine at d 110–114
of gestation; that is, uterine amino acid uptake = A-V
concentration difference x blood flow x (1 - hematocrit) (Ford et al. 1984
). We used the average
value of uterine blood flow in pregnant pigs reported by Ford et al. (1984)
on the basis of the following considerations. First,
Ford and colleagues studied uterine blood flow in pregnant pigs
extensively, and their published values of uterine blood flow are
consistent with those reported for pregnant pigs by other investigators
(Hanka et al. 1975
, Hard and Anderson, 1982
). Second, pregnant pigs used in the study of Ford et al. (1984)
and in our studies had similar reproductive
performance on the basis of litter size, number of live piglets born
and average weights of live piglets born.
Statistical analysis.
Data on gross chemical composition and on amino acid composition and
accretion in fetal pigs were analyzed by one-way ANOVA, with the
gilt as the experimental unit and fetuses nested within gilt
(Steel and Torrie 1980
). Differences between means were
determined by the Student-Newman-Keuls multiple comparison test. Data
on amino acid nitrogen were also analyzed by polynomial regression
analysis, with the gilt as the experimental unit and fetuses nested
within gilt (Steel and Torrie 1980
). Data on uterine
arteriovenous amino acid concentrations were analyzed by paired
t test. Statistical analysis was performed by using the
general linear models (GLM) procedures of the SAS program (SAS
1990
). Probability values < 0.05 were taken to indicate
significant difference.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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During the periods of d 40 to 60, d 60 to 90, d 90 to 110 and d 110 to
114 of gestation, growth rates of the fetal pig averaged 6.0, 15.2,
27.6 and 85.8 g/d, respectively (Table 1). The absolute growth rate of the fetal pig was greatest during
the last 4 d of gestation. The concentration of water in the fetal
pig decreased (P < 0.05), but that of dry matter
increased (P < 0.05), from d 60 to 114 of gestation.
Mineral concentration in the fetal pig increased (P < 0.05) with increasing gestation from d 40 to 90 and then leveled off
throughout the remainder of pregnancy. Lipid concentration in the fetal
pig peaked at d 60–90 of gestation and declined (P < 0.05) thereafter. Nitrogen (crude protein) concentration in the fetal
pig decreased (P < 0.05) at d 60 compared with d 40 of
gestation, and then increased (P < 0.05) progressively
with advancing gestation.
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From d 40 to 114 of gestation, glycine, hydroxyproline and citrulline
increased (P < 0.05) progressively, and
aspartate/asparagine decreased (P < 0.05)
progressively (Table 2). Contribution of branched-chain amino acids (leucine,
isoleucine and valine), lysine, methionine, phenylalanine, threonine
and tyrosine to amino acid composition decreased progressively
(P < 0.05) from d 40 to 110 of gestation and then
leveled off. Changes in composition of other amino acids are summarized
as follows: 1) arginine increased progressively
(P < 0.05) from d 40 to 90 of gestation and then
leveled off; 2) alanine increased progressively
(P < 0.05) from d 40 to 110 of gestation;
3) glutamate/glutamine and 
-aminobutyric acid increased
(P < 0.05) at d 60 compared with d 40 of gestation and
decreased (P < 0.05) thereafter; 4)
cysteine and proline increased (P < 0.05) but
histidine decreased (P < 0.05) at d 60 compared with d
40 of gestation and remained constant thereafter; 5)
tryptophan and ornithine remained relatively constant throughout
gestation; and 6) taurine did not change between d 40 and 60
of gestation but decreased (P < 0.05) thereafter.
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Proline and hydroxyproline were the only amino acids whose
concentrations increased progressively in fetal pigs (P
< 0.05) with increasing gestational age from d 40 to 114
(Table 3). Concentrations of glycine, citrulline, ornithine and
-aminobutyric acid did not differ (P > 0.05)
between d 40 and 60 of gestation, but concentrations of other amino
acids decreased (P < 0.05) at d 60 compared with d 40
of gestation. Concentrations of all amino acids in fetal pigs increased
(P < 0.05) progressively from d 60 to 114 of
gestation. Arginine was the most abundant nitrogen carrier in fetal
pigs at all gestational ages studied, followed by glycine,
glutamate/glutamine, aspartate/asparagine, lysine, alanine and proline
in decreasing order at d 90–114 of gestation (Fig. 1
). Amino acid nitrogen concentrations in fetal pigs also increased
(P < 0.05) progressively from d 60 to 114 of
gestation. Rates of fetal amino acid accretion increased rapidly with
advancing gestation (Table 4). Fetal accretion rate for glutamate/glutamine was greatest,
followed by glycine, proline plus hydroxyproline, aspartate/asparagine,
leucine, arginine, alanine and lysine in decreasing order.
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All amino acids, except -aminobutyric acid, were taken up by the
uterus of pregnant gilts at all gestational ages studied, and results
for d 110–114 of gestation are summarized in Table 5. Uterine arterial and venous concentrations of -aminobutyric
acid were negligible (<0.1 µmol/L). Uterine uptake of
glutamine was greatest, followed by glycine, proline, leucine, alanine,
lysine and arginine, in decreasing order. Uterine uptake of
aspartate/asparagine and glutamate represented only 9–29% of fetal
accretion, and uterine uptake of arginine and proline plus
hydroxyproline met requirements for fetal accretion during late
gestation only marginally. Uterine uptake of other 
-amino acids
appeared to exceed their requirements for fetal accretion by 16–70%.
Uterine uptake of taurine, ornithine and citrulline was 3-, 15- and
55-fold greater than fetal accretion, respectively.
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Fetal amino acid compositions in the five species studied [pig (Table 2)
, human (Widdowson et al. 1979
), sheep (Meier et al. 1981
), guinea pig (Sparks et al. 1985
)
and rat (Southgate 1971
)] are summarized in Table 6. Amino acid compositions are similar between the fetal pig and the
human fetus or fetal lamb. However, amino acid compositions differ
appreciably among species that have relatively short periods of
gestation [guinea pig (67 d) and rat (21 d)] and species that have
relatively long periods of gestation [pig (114 d), human (280 d) or
sheep (145 d)] for the following amino acids: histidine, glycine,
lysine, proline and hydroxyproline.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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), guinea pig (Sparks et al. 1985
),
sheep (Meier et al. 1981
) and rat (Southgate 1971
) have been studied. However, not all amino acids were
measured in these investigations. For example, citrulline, the
precursor of arginine (Wu and Morris 1998
), was not
determined in fetuses of the above mammals, and fetal composition of
ornithine (the precursor of polyamines, proline and
glutamate/glutamine) was reported only for sheep (Meier et al. 1981
). Similarly, fetal taurine, a ß-amino acid critical for
neurological and cardiovascular development (Sturman 1993
), was analyzed only for the guinea pig (Sparks et al. 1985
) and sheep (Meier et al. 1981
). Fetal
-aminobutyric acid (a neurotransmitter) and tryptophan were reported
only for the rat (Southgate 1971
). This study provides
the first detailed description of developmental changes in amino acid
composition and accretion in the fetal pig.
Concentrations of dry matter and nitrogen in fetal pigs increased, but
water decreased, with increasing gestational age from d 60 to 114
(Table 1)
. This result is consistent with the change in gross chemical
composition of fetal pigs (Pond and Maner 1984
). Similar
gestational age–dependent changes in these parameters were
demonstrated for the fetal lamb (Meier et al. 1981
),
fetal guinea pig (Sparks et al. 1985
) and fetal rat
(Southgate 1971
). Although dry matter content of fetal
pigs did not change between d 40 and 60 of gestation, concentrations of
total nitrogen decreased and those of lipids and minerals increased at
d 60 compared with d 40 of gestation (Table 1)
. These results suggest
preferential accretion of lipids and minerals at the expense of
nitrogen during early gestation. Thus, lipid concentrations peaked at d
60–90 of gestation, preceding the period of most rapid growth of the
fetus. Interestingly, during the last 2 wk of gestation, lipid content
decreased markedly, but protein (nitrogen) increased in fetal pigs
(Table 1)
. This is in contrast to the fetal guinea pig in which lipid
content increases much more rapidly than non-lipid dry matter
during late gestation, accounting for 11.7% of wet weight at term
(Sparks et al. 1985
). Thus, energy utilization by fetal
pigs is preferentially directed to protein accretion rather than to
lipid deposition near parturition. This likely results from alterations
in regulatory hormones and substrate delivery from maternal to fetal
blood. As a result, lipid stores are limited in term newborn pigs, in
contrast to many other species (Widdowson 1950
).
Throughout gestation, crude protein was the major component of dry
matter in the fetal pig, representing 62, 53, 50, 53 and 57% at d 40,
60, 90, 110 and 114 of gestation, respectively. Accordingly, in fetal
pigs, amino acid nitrogen represented approximately 88, 87, 83, 84, and
83% of total nitrogen at d 40, 60, 90, 110 and 114 of gestation,
respectively (Table 1)
. These values of amino acid nitrogen are
comparable to those (80–82%) for fetal lambs and fetal guinea pigs
(Meier et al. 1981
, Sparks et al. 1985
)
(some amino acids were not measured in these previous studies). Thus,
ammonia, urea, purines, pyrimidines, porphyrins,
nitrogen-containing hormones and other amino acid metabolites
contribute to the sizable amount of non-amino acid nitrogen
(12–17% of total nitrogen) in fetal pigs.
Amino acid composition in fetal pigs changed with gestation (Table 2)
.
The contribution of glycine (+83%) and hydroxyproline (+333%) to
amino acid composition in fetal pigs increased markedly with gestation,
as reported for the fetal lamb (Meier et al. 1981
). This
is consistent with increased amounts of connective tissue and,
therefore, collagen in the fetus with advancing gestation
(Widdowson 1968
). Because there are ~9.1
hydroxyproline residues per 100 amino acid residues in collagen (or
10.8% by weight) (Devlin 1992
), collagen was estimated
to represent ~7, 15, 25, 28 and 29% of total body protein at d 40,
60, 90, 110 and 114 of gestation, respectively. The contribution of
other amino acids (except ornithine and tryptophan) to amino acid
composition in fetal pigs varies with gestation, indicating changes in
amounts and types of body proteins. It is noteworthy that the averaged
amino acid composition is similar between fetal pigs (Table 2)
and
postnatal pigs (8.5–145 kg) (Mahan and Shields 1998
),
except that the contributions of arginine (+8%), proline (+28%) and
serine (+18%) were greater, but the contributions of histidine
(-39%), isoleucine (-11%), and lysine (-7%) were lower in fetal
pigs than in postnatal pigs.
An important finding from this study is that arginine was the most
abundant nitrogen carrier in fetal pigs at all gestational ages
studied, followed by glycine, glutamate/glutamine and
aspartate/asparagine at d 90–114 of gestation (Fig. 1)
. Such an
abundance of arginine nitrogen in the fetus often goes unrecognized,
but it reflects the important role of arginine in fetal nutrition and
metabolism (Vosatka et al. 1998
), as well as in the
survival and growth of neonates, particularly preterm infants
(Batshaw et al. 1984
, Snyderman et al. 1970
). It should be noted that arginine is the most abundant
nitrogen carrier, in part because this amino acid contains four
nitrogen atoms per molecule. On the basis of mmol amino acid/g fetal
weight, glycine is the most abundant amino acid in the pig fetus at d
40–114 of gestation (Table 3)
. Interestingly, arginine is the most
abundant free amino acid in porcine allantoic fluid at d 35–60 of
gestation; together with ornithine, it accounts for 40–55% of total
-amino acid nitrogen (Wu et al. 1996
). The abundance
of glycine in fetal pigs is consistent with its role in intrafetal
synthesis of nucleotides (Boza et al. 1995
) and collagen
(accounting for approximately one third of its amino acid residues)
(Devlin 1992
). In addition to serving as an essential
substrate for nucleotide synthesis, glutamine plays an important role
in interorgan metabolism of carbon and nitrogen in the fetus
(Vaughn et al. 1995
), as in postnatal animals
(Curthoys and Watford 1995
).
Rates of amino acid accretion in the fetal pig, which represent minimal
requirements of amino acids by the fetus, increased rapidly with
gestation (Table 4)
and were consistent with fetal growth (Table 1)
.
Because the rate of uterine blood flow does not change between d 60 and
114 of gestation in swine (Ford et al. 1984
, Hard and Anderson 1982
), uterine and placental transport of amino
acids must increase with gestation in the pig, as in the rat
(Matthews et al. 1998
). Sheep is the only species in
which umbilical uptake of amino acids and amino acid accretion in the
fetus have been estimated (Lemons et al. 1976
). In
general, amino acids are delivered to the ovine fetus in amounts
exceeding fetal amino acid accretion by 20–35% during late gestation
(Meier et al. 1981
). On the basis of uterine
arterio-venous differences in plasma amino acid concentrations
(Table 5)
and uterine blood flow (Ford et al. 1984
) in
pregnant swine, we estimated uterine uptake of individual amino acids
and compared it with amino acid accretion in fetal pigs. Uterine uptake
of amino acids reflects amino acid utilization (oxidation, conversion
to nitrogenous compounds and protein synthesis) by both the fetus and
placenta. In pigs, there is little or no placental growth after d 70 of
gestation (Knight et al. 1977
). Thus, porcine uterine
uptake of amino acids at d 110–114 of gestation reflects largely amino
acid utilization by the fetus for metabolism and protein accretion, as
well as by placenta for both oxidation and synthesis of non-protein
nitrogenous substances.
Our results indicate that uterine uptake of arginine and proline plus
hydroxyproline met requirements for fetal accretion during late
gestation only marginally (Table 5)
. When arginine catabolism to
creatine, ornithine, proline, polyamines, glutamate, agmatine and NO
(Wu and Morris 1998
) by the fetus and placenta is taken
into consideration, it is likely that uterine uptake of arginine is not
sufficient to meet the requirement for fetal growth. Thus, it can be
surmised that large amounts of arginine are synthesized by the fetus
during the perinatal period, as previously reported for newborn pigs
(Wu and Knabe 1995
). However, an important role for
intrafetal arginine synthesis in providing endogenous arginine for
fetal growth has not previously been recognized. Interestingly,
citrulline taken up by the pregnant uterus of swine was 55-fold greater
than fetal accretion (Table 5)
and was likely the major precursor for
intrafetal synthesis of arginine via argininosuccinate synthase and
lyase (Wu and Morris 1998
). The latter enzymes were
found to be widespread in the conceptus of the fetal pig, including
placenta, endometrium, allantoic and amniotic membranes, the small
intestine, liver and kidney during late gestation (Wu, G., unpublished
data). Similarly, -aminobutyric acid, aspartate/asparagine and
glutamate must be synthesized by the fetus because uterine uptake of
these amino acids appeared inadequate for fetal accretion during late
gestation. Glutamine and branched-chain amino acids, whose uterine
uptake was the most predominant (Table 6)
, are likely the major
precursors for intrafetal synthesis of aspartate/asparagine and
glutamate (the precursor of -aminobutyric acid). The small intestine
and skeletal muscle may be major organs for catabolizing glutamine
(Shenoy et al. 1996
) and branched-chain amino acids
(Goodwin et al. 1987
) in the fetus, respectively, as in
postnatal mammals. Our finding that ornithine taken up by the pregnant
uterus of swine was 15-fold greater than fetal accretion suggests that
ornithine is actively metabolized by the fetus, and its products likely
include polyamines, proline and glutamate (Wu and Morris 1998
).
Comparison of available data indicates that fetal amino acid
composition is similar among all of the species studied, with the
exception of glycine, histidine, lysine, proline, cysteine, taurine and
hydroxyproline in the fetal guinea pig and fetal rat (Table 6)
, both of
which exhibit relatively short periods of gestation (Table 6)
. Our
results indicate that amino acid compositions are similar among the
fetal pig, human fetus and fetal lamb, species having relatively long
periods of gestation. Because digestion and metabolism of protein and
nitrogen are similar between the pig and human (Miller and Ullrey 1987
), our findings support the proposition that the pig
is an excellent model for studying amino acid nutrition and metabolism
in the human preterm neonate and infant (Ball et al. 1996
, Borun 1993
).
In conclusion, total nitrogen and amino acid accretion in the fetal pig increased more rapidly with advancing gestation than non-nitrogen dry matter, and amino acid nitrogen represented 83–88% of total nitrogen. Arginine was the most abundant nitrogen carrier in fetal pigs at all gestational ages studied. Uterine uptake of arginine and proline plus hydroxyproline met requirements for fetal growth during late gestation only marginally, and uterine uptake of aspartate/asparagine and glutamate was only 9–29% of fetal accretion. Amino acid composition changed with gestation, with glycine and hydroxyproline increasing markedly and other amino acids (except ornithine and tryptophan) decreasing to a much lesser extent. The similarity in amino acid composition between the fetal pig and the human fetus indicates that the pig is an excellent model for studying amino acid nutrition and metabolism in the preterm neonate and infant.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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3 Current address: Animal and Veterinary Science
Department and Center for Reproductive Biology, Agricultural Sciences
Building, University of Idaho, Moscow, ID 83844–2330.
Manuscript received September 24, 1998. Initial review completed November 27, 1998. Revision accepted February 1, 1999.
|
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